Bullock, T.H., Orkand, R., and Grinnell, A. (1977) Introduction
to Nervous Systems. W. H. Freeman &Co. San Francisco. Chapter 7
Integration at the Intermediate Levels. pp. 242-290.
to the afferent centers a coded Form of
the sense organs' selection, or fil trate, of
the act ual sti muli. The aHerent netWe are concerned in this chapter with works-meani ng the interconnected
the transactions that occur in organized second-, th ird- and higher-order neurons
subsystems of receptors, neurons, and that receive thei r input primarily fro m
effectors. T heir mechan isms wi ll be cen- the receptors, though also from ot he r
tral to the issues of how the nervoussysttm sources-do not merely pass on this
works as it communications machine information. They use convergence
that recognizes, decides, and commands. of separa te cha nnels (comparison),
Of Ihe va rious domai ns of ope rations divergence of each channel (pa rallel
thai are ava ilable for our scrutiny. we processing), later.ll inh ibi tion (enhancing
include here fi ve, and these form the contrast), and other processes to modify
the signal. Special Attribu tes of the
headings of sections II to VI.
T his is the rirsl encQunte r, between original input a re passed on (recognithese covers, w it h the phys iology of tion), a nd much in form.l lion is disuseful arrays of neurons. It wil l help to carded . The structure and coupling
introduce two dassrs of function that Functions of the network determine what
e merge from a nd pervddc the activities gets through .
Compara ble networks exist on the
of such arrays.
Each pari of th e nervous system-but out put side. They are also fil te rs, but
especia lly the receiv ing s ide, fr om Ihe since they Formulate and send to the
battery of receptors to the networks of eHectors comma nds thill are crucia lly
higher-order neurons of the aHerent patterned in sp.1Ce a nd ti me, they are
systems-ca n be thought of as a filter . oft en thought of as palle rn genera tors.
The sense organs send a pa tt erned T hey convert triggeri ng inpu t or steering
stre.1m of impulses, in space a nd t ime, to input from receptors or their own sponthe affe rent centers, and these represent taneous discharge or a mixture of these
I. INTRODUCTION, DO MA INS IN
THE INTERMEDIATE LEVElS
242
Chapter 7
Integrdlion at the iniermediat(' Levels
Figure 7.1
Rf(rrlilm(ll/ ill /I muscle
IIlru molor III1i/S.
wilh
Silent mOlor
second means is to vary the frequency of
impulses in each unit, since either the
nels. Again the connectivity and dynamic aver,'ge tension in a series of twitches or
properties of the network determine its the teta nic tension is a function of fre outpul, but not merely by passive filter - quency. You can observe frequency and
ing. Often there are intrinsic rhythms of recruitment;control phenomena by placspontaneous impulse bursts, and these ing a stethoscope over your eyelid and
result in the generation of specified con- listen ing to the twitches of its muscle
stellations and sequences of activity in while you control them willfully. Repopulations of units and finally in the cruitment may be important in verteeffectors. Let us look first at the final brate skeletal muscle only at low tensions.
link.
Since there are many motor units in
most vertebrate skeletal muscles, operating these unit s out of phase with each
II. NERVOUS CONTROL IN
other
can give a smooth overall contracEFFECTORS: DIVERSITY OF
tion
even
when the frequency in each is
PERIPHERAL INTEGRATION
so low that it contracts in a series of
The best known vertebrate skeletal twitches. Another possible utility of
muscles consist of muscle fibers whose having many units is that there could be
cell membrane is capable of producing a rotation of activity during low or
propagated all-or-none impulses like medium work loads, sa..that units could
those of nerve fibers. Each muscle fiber is rest. But this old notion is apparently not
innervated, in general, by only one axon confirmed in the best studied materials.
Other muscle fibers in vertebrates arel
with one terminal at the speci"lized
end-plate. A motor nerve impulse arriv- incapable of producing propagated
ing there gives rise to an end-plate or Mtion potentials. They are innervated
junctional potential, like an e.p.s.p., not by a single end-plate, but by numerwhich is usually suprathreshold for the ous spatially distributed motor nerve
initiation of a propagated muscle action terminals. Such multiterminally inpotential. Each motor neuron innervates nervated muscle fibers (Fig. 7.2) respond
many muscle fibers. The motor neuron electrically with junctional potentials
and its muscle fibers comprise a motor only, but since these occur at many sites,
unit. Each muscle contains from one to eJectrotonically spreading depolarization
several thousands of motor units. An can activate the whole fiber. Muscle
impulse in one unit, or a synchronous fibers of this type m"y be mixed with
volley in many, causes a brief contraction others, as in some frog muscles. They are
to summate if they overlap, or to fuse usually innervated by small diameter
into a smooth contraction called a teta- motor axons.
Since individual vertebrate muscles
nus if the frequency is high. When there
are many motor units per muscle, a are excited by many axons, we think of
means of grading the strength of con- them as being driven by pools of motor
traction of the muscle is to vary the neurons. There is a diversity of s ize
number of active un its. This method of within the pool of motor neurons. Gencontrol is called recruitment (Fig. 7.1). A er<llly, the smaller ones have lower
into ad.lplively patterned ("coordil1<1ted")
sire.llTIS of impulses in the output chan-
r
Muscle fibers
Low
'1.
inactive
~sjon
Axons with
impuls.!;. trains
~-v-High tension
j
243
Fig ure 1.2
T!lI'''s of s1 riR /fd /H1/S(lf illlUrvRlio ,l,
"""""""""""""""
£; """""""'""""',:
Unil erminal innervatio n
Mul1i ' lIrminal innllrvalion
";::Z""""""\C""",,z ',,,n, ;:;$';,
Dinou ronal innerva,i on
! I , ~ I " I " :m , ,:::25tii,
Polynooronal innervation
thresholds for natural stimulation and
are more tonic in their discharge. They
innervate relatively fewer mu scle fibers
and produce wea ker contractions, but
are probably principals in th e ord inary
load of muscle work. T he larger phasic
fibe rs are called forth by stronger stimulat ion and produce vigorous action.
T his relation among threshold, fi ber s ize,
and tonic versus phasic mode of discha rge is probably of gener,J\ s ignifi c.mce
in neurophysiology. 11 is easily demonstrated in sensory system s as well.
Many whole arthropod muscles, and
some in an nelids, are in nervated by only
one or a very few motor axons. [n
muscles innervated by only one axon,
recruitment cannot be li ke that in vertebrates, which add motor units by centra l
enl istment of motor neurons. Bul a
s ingle axon can recru it incre"sing Ilu m-
bers of the muscle fi bers it supplies
because diffe rences in the facili talion
properties of the synapses allow transmission to be effecti ve "I different freq uencies of arriving nerve impu lses in
different fibers. There are also differences in excitati on-cont raction coupling
threshold in some muscles.
Innerva tion of all th ese muscles is of
the mul tilerminal type. At norma l fre quencies of "rriv ing nerve impulses, the
junctions commonly ex hibit the t imede pendent properlies of facilitation or
antifacilitation. Contract ion strength can
be controlled not only by average fre quency of moior axon impu lses, but, in
some muscles, also by deta iled tempora l
structu re of the impu lse train. For
example, the opener muscle of the crayfi sh claw is innerva ted by only one
excitatory neuron, and the myoneural
junction shows sl rong faci litation. A
steady rhythmic Irai n of impulses causes
a contraction of a given strength. But if
the same lotal number of impulses in a
given time is delivered grouped in pairs,
the contraction is stronger. The junction
is considered to be pattern sensitive in
that it responds to delai ls of innervating
tempora l p,1 I1ern, nol just ave rage frequency (Fig. 7.3,A). Recordings from
intact moving animals s how Ihat the
eNS sometimes iss ues molar comm.1 nds
in impulse doublets, but il is not yel
certa in how this potential code is employed, wheth er independently of or
correlated wit h mea n frequency.
Muscles may be polyneuronally
innervated in that si ngle fibers can
receive input fr om more than one motor
axon (Fig. 7.2). Each innervating axon
di ffers in the properties of its endings on
the same muscle fi ber. O ne of the axons
is usually d so-c<l lled "("sl" or phasic
axon that normally car ries short bursts of
Se<:tiol'l II
Nervous Con'rol In Effec,o rs:
O ivers il y of Peri pheral In. egra Uo n
244
A
SLOW
B
FAST
20 mV
0.25 9
I
I
-
ltm\\\~~I~II'lI~\I'I\I\I\I\\"\I'I.
~
~
2 sec
C
ISO
2
•
~
.••,
0 _
0
0-
o· 100
"0
_
,"
oE
-=
0 ·-
'~a
•
50
~
0
U
o
~O--:2C--:.--:,C--~8-:-:I~O--:I2;--:I';'--:'~6 ~.3
Excita tory spaci ng interval (msec)
Fig ure 7.3
Differences .llllong mu sc le s in response 10 stimulus inlerv"L A. A mu S( le
fiber in the c!.1\V. cl 05cr musc le o f " cTab res po nd s to repetit ive sl imu l,l!io n
of " "slow" ~ )(on with 1.ITge detion potentials (upper Ir",e) hav ing slow
(,lci lit,ltio n, and wi th gr,u(u,llly SU lllllldling smooth tetani c contTdc! ;o n
(lower I rd CC shows tenSio n). B. T he Sdme Illu scle fib er exc ited vi .. a " foist"
,,"o n shows 5111.111, qllickly pl,l\cduing action pote ntia ls and small, cloni c .
( :::; nonfuse d) co nlrdclions. IAtwood, 1967. ] C. Pd ttern -se nsilive (fi lled circles) ,1lId p,lttcrn-i n sensi livc (open c ircles) mu sc le of (ray fish. At a const,lnt ,,,~n,, freq ue 'lcy o f 30 shocks/ sec (== 33.3 msec {ntervals), trains o f
~ hock s Me d elivered ei ther ,1 t uniform intervals (extreme right) or at alt erndtely short (d b5d ss~ v~ l ucs) ~n d long illter\'~ls; respon se plo tted as a per_
centd ge of the e\'en ly sp~C(!d cO llt ra ction. Refrdctori ness red uces responses
at the shortest int erv.ll s. IRipley .I nd Wiersmd, 1953. 1
impulses at high frequen cy for quick
movements and produces la rge junctional potent ia ls in the muscle fi ber (Fig.
7.3,8), .md these elicit spike-shaped loca l
response potentials and rapid cont ractions. Anotller axon is a "slow." or tonic,
nerve fiber that normally carries long
trains of impulses at low frequency;
these impulses decrement severely as
they approach the nerve ending, and
prod uce smaller and more facilitating
junct ional potentials that cause slowly
developing con tractions. Common ly
there is also an inhi bitory axon. Each
innervating axon may end upon a large
fraction of all th e fibe rs of the muscle,
the fast axon preferentially reaching the
fa st (short sa rcome re) and intermediate
muscle fibe rs; the slow axon, the s low
(long sarcomere) and intermediate muscle fibe rs (Fig. 7.4). Th e presynaptic
endings of the same axon upon muscle
fibe rs of d ifferent sarcomere length and
hence contraction properties differ in
effectiveness, in arousi ng post junctional
potentia ls, and in degree of faci litation.
An extr.lord inary heterogeneity of muscles and actions and thei r smooth grada tion ca n now be understood, even in
such animals as arthropods, in which
only a few axons s upply a whole muscle.
Th is heteroge neity is the resu lt of the
di ffer ent combinat ions of phasic, tonic,
and inhib itory axons, th e different degrees of polyneu ronal innerva tion, th e
d iversity of type of terminal of each axon
upon dirfel'ent muscle fi bers, the divers ity of type of muscle nbe r, and the
diversity of rise and fa ll times of fa cilitati on.
Inhi bitor axons exert two distinct
effect s, presynapti c and postsynaptic
(Fig. 7.5). Postsynaptic inhibition causes
hyperpolariz..ll ion and increased conductance of the muscle fi ber membrane;
245
"Fast""
a~on
Sec tion 11
Nervous Control in Ef(ectors:
Diversity of Peripheral Integration
(phasic)
Large
" fas!" '
e.p.s,p.
+ spike
\LliLJ:LLLL1.LLLL.'.LLJ..LlllLLllJJ.J
Fast conlraction
More
facilitat ion
Less
fac ilitalion
1
j
Figure 7.5
Di~grtHlwmli(
re"restllialioll of
III ~
Hcitatory a"d i"/Iihitory imlervaliml
of a
(msla(e~tI
mllsdt fiber.
Nerve
/termina I S~
Excitatory
Slow contraction
Inhibitory
Presyn. inhib.
Postsyn.
inhib.
m ))) ) ) ) )6
"Slow"
a~on
Large "slow" e.p .s,p.
Muscle
to msec
ExdlMory urn'e It l'ltliuui, form rleIH·O·
mlisO/Ia. ' )I>1apse, . Inlribilory la mi·
Iluis forlll 'Ifllrorllllmdar sy'W/'SfS
(/wslsyrlapli( illhihilioll) I1Ild nxo· axo·
(tonic)
Figure 7,4
Crustacean neuromuscular innervation. The diagram illustrates the matching of phdsic ("f.1St
axon"') a nd tonic ("slow axon") in nervation with different ca tegories of muscle fiber (indicdted
by sarcomere le ngth ) in a crab muscle. [Atwood, 1973.]
•
/lal syrla/lSf, H/wrl fxril~lory lerll/illais
(llre, y>1aplic illllibiliOlI). [LI1IIS IlUd
Alwood,1973· 1
246
,
Chapter 7
Integration at Ihe Intermediate levels
c
,
~
D
F
Fig ure 7 .6
The ,tn"tomical distribution of ,1XOnS to the dista l thor"cic limb muscles of several groups of
Mabcostrac ... BI.lC k lines rep resent motor excitor " xons; colored lines represent inhibitory axons.
Br,Kke!s in dicate tht: distribution ofaxons behveen nerve blllldies. A. Br,lChyu,,,.,.u. AIlDmur" . C.
Stom"lopod,,- D. Palinu,a. E. Astaell'''. F. Stenopodide,' (N"I",,!i.,). The boxes rep,esent the muscles
in the three di stal segments o f the legs, .IS indicated by thei r COllllllOn IMllle5: Il. ,1Ccessory nexor; b,
bender; (, closer; f, exten so r; f. nexor; 0, opener; r, rol,l\or; ~. stre tcher. IWiersll1.l and Ripley, 1952.)
presynaptic inhibition redu ces mi niature
e.p.s.p.'s and the amount of excitatory
transmitter released per impulse. Both
depend on the arrival time of the inhibitory impulse relative to the excitatory,
but in different ways. They are widely
different in importance. Inhibition in
some muscles is mainly postsynaptic; in
others, presyna ptic. In some mu scles the
response to a slow excitor is inhi bited
presytl<1ptically, and the response to a
fast excitor in the same muscle is 'Iess
inh ibited . In the crayfi sh claw opener
muscle, inh ibit ion cau sed by 10 impulses
per second is 90% presynaptic, but a t 40
impulses per second it is only 50% presynaptic. Inhibitory trans mitter is re-
leased with facilitation, which varies
among junctions.
An additional degree of complexity of
muscle innervation in arthropods can be
appreciated if one examines the innervation of the muscle of a whole limb, such
as the walking leg of a crayfish. Several
muscles may be innervated by a single
motor axon (Fig. 7.6). The overlapping
but nonidentical innervation patterns
still .1110w independent action. For
example, the opener and stretcher muscles are innervated by the same excitor
axon but by different inh ibitors. Nevertheless, the whole limb is innervated by
only 12 excitatory and J inhibitory motor
fibers, and this fact of s mall numbers
247
makes it seem possi ble that we will be
ab le to understand fully ,l t the level of
s ingle nervous units the normal control
of movement in arthropods.
The important lesson from the
exa mples chosen is that even ,lt th e last
lin k, the nervous control of effectors,
th ere is diversity in the principles employed, some cases ex hi biti ng a substantial degree of in tegration in the
periphery. Wags have sa id crabs can
think (evaluate) in their legs. We h,we
not exha usted the diversity: fast insect
flight muscles, a va riety of smooth muscles (Box 7.1), electric organs, glands,
cilia, chromatophores, a nd other effectors manifest additional principl es of series and parallel control (Fig. 7.7).
III. ANALYSIS OF
S ENSORY INPUT,
PARALLEL AND SERIES
PROCESSING
The general principles of sensory reception are common to systems as different
as vision and taste and to inputs that
rarely re,lch consciousness, such as those
from pressure receptors and che moreceptors in the grea t Mteries, as well as
those that do. Foremost is the principle
of parallel cha nnels: many receptors independently sample the sti mulu s world
a nd send their imp ulse-coded reports to
the centra l nervous system in parallel
afferent fiber s. The basic independence
may in some organs be abridged by
superimposed in fluence fro m the centra l
nervous system (centrifugal or efferent
infl uence) or from neighboring receptors
(lateral inhibition).
Inti mate ly rela ted is the second
principle, that of overlapping receptive
fields: neighboring receptors are gener-
all y stimulated by a fract ion of the impi ngi ng world that is large but circumscribed (the excita tory receptive fi eld,
ERF) and which overlaps substantially
with that of cont iguous ch,lllneis. T his
applies in some systems to topographic
oV('flap and field s, s uch as areas of the
skin, retina, a nd basilar membrane
(which distributes sound frequencies to
aud itory afferent s). In some systems the
overlap involves ambiguity in modality
(Chapter 6, p. 214).
The third principle relevan t to the
present section states that sensory input
typically exhibits divergence and convergence in th e central nervous system,
the former d istributing information to
analyzers concerned with different aspects of the sti mu lus world, the la tter
permitt ing resolution of ambigu ities,
sha rpening of field s, and abstraction of
special features. Generally, divergence
predominates in sensory pathways, so
that even though each neuron still rece ives synapses from ma ny different
presynaptic cells, there are increasing
nu mbers of cells at each higher neu ral
level enroute to the sensory cortex . One
characteristic exam ple is the first- to
second-order neuron stage in the auditory system, already mentioned (p. 108).
The value of such wide divergence is that
different postsynaptic cells, receiving
in put from subtly different, overlapping,
presynapti c populations, can perform
d ifferent types of information-process ing
operations in parallel, more fully extracting all available in for m'ltion. Thus a
visua l signal ca n be analyzed by diffe rent
cell populations for brigh tness, shape,
color, distance, and movement; an auditory signal, for frequen cy, rate and direction of change of frequen cy, duration,
in tens ity, presence of overtones and
temporal patterns, localiza tion of the
Figure ??
Various Iyl"'s of ,!f,·c/ors.
,
,
:,
- :
~
,
, ... ,
, -,
,
/
'\
--,
Fly wing muscles
Snail heart
Bladder. ureter. u reth ra
0 'VIJ\iIfWWVl M!l!\ilflfV\f\']
rlJlit/lJlJlflJVWW\IWIJV\I)
~'1NlfWV\N\I\I\fV\.I\i\iUvt,'j
e""""'VWINVlIVWWVW]
Elect ric organ
c~,
Salivary gland
Chromatophore
•
248
Box 7.1
T he Nervous Control
,.------
o~
We will briefly revicw the sl.lte of knowledge with
respect to vcrtebr<ltcs. Prosser (1 973), from whom we
take muc h of this .lecount, divides 5moolh muscles of
vertebra tes into two kinds, unit<ll'y and multiunitary,
with some intermedia tes. Unitary muscles include Iho~
of the ma'or viscera - uterus ureter, and gastrolnies!in .. ! IT"'t. These s ow spontdllcOUS rhythmicil ,
and distr ibution of excitation IS
tned ro m muscle
fi ber to fibe r. They ca n be stimulated by st ret ch and
mo(lii1;ueaby nerves. Multi u n itd ry muscles ii1c"l ude
niclildlJ ng membrane an pi omolor, cilia!),•. <tnd iris
nruscles. T hese are norma lly aclivdted not spont.lneo~y or by stretch, b'"Ut by nerves or ho rmones; d is tri bulion of excitation within the muscle is normally by
nerves. I here may be 1 ,lcilitatio n of p.s.p.'s; severdl
nerve- fibers may influence one muscle fiber.
Unitary muscles ,lI1d some o thers ,ue typically
arrJngcd in bund les of fibers glnncctcd to each other by
" nexuses," areas of dose ilpposi tion .1Ild e lecirica l low
resisl,mce. The motor nerve termina ls release transmitter from large numbers of varicosities (swellings).
Only some muscle cells receive d irect inncrvdtion (see
figure). O the rs are excited by their d irect electrotonic
coupling 10 these. Still others aTe excited ind irectl y,
pcrll<lps by a combinatio n o f e lectronic coupling .Iud
diffu se transmitter. In different viscer.l the smooth
muscles vary widely in the proportio ns of these th ree
types,.lS well as in cable prope rties, ion dependence.
the effects o f transm itte rs and drugs, sym p.lthetic ilnd
pa r.lsym p.lthetic innervation, a nd Spont.lIlCOUS activity
patte rn .
~ "Di reclly innervated "" cell with close (200 A)
neu romu scular junc tions
C
iii,'
. :J "Coupled"" cell exhibits junct ion po te nt ials
Carried by e tectrot onic coupl ing
c
~
"" tndirectly coup led·' cell ex hibits only ac tion poten tials
l ow-resistance pathway
Varicose nerve fiber
Schelnatic represenldtio n of the types of autono mic innervation of s mooth mu scle. All th e smooth muscle fibers are In terconnected by l ow-re5 i 5 t~ n ce electrotonic junc tio ns, shown here as bridges.
Some receive direct nerve endings (ddrk shading): othe r.; (light shading) do not, but Me clo~
enough to the forego ing to show junction potentidls th~t h,we spread elect rotonical1y. The mo st
remote (unsh ..ded) show no junction potentials; they n",y be elicited by electroton ic sprNd of
aClion potentials from the preceding d"ss and by tr.. nsmitter rele.. sed fro m the varicose nerve fibers
at some disl"nce. [BurnstO( k and IWJ~·ama, 1971.1
249
source in space, etc. After bu ilding up
s harply specillc response requirements,
these elements can again converge to
combine their specificities.
Ani mals abstract from their total sen·
sory input specia l qua lities of that input
before formulating a motor command. A
frog jumps and snaps at any sma ll, dark,
moving object wit hi n range if it is in the
mood. A male stick leback fi sh attempts
to CQmt with any oval, silvery, redbottomed object of su itable size, whether
it be a female stickleback or a crude
mode l. A few ChM.lclers of Ihe whole
constellation of visual inputs associated
with the female stickleback seem to be
the only relevant ones to the ma le (sec
Chapter 8). How might fil tering of this
quality (recogni tion) go on in the
nervous system?
We could discuss mtering networks
for any sensory modality, but space does
not permit a survey. Instead we will
concent rate on visua l filteri ng. Since
notions of moda lity, submodality,
labeled lines, and tempora l coding have
been dealt with in Chapter 6, we can go
directly to a consideration of relatively
complex network functions.
The histological structure, cell types,
and connectivity of the vertebrate retina
have already been descri bed (pp. 12·1126), together with some of the electrophysiological properties expressi ng the
coupling fun ctions of the connections.
At least thirteen fun ctiona lly distinct
types of optic nerve IIbers carry information to Ihe brain from the eye in the
ca t. Ta ble 7.1 gives ,I recent classificat ion.
Note that 92% have exci tatory receptive
fie lds (ERF's) that are concentrically
organized. These arc either brisk or
sluggish, referring to the promptness and
vigor of their responses, and either
tr.lnsienl or sus tai ned, referri ng to thei r
mainly phasic or mainly tonic char.lcter.
For each of the four combinations of
these properties there are two types,
distingu ished by the sign of their COIlcentric orga niza tion. There are ONcenter-OfF-surround units and Ihe converse, OFF-center-ON-surround units.
Units of the former sorl are excited by
the ON of a sma ll spot of light in the
centra l zone of the ERF or by the OFF of
an annular illu mi nation of the s urrou nding zone. Units of the latter sort arc
converse in character. The table lists all
types of uni ts in the order of their axon
diameter, the largest first. T he largest
and fa stest un its, those in the brisktransient group, are also ca ll ed
V-neuro ns; the next la rgest un its, those
in the brisk-s ustained group, arc also
called X-neurons. (All the rest, both
concentric sluggish and nonconcentric,
are coIiectively ca lled W.neurons, but
this term embrilces too heterogeneous a
set to be useful. )
For ma ny years the cat was descri bed
as havi ng ess·e ntially only two types of
optic nerve fibers, ON-center and OFFcenter. In contrast, the rabbit, ground
squirrel, and gray sq uirrel were described as more frog-l ike in having
several com mon nonconcenl ric and more
complex types-for example, those preferring movement, some specillc for
direction of movement, some even for
orientation. It now appea rs that the cal
has about the same v.uiely of Ilonconcentric units, including th ese complex
types, but in much small er propo rtion,
8% compared 1034% in the rllbbi t. In the
cal, "loca l edge detectors" are fi ve ti mes
as com mon as "direction selective" units;
in the rabbit the lalter predominate,
except in the viSual st reak (the equivalent of the are.' centralis, for high resolu tion) .
5«lIon III
AnJiY5iJ of ~n'iOry Inpul:
I'Molliel ~nd Series ProcesSi ng
Overlap 01
receptive lields
Convergence
250
Clupler 1
Intcgr.ltio n at the
I nter l11ed l~ 11!'
leve ls
All of these optic nerve fi be r Iypes
bespeak transa ctions tha t process the
information encoded by rods and cones.
La tcra l interact ions, convergence, and
highly specified connect ivity (see
Chapler 3) among receptor, horizontal,
bipola r, amacrine, and ga ng lion cells are
a ll indicated. This is usua lly referred to
as early extraction of fea tures to distinguish it from further changes in the
mea ning of cell discha rge at laler stages
in the visual pathways. It also evidences
paralle l processing for centra l destinations of q uite differe nt fu nction. The
c£>l1lr.11 targets of these o ptic nerve fiber
Tabte
types are known o nly in parI. In the ca l,
X- a nd V-fibers go ma inly to the dors.l l
late ral geniculate, e.lch to its priVate class
of geniculate ne urons; these in turn
project 10 the vi sual cortex, X-fibers to
the so callea simple cell s and Y-fibers to
the complex cells. W-fi bcrs go to the
midbr.l in, largely to the tectum. It sho uld
be pointed ou t here that the re are a t least
s ix cent ral targets of optic nerve fibers, of
whi ch the dorsa l later.ll genicu la te and
th e tectum are on ly two. Evidence suggests that they have d ifferent functions.
T he retinas of frogs. lizards. and
pigeons have even fewer concentrica lly
7. 1
Recepti ve fi eld types of 960 cal relina l ganglion cell s, Latencies are the ranges of a ntidromic conduc tio n ti mes (rom the optic tract stimulus site, and can be t,lke n as proportional 10 Ihe reciproca l of axon diameter.
Types
Concentrically organized
Brisk
Transient
ON -center
OFF-center
Sustained
ON·center
OFF-cenler
Sluggish
Sustained ·
ON-cenler
OFF-cenler
Transient"
ON -center
OFF-cenler
Nonconcentrically organized
local edge detector
Direction ·selecti . . . e
Color-coded
Unilormily detector
Edge.lnhibitory OFF-center
Unclassilied J
-
Larency
(msee)
Number
Pereen/age
887
92
243
115
25
1.0-2.4 ) y."I1,
128
531
271
260
55
2.5-5.9 ]
113
44
12
m
BO
4.6 - 2 4.0
22
22
27
13
6.1-18.7
14
W·cells
73
45
B
11
1
6
5
3
3
X-cells
5
<1
<1
<1
<,
6.6-15.9
6.1- 12.4
3.8-14.2
8.7-13.9
3.9-6.6
Sou"e. Cleland and Levl&k. 1914
' In e lurtl'lOr 42. Ihere wera insuiliciont obserYlllLorlS to distinguish whelher sustained Or transie nt
22 OFF·center)
I Insu1liCIIlnt ObServalions 10 reach e conc lu sion.
(21 ON-center.
251
organized ganglion cells and many more
movement-specific cells. This is probably not a phylogenetic trend; it may
have some relation to habit of life and
the roles of vision. frogs are known best
from ~onee ring work by ~et vi n,
Maturana, NrccU11iJcI~s, who
SeCI-Aim:u! h5f more Itah.lf<frk1ilOs than
flashes of diffuse fields or focused
beams, and from the quantitative work
of the Griissers (Fig. 7.8). In contrast to
the cat, in which all optic nerve fibers are
myelinated, the vast majority in frogs are
very fine and unmyelinated. The five
types of optic nerve afferenls may be
summarized in the following way. (a)
Type 1 fibers, called "susta ined-edge
detectors," respond to a sharply focused l
edge of an ob ject, light or dark, moving I
or recently having moved into the 1 °
ERF. (b) Type 2 fibers, called "convexedge detectors" (Fig. 7.9) respond only to
a sma ll object, darker than the background, that moves into or has recently
moved into the field; they must detect
not only the change of position in the ca.
3° ERF but also tha t there is little or no
change of position in the ca. 15° surrounding inhibitory receptive field (IRF).
(c) Types 3 fibers, called "changing con-I
trast detectors:' respond to any edges in
motion, large 01' small, dark-an-light, or
light-an-dark, if the contrast and rate are
adequate and the edge is not too fuzzy.
These fibers give a weak response to
nonmoving tempor.l[ changes in light;
they aTe classical ON-OFF units, but
much prefer motion. (d) Type 4 fibers,
c.llled "dimming detectors" respond to
any dimming or darkening, whether
caused by motion or not; these are OFF
fibers but not like the concentric OFFcenter units of the C.1t. (e) Type 5 fibers
respond to any brightening; these are ON
fibers, but not concentrically organized,
-30l
with a n OFF-sensitive surrounding excitatory field, as in the cat; they are more
sensitive to blue light than to white or
other colors.
Types 1 and 2 are fine, unmyelinated
axons in the optic nerve and by far the
most numerous. Types 3, 4, and 5 are
myelinated. Types Ito 4 go to the optic
tectum of the mesencephalon, type 5 to
the dorsal [ateral geniculate of the
diencephalon. Histo[ogica [ types of
ganglion cells with distinctive dendrite
branching patterns are probably associated with these fiber types (see
Fig. 3.4).
Types 1 and 2 do not respond to general illumination, and their responses to
movement are not influenced by the
[evel of ill um ination over a range of
intensity of mOTe than a hundredfold.
Given their req uirements they di scharge
at a rate tha t encodes contrast of the
moving object (but not light [evel) and
rate of motion of the object minus that of
background objects in the IRF (but not
relative motion). The discharge is
ambiguous for certain severely constra ined combinations of object size,
contrast, speed, and amplitude of movement.
Change of position is as good a stimulus .15 visible movement; th us a good
res ponse is elicited by briefly illuminating a sta tic scene (no response) and th en,
during the dark period between flashes,
moving an object within the ERF. The
"memory" of the position of objects
during the first flash lasts through at
least one second of darkness (Fig. 7.10).
An additional and remarkable property
of type 2 units is erasability. When such
a unit fires upon motion of a sufficiently
convex edge toward the ERF center, it
continues to fire at a [ower rate for some
seconds after the motion stops; but it
Seclion III
Analysis of Sensory Input:
I'arallel and Series I'rocessi ng
252
Movement of a 2' black spot
Oitfuse light
---I
Class t
00
f"
1 sec I
Of<
Class 1
Class 2
Class 3
11111
Class 4 - - - - - - --
Class 2
I
Class 3
Class 4
I II
111 11111111
Horizontal movement
of a 2 x 10' vertical
black bar
_ __ _ _ _ __
. /-
Class!
Class 2
. Class 3
Class 4
11 11111 11
11111
11111 I I II
J
ERFsize
-- tttHtIHHlHtttttHtttttttt--~ 2- 4'
11111 1111 I II
25-4'
Location of optic
nerve fiber endings
Horizontal movement
of a 2 x 10' horizontal
at tacta l cell
black bar
6_8'
~ 10'
dendrites
./
~
~~~
Class 1
....:::::::::
Class 2
~
111111 1 I I
Class 3
1111
Class 4
111 1 I I I I I
----"'- .
,.,.".g05.
61111 111111 11 I I I I II I I
I
R
_
Excitatory synapses
----l Postsynaptic inhibitory synapses
~I Presynaptic inhibitory synapses
Fi g ure 7.S
Types of ganglion cells and their optic nerve fibers in the frog. Above. The four types found in the
optk tectum, distinguished by thei r responses to four kinds of tests. ER f, excitatory receptive field;
s.g.r., stra tum griscum ce ntrdle of the tectum; •. g.s., stratum griseum superficiale. Below. Diagram of
the connections between the elements of the retina converging on a ganglion cell; presumably differences in the details of these connect ion s and their transfer functions account for the types. II. amacrine cells; B, bipolar cclls; G, ganglion cells; fi , horizontal cells; R, receptor cells. [G rilsser and
GUsseT-Cornehls, 1972.]
253
Type 1
tlbor
No spikes in response 10 room light ON
or OFF or to e large moving bar
Flash
Flash
Light
inion sily
0
or to illuminating or moving
a natural-looking image.
-'
8
No
response
~
8
•
Stationary obloct
Good re5ponse to small, dark
mOving object In II 3" field,
Flash
Flash
light
0
inten sily
Response
1p::..J
'~.
8
even if th e illumination is
very taint. but
Change in position
during dark
Figure 7.10
"Movement neurons" mdY respond to chJngc of
pos iti on, with ~ forgetting time.
not ilthe edges ere too fUllY ,
or to reversed contrast.
Figure 1.11
Abstrdctlon e.. rly in ,m .1(ferellt pJthway. 1m·
pulses recorded from .. frog oplk nerve fibe r
in the roof of the midbr.. in. [Based on d .....
of M"t ur"nil al aI. , 1960. )
254
Chapter 7
Integr~lion
at the Intermediate levels
promptly (eases if the light is turned off
briefly, and does not resume after the
light is back on.
Notice that units of type 2 respond to
any sma ll, dark, moving object, espe(i,llly if the motion is jerky. A hungry
frog will jump at .my such object.
Normally any object having these characteristics in the environment of a frog
will be a bug, an edible object. Since
there are many detectors of type 2 spread
over the visual field, the activity of one
or morc fibers of that type can both
signal the presence of a bug and give its
spatia l coordinates, hence both activate
and steer a jump and a tongue flick.
Tadpoles may lack some of the Iypes
more important for the metamorphosed,
hunting frog. Type 4 units in the frog's
optic nerve signal general dimming,
perhaps the approach of a predator or
any large object.
The known visually oriented behavior
of frogs in a natural environment in~
cludes finding food and avoiding obstacles and large, threatening objects.
The fi ltering processes that occur in the
retina in frogs can abstract the relevant
aspects of the whole visual input signal
for those behaviors. Studies by Ingle and
by Ewert, us ing single-unit recording,
ablation, and stimulation suggest that
central processing builds on the retinal
filtering by separately analyzing optic
input for different behavioral meanings
in different structures. The frog's attraction to blue depends on the dorsal
geniculate; its avoidance of large obstacles in jumping and its retreat from
large threatening objects may depend on
distinct, overlapping parts of the pretectum, and its approach to food upon the
tectu m. We may speculate that the phase
locking of its circadi,'11 rhythm with the
environment.,1 photoperiod depends on
a hypoth.1lamic center, the suprach iasmatic nucleus, .'s has been shown in rats.
Each of these four central structures receives its own optic input, consisting
la rgely of a distinct mix of the ganglion
cell types.
As activity proceeds through first-,
second-, third-, and nth-order neurons in
a sensory pathway, the me.1ning of the
impulse activity changes. We have been
considering differences in meaning in
parallel neurona l pathways as a result of
divergence; we should note the differences in meaning in successive neurons
as a result of convergence. When the
criteria for firing include .1 significant
fraction of the complex features of .,
stimulus that releases norma l behavior,
we m.,y speak of recognition cells; th is is
a matter of degree. Higher-order ce ll s
may add dimensions to the criteria, such
as novelty or familiarity. A novelty un it
deep in the frog tectum may fire in
response to a small, dark, moving object
anywhere in a large (30°) field, but will
soon cease, only to resume if th e same or
another object wiggles in a fresh part of
the field. A familiarity unit fires in
response to a similar object, but, instead
of ceasing, continues, even maintaining a
low rate of discharge ("muttering") for
many seconds if the object stops moving.
It now ignores fresh, moving objects
within its la rge (30°) field. It will fla re up
if "its" object s lowly moves about within
Ihe field, but will lose it and go silent if
the object jumps too far-to a fresh part
of the field!
In the auditory sphere too, we know of
units of a wide r,lllge of co mplexity of
criteri;!., In bats, for ins tance, a series is
found leading to ce lls that do not fire in
rcsponse to any pure tone at any
intensity but on ly to frcq uc ncymodulated to nes with a certain range,
rate, a l.l d direct ion of modulation, like
the bat's echo-ranging cry. In squ irrel
monkeys, cells arc found that s tro ngly
pre fer a certain one out of some 20
tape-recorded sounds chosen from the
35 or so natural vocalizations in the
species' reperto ire.
Some workers distinguish between
recognition of natural sti muli and feature
extraction; thc form er is potentially more
complex a nd may result from convergence of cells of th e laller type. The
term "fea ture" in this context means
lim ited aspects of a complete natural
stimulus, such as duratio n or frequen cy
modulation . Our information is still too
lim ited to decide whcthcr some subsystems in some a nimals work differently from o thers in a fundamental
sense. It is oft e n s upposed, fo r example,
that some subsystems fu nnel s uccessive
featu re detectors down to a s ingle recognition unit, like a " bug detector,"
whereas o thers never quite converge the
set of re leva nt feat ure detccto rs. We d iscussed the samc problc m from ano ther
di rection o n pp. 238-240. By whatever
means, complex natura l stimulus recogniti on mu st occur widely in nervous sys·
tems-sometim es early in the pathw.1YS,
sometim es late.
M odulation of input by ce ntral influence via centrifugal (efferent) fibers is
a potentia lly important part of the active
fil tering in many sense o rga ns, as was
noted on pages 170 and 225. Inh ibito ry
•
255
,
d,
Secllo n IV
Elemen' MY Ne uronal Nelworks:
Eme rgen t P,o!,(, rties of Ci rcuitry
f/
"
.,
ga
Figure 1.11
Efferent fibers ' 0 <l sense o rgd n. Axons from the
brain to the ret in~ in the pigeon. Golgi prepdfation. ig, displaced gang lion cell; f, n~t ~macr ine
cell; gil, ganglion celt I~yer; ir, inner nurleM
I~ yer; ip, inn er plexiform I~ yer; 5, Snl,l 11 pM,Isol
amacrine cell. [Maturana and Frenk, 1965.J
fibers to m uscle receptor orga ns in crayfish are illustrated in Fig ure 2.75. The
y-effcrents to muscl e spindles a rc trea ted
below (p. 267 el seq. ). T he mammalian
coch lea (Fig. 2.80,C) and the avian retina
(Fig. 7.11) arc also well-known exam ples.
but the fu nctio nal Significance of the
effercnts is no l yel adeq uately understood.
IV. ElEMENTARY NEURONAL
NETWORKS, EMERGENT
PROPERTIES OF CIRCU ITRY
In Chapter 3 we introduced some wellstud ied examples of connectivity and
ccrtain general prin ciples of circuits of
neuron-like units. Here we extend the
di scussion to emphas ize th e physio logica l consequences. Three kinds of ,Hrays
will be chosen; these may be c.lllcd
" networks," fo llowing th e usage in th e
literature o n neural mode ling, me,m ing
any assemblage of con nected ne uro ns .
I
256
Ch3pter 7
Integration at the Intermediate levels
A. Mutually Exdtatory or
Positive-feedback Networks
If two or morc neurons are capable of
exciti ng each other, then input tha t exceeds th e threshold of one will likewise
excite the others (Fig. 7.12A), Should the
others exceed threshold as it result, they
feed excitation back to th e first, a nd a
runaway process ensues. The whole
Inetwork may come into a state of maximum activity a nd, without lim iting
/ processes, might stay in that condition.
Most neurons have relatively long-term
sel f-inhibitory processes, such as adaptation, accommodation, or fati gue. As the
neurons in the positive-fe ed back network begin to fatigue, one or more of
them will decrease in frequency. They
then excite the others less, and hence
also receive less excitatory Feed back. Just
as the whole network was able to rUIl
away to maximum activity, it now ru ns
away negatively to a min imum state.
Once the adaptation or fa tigue has worn
a way, a n~ cycle C,lll begin. Networks
of cells, each of which may not be capable of rhyth mic bursts of activi ty, can
produce bursts of more-or-less synchronous activity in all mem bers.
Networks of this kind have been
demonst rated in severa l cases and may
be widespread. Inspiratory interneurons
in the medulla are probably so connected, perhaps leading to their rhythm ic
bursting. Certain cells in the brai n in
several gastropod molluscs have been
found to be positively coupled. They
produce synchronous rhythm ic bursts ')
that act as triggers in the control of
feeding and other activities. D eca pod
crustacean hearts al'e controlled by t,ri\
ga nglia containing only nine cells. ®-; ~ ~
baweerr- some of these is known at
least to aid in the build up of the heartbeat.
B, Mutually Inhibitory or
Negative-feedback Networks
I
I
Figure 7.12
Simple networks wilh (AI mulua1 excitMion and
(B) muhIJ I inhibition. lnpu l (omes from presyndplic axons. Excitatory synapses shown by
forked axon terminals, inhibilory by te rmi nal
balls.
Two cells, or two clusters of cells that
inh ibit each other, may produce alternating single impulses or rhythmiC
bursts.
This
arrangement,
ca ll ed
reciprocal inhibition, is a common feature of the control of antagonistic effectors or actions. The activation of motor
neurons of one group of muscles is often
coupled, both by feedback and feed for ward, to inhib ition of the motor neurons controlli ng a ntagon istic muscles (see
Section V, p. 266) . This ki nd of reciprocal
inhibition is di,lgramma tically simple in
257
Vest>bular l'Iuclel
VIii n(trve roolS
Figure 7.13
A reciproedlly inh ibi ting pair of neuron s. The gi.1l1 t cells of Mduthner in the medull~
nsh, sc he·
'll~ticdlly shown, with the inhib itory colldlerdl (/I) Indicd tcd only on the left, the indirect VIII nerve
afferenls (8) only on the lefl, ~rrd the dired VJJJ netve dffercrrts (e) CO.lllrlg orrly from the right,
~lthough .III the5e components ~re ru lly bildleul. I Rct~l.lff dnd Fontdlne, 1960. 1
0'
the Cdse of the paired giant Mauthner's
fibers of teleost fish and tailed amphibia
(Fig. 7.13). T he cell bodies and large
dendrites ofl hese neurons are situated in
the medulla, where they collect input,
including particu larly Ihat fro m Ihe
eighth crania l nerve (sec also Fig. 2.17),
The axons cross over before descending
the spinal cord to synapse on the motor
neurons of the longi tudinal musculature.
Each axon has a bra nch that ends in an
inhili,ilQry: 5 na se on til contra I ral
Maulhner's cell axon hil
, nca r the
spike- initiating site. (This is an electricill
synapse. ) An impulse in one cell prevents a simu ltaneous one in the other.
Each descending impulse activates,
nearly synchronously, an extensive longitudinal body wa ll musculature on one
side, causing a twi tch-li ke curvature of
the posterior body region or tail. This
startle reaction begins the familiar, sud-
,
den "jump" of some fish when the
aquari um glass is struck. The vibrations
excite the sensory endings in the vest ibular apparatus of the ear. Although these
cells have the largest axons in the body,
and although each has thousands of
input terminals and must be often bombarded with very many impulses per
second, they produce on ly the occasional
output necessary for start le reactions.
Another system of one-to-one alternation is found in the neurons driving the
tymbal muscles in some cicad.l s. A pacemaker interneuron firing about 200 impul ses per second drives two mola l'
neurons, which each fire at halF this rale
in exact alternation and precisely phased
with respect 10 the pacemaker. The
alternating clicks of the two tymba ls
during song double the sound frequency
poss ible if they were synchronous.
Reciprocal inhibition Cdn lead to
Secllon tV
Eleillelltuy Nr urorrdl Ne tworks:
Emergent Properlie5 of CIrc uit ry
258
Thresho ld
C hapter 1
[tlt cgr~tlon
20 mV
I
at th e [nlermedl.t!e le ... el~
Rebound "'lI f table (Iorma l)
Stimuli
II III
,
Inhibitory spike s in
I Spikes out
I IIII I
1
A
~II I
3
1111 1 1111+1--111111 1 1111111 1I1IIH-lH+1II1-1--+m-----11111 1 111111 1111111 1111111
III III I
~III IIUIII!llIIllllllyllmllYilll
iIIl
Briel I.p.s.p. barrage sta rlS
long barrage
altern at ing bursts
sl ops
8
O>---~
'--IlIII----!IIIUIIIIIII -IIIllllIIII
lIlIlIlIllI--IIa8111f--IIIII-~IIII'BIIIIllHlIlIlI----III!IIIiIIIIIII--II~1
'-.
'-
I
--+1111111111
1I11 1 1 111l---111111111
I
3
Single I.p.s. p.
l a tephsse
triggers paUern
intens ifies
lI ;mllll- 11IIlI1I1I
I
I
La ler
pha se resets
1I1"1111U1l
111111111 1111
I
1l1li
RIll-I
c
Figu re 1.14
Rccip rOC.t1 il1hibilion .. nd pastinhibitory rebound provide ncx ible mechanisms (or ~cnerJling bursts,
A. POSlinhibitory rebound in a model neuro n. A neuron 11t.11 is not spont.lneously ,lcli"e receive s dn
inhibitory input and produces spike o utput by rebound . lJ. Two such neurons, reci procally in hibi.
tory. c;on giW! a long 5eries o f altern ating burst s to ~ brief input bArr~ge from ~ third neuron. C. A
single inp ut impu lse has d iffe rent effects .according to t he phase of the .altern ation when It url\"!'s.
[perke l and M ulloney, 1974.1
1
alternating bursts of act ivity in otherwise
nonbursting cells. The networks shown
in Figure 7.14, B and C cons ist of only
two interconnected cells, but they could
represen t two populat ions. Input to the
network is inhibitory in this exam ple,
.1nd reaches only one of the cells. Th e
com mon neurona l property of postinhibitory rebound (Fig. 7.14,A) is
invoked in this model, and causes bursts
that suppress the ot her cell. As the rebound burst in the first cell s lows down,
the second is dis inhibited. Released and
rebound ing in its tum, the second fires
259
and inhi bits th e first. As the seco nd ce ll
s lows, th e fir st recovers, and the whole
cycle repc.l ts.
Whether dependent on rebound or
not, some such si mple mecha nis m for
alterna ting burst acli vity, though difficult
to demonstrate, see ms to operate in
f.wo rable mate rials, like the lobsler
stomatog.lstric ganglion. We believe it to
be an important mechanism for many
kinds of rhythmic and alternati ng behavior. Ins piratory and expi ratory interneurons in the mam malia n medulla
probably inhibit each other. Locomotory
syste ms in ma ny a nimals may involve
r~i p rocal
inhibition between pacemakers for antagon istic muscle sets.
Ikciproca ll y inhi biting networks can
pe rform a variety of fu nct ions, according
to the pa rt icular trans fer functions of the
' synapses and the input and output connections. T he following examples are
theoretica l and q ualita tive; proof that
reciprocal inhi bition is the mech.1 nism
that operates in living an imals is incomplete. G ive n certain properties, reciprocally inhibiting networks can act as
gates, switching ra pid ly fro m control of
the output by one input line to another.
This can recur at a steady r.lIe, for ,1
steady-s tate input, providing a pacemaker in which no s ingle cell is the
essential clement, as discussed above.
With cert ain dynam ic properties the
same simple circuit C,ln act as a n
intensity-lo-Ii me con verier that m,l Y be
useful in comparing the strength of two
inputs by their relative dura tion of control of some downstre,lm system. Slight
changes could provide sensory sca nning
by periodically or irregularly sampling
e,lch of a number of input li nes a nd
giving them control, in turn, of some
later elements. In a cell w ith a large
number of input li nes converging on it, a
,
drastic increase of acti vity in one li ne
would ord ina rily be drowned in the
background activity of the ot he rs; but
reciprocal inh ibi tion in the same cell
might all ow one line to dom inate if its
activity were to rise above some level,
and thus serve to d irect allention or to
switch control. Still a nother possible use
of such circuits, with only slight cha nges
in the coupling functions, might be as an
ala rm system. Time- a nd load-sharing /,1
delay lines. null detection, and filt ering !
are othe r theo retically availa ble con- I
seq uences of such ne tworks.
An array of inhibitory cross-connections can be thought of as a n arelM
in which there is competiti on between par.ll1el streams of impulses.
Both the nonlinearity of dependence on
act ivity levels a nd the cri tical inflections
in the input -output functions wou ld
all ow one strea m to win control. A
spectrum of properties is possible from
democratic to oligarchical to dictatorial.
The reliability of performance of
networks is considered on p. 233.
C. La teral Inhibition Networks
Th is term differs from the precedi ng
head ing in directing a tte ntion more to
l'l yers or arrays than to alternate cells or
groups. Many neural tissues consist of
layers of similar neurons that inh ibit
e.lch other eithe r direct ly or ind irect ly.
The inhibitory connections spread from
a ny part icular cell to make conta ct wit h
neighboring and more distant members
of the layer, but wilh decreas ing de ns ity,
aSwe saw in Chapter 3 (p. 11 1). Hence the
effect iveness of inhibition decreases with
dista nce.
Some effects of latera l inhibition a re
ill ustrated schematically in Figure 7.15.
Seellon IV
Etrmt' nluy Ne uron,,] Ndworks:
EIlIt'rgt'nl t'rop"'rlies of C ircuitry
260
Inhibitory
Interneu ron s
5
sensory nOl,l ro ns
/0
-
+ $
O..;'-------~,,?--~J:0"''---0..,/
,s'---------<<E;"s
- a.."~"
__(0,:'----'"
0'~
o,:s'--------~C~"-'-<'~-(o,:S'--C+~1
"Yo"v/'"
S + E+ I
~ +"E'--_ _ _ _~O"-'-'-"J
(0':'-'--"-''-'
O,S'-"
;<,',).
0;s'-+:':.!E'--_ _ _ _~<::~"~,-,-:'~,1os + E + 21
O"S'-'+"E"--____~cr:c"-'-'-'~(OS + E + 21
0;;;;:0..,,/"
"S'-+:':.!E'---_ _ _ _~C:"-'', (O~'-"'-'--"
5 + E + 21
0~ ''--Re ceptors
0
Inhibitory
Second-order
sensory neurons
Interneurons
"Brighter"
" Darker"
~----.
Physiological
Stimuh.l!
in tensity
A
B
ellect
c
o
1
261
Flgu.~ 1. IS I/llriHg r~SO')
l .ltl'r.ll in hibillon. A. A p.lUl'rn
unifolmly gr.y ,"r.lS with shup f>dgn. rrpr~rnlinR .I "isu.1 fit'ld
_n by .I n eye. (M.lch b.nds • .In illusion in ",hlch .Ipp.onmtly d.lrk er .nd lightl'r lunds .Irt' _ n
.I round t'.tch t'dgt', Mt' not evidl'nt to us in this conrrguration.) B. The sllmulus ploul'd <IS inlensity
(horizontlll) .Ivinsl lpo1 lial e>:tt'n t (,-ert ic", IL emphllsizi ng the unifonn ily of the pnysiclll intt'Mily
wit hin ('IIC"h IIrt'll. C. A network of rtc~ptOfS ",nd S('cond ~rd('r neurons with rt'ciprocal Inhibitory
C"o nntelions vi. inll'rneurons (brokr n linrs). Spont.l nrous act i\~ l y in the re«plors (5) is .I ugmenlOO by
ucildtion (E ) d ue 10 light. Thl' network CdU$e5 Ihe sl"<ond ~rder nl'u.o ns 10 show 5 dC"ti vity dU g1111'ntl'd by E . nd/ or rt'd ucl'd by inhibition (I ) in single or doubll' (11) dose. D. Th(' output, ('(j Ui"d'
len l to our $ensdlion, piatti'd .IS dMker or ligh ter th.n tht' bolCkground dut' to S.
0'
First consider Ihe behavior of one spontaneously active cell in the network
while a stimu lus is moved about its input
field . As the stimulus approa ches, it first
excites neighbors of the recorded ce ll.
Si nce they inh ibit Ihat cell, it res ponds
by a decrease in firing frequency. If the
stimulus passes directly over the recorded cell, it is excited 10 fire above its
normal ra te, but as the stimulus moves
on il is again depressed by ils neighbors.
Any cell in Ihe network may be characterized as having a recept ive fi eld that
has an excita tory center and an annular
inhibitory s urround. Th is is compa r.lble
to the ON-center ganglion cells of the cat
ret ina.
If, ins te.ld or looking at the response
made by a single cell in the s patial array
or Figure 7.15 to a moving sti mulus, we
examine the ou tput of a whole line of
cells in the array while one hal f of the
array is stimulated more than the other
half, lVe see an abstracting function of
the network. Cells in either uniformly
stimula ted half of the fi eld all in hi bit
each other symmetrically, but th ose at
the edge do not. Ce lls on the strongly
stim ulated side of the edge are inhibited
wcak ly by their nCighbors across the
edge whi le they strongly inhibit those
!lame neighbors. T he result is especially
high .llld low firi ng frequencies CI t the
,
stimulus edge. In terms of the fir ing
frequencies or Ihe cells in the network,
the stimulus edge has been enhanced;
there has been a spatial di ffere ntiation of
the input signal. A second layer of
neurons cou ld be so constructed tha t it
lVould detect the edge only. Latera l inhibition probably explains our psychophysical illusion known as "Mach
bands" (Fig. 7.15,0), and perhaps operates widely to en hance the sensitivity to
cont rasts.
Since the lateral spredd and ex trd
synapse take time, there is a delay in the
inhibi tion. Th is confers a tem poral property of freq uency se lect ion or fil tering
that acts to attenu.l te ra pid changes as a
function of dista nce rrom the center and
to prolong the exaggerat ion of the primary response at the center, again fa voring low frequenci es.
It Cdn also be seen that the inhibition
exerted on a given cell by those surrounding it can be redu ccd by stilllulation
of a slightly more distant popu lation.
T he di stant popu latio n red uces the lcvel
of activity of the nearer one, wh ich
"d isi nhibils" the center.
These phenomena were first described
by Hartline and his .lssocia tes in a se ries
of elegant ex periments on the compound
eye of Lil/IIIIIIs. The same latera l interaction exist, however, in virtua lly "II
51"<1Ion IV
El tm~nl.lry
Neuronal Ntlworks:
Emt'rgtnt Propt'Tl ies of Circu itry
262
Chapter 1
Integr.lHo n at the
Inlerm~d l~te
l eve ls
sensory syslems in both vertebra tes a nd
invertebrates and may o peT,l le at the
earliest stage in the pathw,lY a nd / or at
later stages, even in the cortex (Fig. 7.16).
We h,wc seen in Chapter 3 how lateral
inh ibition might result from recurrent
collalera ls of the axon e nding on neighbori ng cells (Fig. 7.17). We saw holV such
inhibition ca n be complicated in the
cerebellar cortex by th e inhibitory influence of recurrent coJlalerals of Purkinje
cell axons, not only on neighboring
Purkin je cells bu t on basket cells,
thereby disinhi bit ing Purki njes in a certain geome tric pattern. Re nshaw cell
laler,l] inhibition via molor neu ron recurren t collaleraJs is trea ted on page 269
(Fig. 7.24).
D. Mixed Networks
known <l nd presu mably main ly che mica l.
All the fu nctiona lly established connections can be an.l torn ica ll y justified by
fibers vi sualized by inj ection of Procion
yell ow. How mu ch spontaneity there is
cannot be sf'ated, but it must be cons ide rable. Among these junctions, .,
v,uiety of integrative input-output properties are found. It seems like ly tha t if we
could unrave l the web of influences,
there wou ld be bot h excitatory a nd inhibitory reciprocity, latera l effects, a nd
mixtures of spontaneous rhythmicity
with imposed bu rst-sha ping effects. The
norlllal activity is largely a rhythm ic
se ries of bu rsts of repeatable but la bile
s pike pattern; the known connections
ex plain much of the detail of the bursts.
Alth ough many of the connections of
this network are known (nearly all;
hence far more in proportion than for
a ny ot he r known system of some complexit y), it is difficult to assign causes to
th e bursting phenomenon itself. Does
th e pos itive feedba ck, by itself, cause
one group of cell s to burst, or is the
reci proc.ll inhibition relationship with
a not her group necessary, or even s ufficient? In theory, ei ther mechanism could
prod uce bursting, but physiological evidence suggests that both kinds of connect ions exisl. Perha ps both mechanisms
oper.lle synergistica lly to make th e
whole system more stable.
If both excitatory and in hibitory connections exist in homogeneously in a set of
cell s, the variety of possible outputs
expand s to the degree that it is useless to
make (l priori or genera lized, unconstrained models. A recently studied real
exa mple is, however, worth describing
(Fig. 7.18). T he stomatogastric ganglion
of crustacea ns controls the stomach, one
part of which contains the gastri c mill
used to grind food. The gangli on conta ins 30 cells, almost all of which a re
identifiabl e ,md consta nt in con nections
a nd influe nce. Te n a re motor neurons to
the g.lstric mill part and 14 to the pyloric E. Connections Ensuring
part of the stomach, but both groups also
Synchrony of Activity
have direct infl uence upon each other.
Furthermore, two interneurons are pres- Although exactly synchronous activity of
ent with connections to both sets of neu rons is not known to be req ui red in
motor neurons. There are 123 known m.1 ny insta nces, it is importa nt in a few,
inhibitory connections and only 6 ex- and these a re interesti ng in s howing the
ci tatory junctions. Twenty-nine of the fl ex ibility of design with whi ch cells ca n
junctions are electrotonic, the rest un- be connected, among th emselves .l nd to
",g ill
:g 20
.,.30
'~ 40
50
- 20
30
40
50 20 30 50
100
Vi b rat ion freq uency (Hz)
•
"'.
-"
100
i ~~1iI
A
0
·
~ SO 20 30
~
263
,,
m
- 60
- 80
•.~ - '00
oE
,."
£~
0>
00
_
Lower
aUditory
ce nter
0.2
0.5
Sh~ rjX'n i ng by suppressing sensitivity o n e.lch
side of th e best frequency, with converging
inpu t. A. Th resholds for sensMion as the e nd point; vibr<ltion felt by 2 or 3 fi ngers. 8. Th resholds for si ngle neuron firi ng as the end poi nt;
un it respo nses to sou nd at lower and higher ~ udi ­
tory centers. It should be noted t h ~ 1 such narrow
cu rves at h ighe r cen ters are no t common; units
wi th m.my types of cu rves are found. {Von
Ilckesy, 1967.)
••
•.. •t
• ••
-"
- 60
- 80
Higher
audito ry
cen ter
V•
..\1•
\
H
- 100
0.2
B
0.5
2
5
Sou nd Irequency (k Hz)
~i
f igure 7.11
Recun en! (011,,11'. ,,15, The li ne fibers are the array of colliller.. ls of th ree pyra middl
cells in the corte .. of the killen. IScheibel and Scheibel. 1970d.)
•
20
!
- 20
<
~
10
0
<
Fig u re 7.16
5
2
10
20
264
ALN
'1 $ " hO' !· ..·· t!
!::; 'J ' Io\;" ,IHI I!
LGN
j ' " . ," "'
"
.
~~~
ifjirgii"1'. k
':: :: •. -".,If:;'; 'I:;:: }ff
PNI ~ I • , I I , I , , • I I I ! , , I I I I I I I I I I I , I
d-l VN : ' . • • .
.:!",': . •.. · ... ..... I.' •••
""
'r
!. ' ~,.
- .~ ·
B
"
'"
GASTRIC MILL
REGION
~
____ r,
:
E
I i ibe.s
:
(2)
of
o
.... n
___
I
I
leG's
0
J0
PYLORIC REGION
A
Inl 1
•E
al
lPG N
MGN
LGN
(2)
gm l .2,3a gm 4
c
,,'
cpv l a. lb. 2b
,2.
c7
p2b- 13
265
the periphery, to ,lccomplish precise com n1.1nd or p.l ccmaker neurons ,1rC
ti ming. These can be rcg,lrded as s pecia l usually located in the medull'l 01' midcases of the gene r,\l problem of ass uring brain and act th rough interne urons and
precise lim ing of sequences of activ ity. motor neurons on the electrocytes. In all
Among the best exa mples of systems C,lSes, these neurons are electrica lly
requ iring nearly exact synchrony are the coupled to each other via gap junctions
electric organ discharges of electric fi sh. (see p. 333). The electrotonic connections
(Ot her exa mples are the oculomotor may be between celi bod ies, or denneurons and the neurons innervating drites, or via presyn,l ptic fibers that form
sound-producing muscles and wings in electrical synapses on Ill.lny of the cells.
certa in ani ma ls.) The electric organ celis T hese synapses, by equa lizing the level
(electrocytes) are in most cases com- of depolarization between different celi s,
posed of modified muscle cells thai are are both excitatory and inh ibitory, but
oriented in seri es so th,ll Iheir depola ri- ensure synchronous acti vity of all couzalions ca n be sum med. It is necessary in pled cells. The simplest exampl e of such
Ihese orga ns Iha t all the elect rocytes be coupling is in th e electric catfish,
activated nearly sim uli,lneously, and in Mn/npierllrJIs, in which there are two
some species wit hin « 0: 1 Insec. Th e electromotor neurons, one on ei th er s ide
Figure 7.18 URdHS P~8t)
A si mple sys tem of so me th irty neurons; the stomdtog<lslric gdnglion of .I lobster. A. Side view 01 lobster stom..ch. T he two princi pal funct ion~ 1 divisions, the g.1strk mill region .Ind the pyloric region, are $Cpdr.. ted by ..
broken li ne. PMt of the st Ont.l t og~ st ric nervous syste m is shown togethe r with. few of the stom ..ch muscles
th .. t it innerva tes. T he stomdlog..stric g.1ngl ion (SIG) ",n be seen on the dOrs.l1 su rf..ce 01 the stom ..ch just
dbove g.>stric mill muscle I (gm l). Other lettering identifies muscles .. nd nerves. B. The two bdsic rhythms produced by the isolJ ted g~ngl ion Cd n be $Cen in the extr..cellul.. r recordings from neryes supplying the hvo
different regions of the stomdch. T he top thru nen'es (/U N, LGN, DGN), not all shown in pa rt /I.. supply
muscles th.. t oper.. te the g.lstric mill. Note thdt the bUr5ts of dct ivity be.. r a particuldr ..se rela tionship wi th
e..ch o ther . nd th .. t the d ura tion of cadi burst is ~lseConds. -The th ru lowe"i=tr..ces cont ~ in axons of
mot~ns (MVN, PN, dol VN) suppl ying p.1!2ric musclt!"s. The bunts are much shorter in d ur... ion, and the
o vera ll frequency is •• bou t seven times t ha~U!!.e g_~st~1. Note ~ I so t hat the bunts of ~ctivity ,;;afnt ~in d
pJTticu lar phJse rel ... ionship. The d.LVN t r~ce cont.. ins dxons innervating both regions (sec 'lbo\'e) and the long
bu n ts sun in this tr,lce ,I re from .. xons to muscle 8111 3 ~ . WoIrts A ~nd H, Selverston and Mulloney, 1974. 1 C.
Neurond l con nect ivity di agrdm for the lobster sto m.. tog.ilstric ganglion. All th e cells except int erneurons 1 and 2.
Me motor neuro ns. The top ten neu ro ns control the g..st ric mill cycle, and th e bo tto m fOllrtee n ce lls cO'ltrol the
pyloric rhythm. The dxo na l pathw"ys, ~s well as th e musc les inn ervat ed by the celis, Me kno wn. So mol, neu ropile, and ~ xon .. 1 pMtS of the celis Me Indi cated o n the left. Broken li nes Mound so me of the neuropile Meas in_
di cate that ce lls of tl1.l1 group Me elec troton ically conilCc ted and can be co nsidered together. Kn own con nections wit h the ce ntrdl nervous system Me shOWIl at the top. Ro und dots represelll che mi c.ll inhibitory syll.lpse5;
tridngles represe nt chem icoll excitatory synapses and resistors (= electrotonic junctions): F, functional sy napse
wi th strong effec t but no clear uni t"ry po5t syn ~pt ic poten tial; f, exci tatory fiber input from commissuroll 8<lngli... LPGN, Iolterol l post('rior g.st ric neu ro n; MGN, medi .. n gas tric neuron; LGN, latera! gastr ic neuron; ' "' I
,md 2. interneuro n neuron I .. nd 2; GM, g..stric mill neuron; DGN. dorS<l1 golstric ne\l ro n; AMN. ,Interior medi.lI1 neUTOn; IC, infe rior cMd iolc; VD, ventr iculM dilator; PD. pyloric dil .. tor; A8, .Interior burster; LP, l"'er .. 1
pyloric; PY. pyloric; eG, conlmissu r.. 1 8"ngli.; STGN. stomd tog.lstric nerve. ICourtesy of A. Seiv('r5ton. j
•
Sectio n IV
Elfnlent.lrY Neurona l Ne two rks:
Emergent Pro perties of Circ uitry
266
Clupl t'r 7
Integrdtlon .at Ihe Inlerp.edi.alt' uvels
of the /lrst spina l segment, lightly sponse to IMturaJ stimuli . What can we
coupled to each other. In ot her fi sh, the re say is the s implest ne rvously mediated
may be as many as 20- 50 p.lccma hr response?
The verlebrate stretch reflex, while
cells coupled to each other, all of which
electrically excite internuncial relay cells specialized for simplicity and speed
rather thaI!, be ing primitive, is a good
that are also electrotonica lly coupled.
G iven a synchron ized command, how starting poi nt because it is monoaTC electrocytes at di fferen t distances
synaptic-that is, no interneurons a rc
from the brain activated synchronously? interpolated between afferent fib ers and
Thi s is accomplished, in most cases, motor neurons (Fig. 7.19). Skeletal museither by systematically shortening the cles contain numerous sense organs,
lengt h of branches to the progressively called muscle s pind les, that a re se nsitive
mOTe dista nt electrocyles, or by altering to s tre tch in the ax is of the muscle fibers
their diameter so that the s lower con- (Fig. 7.20). Passive stretch, as by the
duction velocities ofaxons inne rva ting action of gravity or of other muscles,
the nearer electrocytes compe nsa te for causes a train of im pulses to arise in the
Ihe shorter distance. In several s pecies term inals of a sensory axon in a muscle
the gra ded delay is built into th e electro- spindle, and these are conducted via the
cytes. Dista nt ones a re innervated nea r dorsal root to the spinal cord, the re 10 be
their principal surfa ce, nearer ones at the distributed in axon collaterals to the
end of long, slow-conducti ng stalks of dorsal and ventral horns of the same
segment on both s ides of the cord, 10
the elect rocyte.
The ex istence of these mechanis ms for nearby segments up a';;'d down the cord,
building compensating delays into neu- a nd to the dorsa l colum ns ending in
ra l ci rcuits opens the poss ibility tha t nuclei in Ihe medulla. Of these destinasimilar refinements of st ructure may be tions one is the large alpha (a ) motor
involved in other systems that are sensi- neurons of Ih e sa me muscle, wh ich a re
tive to the precise tim ing of inputs, such excited. This excitation is distribut ed by
as the parts of the auditory system re- the axon branches of the motor neuron
sponsible for sound localization or the to a group of mu scle fibers, usually
motor systems controll ing speech, eye between WO and 1000, called a molor
movements, midd le ear muscles, and the unit. Conlrdction of the molar unit tends
to ca ncel the s tretch. This proprioceptive
li ke.
refl ex acts as a tonic muscle-length servo
(like a gyrocom pass), tending to maintain the length aga inst any change in
V. STIMULUS-TRIGGERED
load either way. Gravity is an import.lnt
REACTIONS, THE
norma l stimulu s; th is re Aex arc is the
ORGANIZATION OF
principal a nt igravity circuit.
REFLEX ES
AI th e sa me ti me, coll alcrals of the
With some of the principles of effector spindle afferents fil'c interneurons thai in
control. of sensory input, a nd of ele- turn exci te synergistic motor neurons
mentary circuits in mind, we can now a nd inhibit motor neurons of a ntagturn to the lowest levels of motor re- onistic muscles on the sa me side whi le
267
FIgure 7.20
Til, mll"multiaH /IlI/SlI, sp;/Jdl,.
1111
'-H -t-7 raxons
Molor
J
Figure! 7.19
T he monosYn.lpli<: slrttch rrAu p.ilhlV"Y in IllAmm.. ts, si m pl ifi~ by
oml .. ing Ihr ol her dtslindlions of Ihr s.am(' ..ffrrr ni n('U ron, Ihr oIher
inputs 10 Ihe s.amt mo lo r nturon, ils oulpul rt.'Currenl coll.. ler~ ls, .md
Ihe molor conlrol of Ihe spindle!. IGlrd uer, 1963.[
Nuclea r
c hain
fibe r
Annulo ·
splrlll
endings
Flower -'.-,...,~
s pray
Type Aa
affe ren t
axon
Type All
al/eren!
aKon
Nuclear bag
fiber
endings
motor neurons of the homologous muscle and its synergists on the contralater.ll
side are inhi bited and antagonists excited. The phenomenon of reciproca l
innervation contributes to coordination
by prevent ing antagonists from working
against e.lcn other.
Given this iength- maint.lining re Aex.
how ca n the organ is m walk or voluntari ly ch.l nge muscle length? If higher
cen ters were simply to comma nd "" motor neurons to greater or less activity.
the stretch renex wou ld quickly cancel
the effect. Somehow. the set point
(SoHwert) must be changed. This c.lIl be
done by adjusti ng tension in the muscle
fi bers within the spi ndle. ca lled in trafu sal fibers.
There is another set of motor neurons
in th e s pinal eOI'd that also se nd th eir
e(ferents to th e mu scle. These are the
gamma (y) effcrents. emana ting fro m
small motor neurons (Fig. 7.21). T hey
innerv.lte the muscle fi bers in the muscle
spindle and alter its sensitivity. In the
centr.ll region of the spindle fi bers is a
•
..... Sill S' orgjHl ,x(;I,d by j1fl$S illt 51ft/ell ,
IIdi vII/ioli 01 ;/$ 01011 ;III,i,Jsir ml/Sllt
fibtr5 by ga"",111 m% r axo/IS.
0'
noncontractile enlclrgement filled with
nucle i, and it is to this zone that the
stretch receptor fibe rs come (Fig. 7.20).
The end regions of the s pind le fibers are
contractile and are innervated by the
y-efferents. W hen the y-effe rents increase their activity. the spindle fibers
shorten, the cen tral region is st retched,
and the stretch receptor fi bers are exci ted. It is as if the muscle had been
passively s tretched. T he opposite effects
obtain if the efferents have reduced
activity or the main muscle has increased
activity.
Th e set point of th e postur.ll renex ca n
be affected by tens ion changes in the
spi ndle muscle fi bers. When these contract they stretch the muscle receptors
but do not change the lengt h of the
muscle. T he resulting increase in stretch
Exl ralusal
skelelal
m uscle fiber
>68
From brain
Chapter 7
Integr~tion
at the
Interm~dlale
levels
2
Spinal
cord
I
axon
Muscle
tiber
Figure 7.21
The y·loop servomechanism. Commands (rom the brain may operate by contracting the mu~le fibers
of the spindle via the y-efferents in th e venlral root (2). This excites the stretch reflex (3) Jnd hence
the main muscle. There are also direct conllections (not shown) from the brain to the Ill,,;n motor
neurons. [MNton, 1972. J
receptor firing f<lle excites a -effercnts,
which elicit greater tension and hence
muscle shortening. Shortening continues
until stretch receptor firing rate is reduced again to normal values. The central nervous system can command a
long-lasting new length by varying frequency in the ),-efferents and thus
changing the sensitivity of the stretch
receptors with respect to muscle length.
The setting of muscle length by way of
the y-efferent is called y-loop activation.
The motor neurons (both y and n) for
one muscle are loosely grouped in the
ventral ho rn of the spinal cord. T hey
receive many inputs, usu.1lly in parallel.
The stretch receptor afferents excite only
the n-efferents. If they excited y-efferent s
the reflex would comprise a positive
feedback loop, which would run away to
maximum or minimum tension . Descending excitation or inhibition from the
brain impinges on both y- and Ct,-fibers.
We have already encountered the general rule- that small units are more tonic
and have lower thresholds for n.1tural
stimulation. The y-neurons are smaller
and more sensitive than the Ct"s. A weak
command from the brain excites the y's,
which in turn change the set point of the
muscle-rece ptor-Ct'-efferent reflex, and
muscle length changes to compensate for
this. Strong descending-movement commands excite both y's and n's. The
faster-conducting a's initiate a movement that wou ld be later cancelled by
reflex function were it not for the more
slowly developing effect of y-excitation,
which changes the set point of the reflex.
Thus volunt.wy and other brain control
269
Go igi
tendon
recepto r
Figure 7.22
The tendon recep tor for st retch. Anothe r se nse
org~ n, besides the spindle, is in th e tendon,
which differs by being stretched (excited) when
the muscle con lr~cts as well .1$ when it is
lo ..ded. T he sign of its innucnce is such as to
preven t overconl r.l(lion.
of movement oper.l tes largely via the
y.loop balanced in vc1rious degrees with
coactiv<l tiol1 of a's.
Anoth er set of receptors is on the
muscle tendons, and these respond to
stretch of the tendon (Fig. 7.22). In can·
tr<lst to s pind les, therefore, they respond
in the same d irection to im posed load
and to contr.1Ction of the mu scle (Fig.
7.23) . These receptors (Colgi tendon
organ receptors) have no monosyna ptic
endings, but, via inlerneurons, they send
(a) inh ibitory input to motor neurons of
the muscle they innerv.1 tc and to its
synergists, (b) excita tory input to molar
neurons of antagon ist muscles, and (c)
opposite inputs to motor ncurons of the
correspond ing muscles on the opposite
side of the body. T hese inputs might be
said to perform a tension- regulating
fun ction, restraining th e motor neuron
from causi ng the muscle fibers to COlltract too violently.
O ne more automatic s ubsystem is
important in hel ping to determine motor
neuron activity loca ll y; this is thc
Rens haw cell nega tive-feedback loop,
acting on motor neurons in the s pi nal
cord (Fig. 7.24). Situated in the ventral
roots there are branches of a-motor
axons called recurrent collalera ls because
they turn back and reenler the ventra l
horn to synapse with small interneurolls,
na med for Renshaw, who discovered
them physiologically. These cells fire at
high frequency when excited by motor
neuron output and have the effect of
inhibiting the same and neighboring
motor neurons. The roles of this inh ibition may include preventing motor neurons from excessive activity, focusing
activity upon certain cells and perhaps
su ppressing phasic responses more than
ton ic ones.
Many refle xes are elicited by cxtramuscu lar stimuli. For exa mple, painful
cutaneous s timulation often gives rise to
fl ex ion of a limb (Fig. 7.25). The fl exor
refl ex to nocicept ive stim uli is not
sharply loca lized; it may affecl all the
muscles of a li mb. Both strength of res ponse and degree of s pread of response
are related to stimulus strength. Input
fibers do not impinge direct ly upon
motor neurons, but on interneurons; the
reflex pathw.1Y is polysynaptic. The
input excites flexor action and at the
same tim e inhibits ext ensor motor neurons. If the stimulu s is quite strong its
effects may s pread even to the conlralateral limb, where they are opposite in
sign. The crossed extcns ion refle x prepares one limb 10 bear the extra weight
s hifted to it when the painfully sti mulated one flexes . Similar refl ex con-
Seello ll V
Stimu lus-Triggered RNc tion5:
T he Organization of HeOu t'S
figure 7.23
Spimflt IIfrsrl5 I"rdorr
j Pll llorr , 1965.J
't(flrlor~.
Muscle con tracted
SPINDLE RECEPTORS
" IN PARALLEL"'
~
Discharge
Musc te stre tched
Acceterated
discharge
Musc te contrac' ed
TENDON RECEPTORS
""IN SERIES·'
270
+eo
Motor neuron
+<0
0
•
- 40
- eo
,.s,
'~
~n
•
•
•
0
+ 80
+<0
0
D
,•
E -40
- eo
- 120
Motor
~"'"W"
•
-60~
-70 _ __
-80
:_p_s_p,
I
0
5
"
15
20
25
a!
30
msec
Figure 7.24
The Renshaw type of inhibitory interneuron. Axon collaterals from motor neurons activate
Renshaw cells to high frequency discharge, which set~ up summa ting inhibitory postsyfl<lptic potentials in neighboring motor neurons of the same pool. [Eccles, 1964.)
ncctions are seen for cutaneous touch,
pressure, and temperature receptors.
We have seen now some qui te genera l
contrasts between flexion ,lnd ex tension
reflexes, nociceptive .1nd proprioceptive,
pain and postural, cutaneous and
muscle-afferent, phasic and Ionic reflexes . These are overlapping but not
synonymous d ichotomies. Anothet useful one, referring to their roles in causing
normal behavior is the distinction between elementa l and tuning reflexes; the
fonner cause the basic sequences, th e
laller adjust to momentary conditions.
Sherrington sta ted the concept of the
reflex, one of the truly great and fruitful
abstractions in biology, with these
words: "The Ullil reae/iOIl hi l1erVOU5 integraliOlI is the reflex. because every refl ex is an
integrative reaction and no nervous
action short of a reflex is a complete act
of integration" (1906, emphasis his).
Many authors have pointed out the
limitations of the concept or criticized it
as art ificia l, and Sherri ngton, as clearly as
anyone else, emphasized the nonexistence of a discrete circuit insu lated
from others. Nevertheless, the funda-
271
Nociceptor
/
in skin
Figure 7.25
Nociceptors .. nd the polysy n.. ptic p.. thw.. y. An·
other !OCt of inputs impinging on th e motor neuron comc fro m pain and sirn ila r receptors. T he
sign of their aclion is generally excitatory to the
ipsilate ral Aexor a nd con tra lateral exten so r mus·
cles ~nd inhi bito ry to th e ips il ate ral extensors
.m d con tral ateral nexors.
mental usefu lness of recognizing this
category of responses has been amply
proved by th e ins ight that experi ments
based upon it have provided. The refl ex
is a useful abstraction, but we qualify the
bro.."ld sta tement that it is the unit of all
nervous integration: (a) the arousal functions of the reticular activa ting system in
ma mmals cannot be resolved into refl exes, nor can (b) mere sensing, (c)
autochthonous action (arising from
within), or (d ) many instincts.
Familiar examples of the phenomena
under consideration are the stretch
refl ex, the fl exion, crossed extension,
sha ke and scratch (dog) refl exes, the
refl exes of micturition and defecat ion,
,
the pi nna, swallowing, stepping, s neezing, sal iv.ltion, blink, accommodation,
and tonic neck refl exes, placi ng, hopping, and righting reflexes. T hey arc
re.ldy- mad e, un leamed, adapti ve movements, prompt and coordinated . The
coordination is not observed just withi n
each refl ex, which we might ex plai n as a
fi xed pattern, but is observed even when
conflicting refl exes are sti mulated simultaneously, for th ere is al most in va riably a
resolution of the pote nt ia lly maladaptive
conflict or intermed iate action in fa vor of
adaptive selection .lnlOng them. Cooperative interplay is also marked between
sim ple segmental refl exes, long spinal
intersegmental refl exes of foreli mbs and
hind limbs, and coord ination of body,
li mbs, neck, hea d, and eye refl exes, as in
visually guided wa lk ing.
T hough the present account of reflexology necessa rily draws mainly from
ma mmalian literature because lower
forms have been less studied in this
respect, we believe the princi ples
en unciated are probably gene ra I. Jm pl ici t
in the conce pt of refl exes-si nce there is
almost invariably more than one refl ex
util izing a given muscle, and hence more
than one cent ra l mechanism converging
on the sa me motor neurons- is the concept of the fin al common path. The very
ex press ion em phasizes the int egrative
function.
The propert ies of refl exes (see Box 7.2)
and the ru les by which they are used
ma ke the best case for their reali ty and
importance. We have already learned
ma ny of these rules in the exam ples
detailed above. Let li S look furth er at the
ways they com bine.
Separate reflexes may be either compatible or incom patible. The fortner
combine adaptively into compound re~
flexe s. For exa mple, a grav ity refl ex that
Sec tio n V
Stimu lus-Tri ggered RCd cllo ns,
T he O rga nlutio n or Hrncxe5
272
Chap ter 7
In tegration at the Intermediate Levels
keeps a fish u prigh t adds to a ligh t reflex
that keeps the dorsal side toward the
light, so that if light comes from the side,
cert.lin fish tilt to a degree graded
according to the ligh t intensity, the
strength of gravity, and a central evaluation thai multiplies each in put by a
weight ing faclor. The weighting depends
on time of day, temperature, hunger, and
other inputs, such as chemical signal s
associated with food, m echa nica l inputs
that ind icate a 5ubslr,liul1l, and visual
input su fficiently imaged and "understood" to represent a substratum.
Incompatible reflexes are those that
cannot be accomplished at the same
time. If the hind leg reflex to scratch the
back is elicited on one side in a dog and
at the same time the sti m ul us for an
extensor thrust of the same sid e is given,
Box 7.2
Properties of Reflexes
WIMt are the properties of reflexes that mani fest
integration? (a) The th reshold st imulus is very much
de pendent on conditions. (b) Above the th reshold,
gradation of response does not closely correspond with
grJd,ltion of st imulus, (c) If the stimulus is repetit ive,
there is USUJlly a poor correspondence between its
rh ythm and that of the reflex response. (d) Single
afferen t impulses are U511,11ly not adequate; temporJl
summation is usually necessary to el icit a response. (e)
A depressed excitability typically follows a reflex and is
oft en qui te long. (f) Afterdisch.uge, or the prolong.dion
of the motor neuron activity after the cessation of the
stimulus, is ,1 prom inent fea tu re of nl.lny reflexes, as
though the mecha nis m were org,lIlized to com plete a
certai n movement in a controlled W<1y. (g) Spa ti.l lly and
temporally patterned con trol of severa l muscles is
probably involved in .111 reflexes.
the nervous system d oes not release
them both, One o r the other is suppressed, at each moment. Incom pa ti ble
reflexes do not add algebraically or com bine li nearly; instead, s witches or patterned contro l ins ure normally adaptive
interaction. This may show either inhibition or facilitat ion . It is as though the
system were preorganized for useful
m ovements.
The tonic nec k reflexes and a number
of related postural reflexes d ue to
vestibular and proprioceptive input
interact with each other and with phasic
movements as though add ing a bias o r
"tuning" the res ponse to the conditions
o f th e m oment. For example, if a load is
li fted by wrist flex ion, mo re wor k c.1I\ b e
done (stretch reflexes faci lit.1ted) wi th
the head bent down or turned away from
The ti ming of inhibition is coord inated with that of
excit<1tion, as is cleMly seen in the alternating reflexes,
s haking, stepping, .lnd scratching. Even sim ple flexion
and crossed extension reflexes show ch.lfacteri stic
tem poral patterning. (h) Irradiation wi th increasing
intensity of stimulus occurs in some reflexes-for
example, the protective flexion reflex. At th reshold <1
response lll<1y involve a lim ited part of a synergic
muscle group <1cross one joint, but with irrJd i,ltion it
may spre.ld to other joints of the same append,lge, to
other appendages and segmcnt.llievels, to the he,ld and
neck. The spre<1d is generally salt,ltory and is confi ned
strictly to certain Jines or muscle groups. However,
apparently uninvolved muscles m,lY in fact be involved
as objects of inhibition. The possible movements Me
thus cirnllTIscribed in a chM<1cteristic p<1ltern. These
properties help to define reflexes, to bring out thei r
integrative nature, and to emphasize th e centr.ll determination of detai ls of form and timing.
273
tha t Mill, because of the tonic neck refle xes; if the Io.ld is met by wrist extension, the opposite head movements
e nh'lIlce ou tput.
Refl exes Me normally \'/Oven into a n
integra ted f" brie, without s harp li nes.
They Me gr"ded in amplitude by influ ences descend ing from highe r cente rs
and comb ined unde r the ru les of ,l
hie ra rchy. We ca nnot help wondering
whelher the sa me ci rcuits Ihal a re refl ex ly t riggered from Ihe periphery might
be centrally triggered in patterned
sequences.
Hav ing erected this edifice of plausible
ass umptions and conclus ions from
studies of reflexes, we should now raise
the questi on as to wh.,t evidence th ere is
for the centr"l origin of patterned impul se discharge.
VI. CENTI!AllY SCORED
BEHAVIOR: PATTERNING IN
SPACE AND TIME
One way to sta te Ihe fu nction of the
n('rvous system is that it formulales
appropriately pa tte rned messages to
drive the effectors. A core qu('stion in the
study of intermedia te level integrAtion is:
" How is this doner' T he patterni ng in
tim(' may be treated as a more serious
issue than tha i in space. Theoret ica lly it
could a rise in either or both of two W.1YS:
by followi ng (a) timing cues from
peripheral se nsc organs or (b) liming
cues frOIll central pace makers or patt el'll
generators. We may call the second
mecha nism ,I central scor(' to empha size
its potential complexity of detail, its
mod ifiability from outs ide on any given
occas ion, and its reali ty as a slored
progr.un dPdft from external inputs. A
score hdS ti mi ng built in, though subject
•
to exterlld l influen ce; a progr.1Il1 might
have the same, but the te rm ,' pplies also
to cases tha t merely ca ll for reactions,
leaving the tim ing to effectors, trdnsducers, loops, .lnd largely peripher.l l
events.
Instead of a s imple d ichotomy we may
disti nguish several poss ible mecha nisms
(Fig. 7.26). In A, we have a s imple reflex, .
such as a n eye blink, a sWdllow, or a
cough, triggered by a stimulus. Sla rtle
responses media ted by gia nt ribers
belong in this category (see Box 7.3).
Even here the t('mpora l pa Hern 0
messages to various muscles is determined by central pathways and integrative junctions. In B, the re is sensory
feedback from proprioce ptors ea rly
enough to determin e a rh yt hm of recurre nce; a chain refl ex aCCOli nts for frequency, phasing, and amplitude. The
cxtreme case, in E, is purely centra lly
timed, without any immediate feedback.
C a nd 0 are combi ned mechanis ms in
which the central s ponta neity ca n determine the bas ic rhythm but feed back may
alter either the rhythm (C) or only the
details of the expression of the rhythm
(D).
Probably all five mechanis ms a re comilion, though us ually there has not been
enough analysis to be s ure which class
a n activity belongs to. In this section we
are concerned particul.uly with some
examples of C, 0 and E. In each
exa mple, there is permiss ive or essentia l
input from sense org,lIlS that may start or
stop the whole pattern or innu ence the
overall "central exci tatory state," to lise
ShNrington's phrase. This is what lVe
mean by spontan eit y, not that there is
independence of the envi ronment for
permissive conditions, bu t only for triggering the s uccession of ,1(tions. S pontaneous rhyth ms ca n be in nue nced in
I
5~dlon
C~nt '~ lI y
I'.! tln ning in
VI
5c:ored
8~h~y lor:
5p~c~
.and Time
A
B
c
o
E
Fig ure 7.26
Five mechanisms of pattern fOTmulat ion. The three levels of neurons are understood to represent
brJnch ing cha ins in whose functions integrat ive p roperties may a lter the actua l impulses ,md distr ib_
ute them spat ially as well as temporilily to the effectors (bollo"I). A and B are shown with receptors;
C, 0, and E, with spontaneous p<lcema kers giving simple or group dischMges. Band C have proprio cept ive feedback acting on the trigger neuron; D, o nly on the shaping of the pattern. [Bullock, 1961a.)
Box 7.3
Giant Fi bers and Startl e Responses
Striking among the behaviors tha t are merely trigge red
by environmenta l st imuli, but not further guided by
either environmental or propriocept ive inputs, arc the
responses med iated by giant fibers . Giant fibers are
Found in many invertebrate .m imals and fish (see
ChJpter 10). T heir phyletiC d istri bution is scattered Jnd
their st ructures are diverse; hence they a rc likely
correl<1 ted only in func tion, not through evolutionJry or
developmental relationships. BecJuse of this diversity,
the follOWing generalizat ions l1lily have exceptions.
Beciluse of their size they conduct impulses TJpid ly.
Perhaps related to size is the fact that they can have ,1
large divergence rJtio-that is, one giant fiber can excite
mJny other neu rons or muscle fibers . Moreover, the
curren t available for electricJI trJnsmission of the
act ion potenti<l l to downstre,ml neurons is large; electrica l trans mission may be common in these systems. In
all of the adequ,ltely studied C<1ses gi<1nt fiber ac tion
results in rapid, neJrly synchronous, widespread muscle act ivity. Behaviora lly, g iant fibers ordina ri ly fire
only with rather special input requirements; these often
have the ch'Hacteristics we call startle.
The giant axons of sq uid arc the best known of all
nerve fibers. We may briefly review their funct ional
ana tomy (see <1lso Ch,lpter 10, p. 434) and behaviora l
role. The muscles of the mantle of the squ id a re doubly
innerv,lted. Many small mo tor axons From the stellate
g,l1lglion excite rela ti vely few muscle fibers each, and
these slnJIl neurons control the slower movements
involved in respir,l\ion and ordinary swim mi ng. The
single giant fibe r in each of the 6 or 8 stellar nerves on
e,1(h s ide together innervate most or all of the muscle
fibers of the m'11l tle. EJch giant fiber has In,my cell
bodies in a lobe of the g,lnglion and is therefore a fused
syncytium of many Illotor neurons. "The" giant fiber of
the squid is the I<lst, longest, ,md I,lrgest of t he 6 or 8 on
275
Box 7.3
(wlI/'-mud )
c.leh side; these fibers arc properl y thc third~ordcr
g ianis. Their input is from two second-order giant fibers
Ih.lI arise in the viscera l lo be of the bra in, enter the
stell.ltc g.lnglion, and synapse all each third-order giant
fib er in tha t gilnglion. The 8 i.1nl synapses are oneto-one re lays; every input impulse causes an all-orno ne twitch throughou t the mantic, nearly simultaneously, .md a vigorous ejection of water through the
funnel . When a squid is slilflled. it aet iv.lles Ihe g iant
fiber system probolbly Viol the 5ingle bilaterally fused
firs t-order giant unit in the ped.d lo be of Ihe brain. This
unit is .J cornm,llld unit. as ddlncd o n p,lge 279. There is
pro bably no immediate feedback influcndng Ihe opera tion of the giant system.
The gia nt fiber syste m of earthworms consists of two
pd ra llel cha ins of elec tric~!ly coup led segmental COl11mand units: a median fiber and a latera l eledrotonically
coupled pair of fibe rs (see p. 405). These premotor
inle reurons control largely overlapping musculature,
the longitudina l or shortening muscles, plus separate
muscles for the setae of a nterior .lnd poste rior segments. The inputs h.we some labi le overlap. The
median giant is activated by stilrtling stimul i, such as a
vibration or a tap anywhere o n the an terior third of the
worm, and causes anchoring by pro trus ion of setae in
the tail, plus shorten ing, which therefore retracts the
head. The lateral giant pair is activ<l ted by mecha nica l
stim uli in the posterior two-th irds, and causes anchoring of the head end, hence pulling up the tail. Each giant
is the re fore a unique, consistent chain of neurons acting
as a decision unit. The adeqUAte input is from m,my
receptors, dnd redches thres hold only when some su btle
criterio n is met thdt involves ra te of rise, recent history,
s p.ltial pattern, and a centrill excitato ry st.lte.
The crayfish giant syste m hols been more completely
studied, and its circuitry is diagr,ul1l11ed in the sketch.
Ma uthner's fibers in teleosts and .1Cj uatic amphibia
are likewise premotor COllltll<lnd units receiving a large
input from many sources, especially vibrdt ion receptors
(see pp. 30, 106,257, 440). They normally fire only once
o r twice, firsl one side and Ihen the olher, causing the
•
Tactile rBceptors
Anlilacilitating
'h~'r".p""
~,
1L
/
B
","W", ,,,""
'"""'''00'
LG ;---electncal synapses
Lateral giant fiber /
en and iJ responses)
Fast
"
lIexol motor
neulons
/
Rectifying synapse
MG
MOlor gian t cell
FleJ;or musculature
Zucker's dwit for the Tdpid tail nexion of the crayfish.
Schem~ti(' diagrolm of the known elements and ronnl"Ctions
for ph.sic mec hanical 51imuli to abdomen. [Zucker, 1972.1
initial body bend of a s tdrile res ponse. The wea lth and
v<1rie ty of synapses known-on the so ma, axon hillock,
,lI1d large dendrites-sugges t tens of thousands of impulses may arrive per second, during the reaction time
of a single afferent impu lse, representing a high degree
(but perhaps not dtypical for neurons) of integrative
filtering, recognizing. decid ing, .1l1d com manding .
276
occurrence and Frequency both by tonic
input and by higher central levels (e.g.,
by changes of mood).
A. Central Rhythms
and Reflex Modulation
The peripheral or reflex hypothesis fails
to account adequately for respiratory
control of vertebrates. A crucial test, total
deafferentation, leaves a functioning
central system. Similar tests have shown
that many other rhythmic control systems have built-in central scores. The
motor neuron discharge seq uence, which
withdraws the mantle and closes the
valves in a clam, Mya, occurs after deafferentation. The copu latory movements of a praying mantis, the flight
rhythm of insects, the walki ng patterns
of insects and amph ibia, respiratory
movements in insects, beating of the
swimmerets in decapod crustacea, stridulatory singing in crickets and grasshoppers, side-la-side alternation of
longitud inal muscle activity in sharks,
heartbe.1t and gastric mill contro l in
crustacea, and the swimmi ng beal of
jellyfish have been shown with varying
degrees of rigor to be centrally controlled.
A few of these examples deserve more
detailed discussion. But first we should
poi nt out that proprioceptive feedback
functions have also been demonstrated
in nearly all of th em, and in the discussion of centrally patterned motor
output we should attend to the role of
reflexes as well. In studying cases of
oscillatory behavior, as in all considerations of oscillatory phenomena, three
measures always merit notice: frequency
(or the reciprocal of frequency, th c period) of the osci lla tion, amplitude, and
phase of one element of the oscillatory
pattern relative to another. In severa l of
the known centra lly driven beh.wiors,
we can relate the functions of peripheral
feedback to one or more of these pMticular parameters.
Lomsl Flight . One of the most decisive
studies on central rhythms is tha t of
Wilson on wingbeat control in grasshoppers. These ani ma ls will sometimes
fly when the g.1nglia of the head and
abdomen are removed, so that the pattern generator must be present within
the thoracic segments. Th e normal motor
score has been analyzed in such detail
that the temporal sequence and phasi ng
of every motor neuron impulse during
Aight is known. This pattern of motor
neuron discharge can be recognized in
the central stumps of the thoracic nerves,
even after all those"'11erves have been
severed. Isolated thoracic nerve cord
preparations are not spontaneously active in the flight rhythm, but random
electrical st im ulation of the nerve cord
ca n elicit nearly the same pattern as is
found in intact animals during Aight. The
output pattern of deafferented preparations is defi cient in one major respect; it
is low in frequency. The decre.1sed frequency can be ascribed to lack of input
from four stretch receptor cells, one in
the hi nge of each wing. These stretch
receptors discharge when the wing is
elevated. During flight they fi re one to a
few impulses toward the end of the
upstroke in each wingbeat cycle (Fig.
7.27). The number of impulses in the
burst is correlated with wingbeat amplitude, the timing of the burst with wingbeat phase, and the burst repetition rate
with wingbeat frequency -all the measures of a n oscillation. This information,
277
Sec tlo n VI
Cenerall y Scored Behav ior:
l'.IU ern ing in Space and T ime
I
o
I I I I
I
I I I
, I '
'00
I I I
I
I
I I I I
'00
I I I I
I
I I I
, I '
300
I I I
I
I I I
,I
400
Tima (msec)
Fig ure 7.27
Propr iocep tive feedbac k in a fly ing insect. ~nsory dischMges in nerves from the wing and
wing h inge in a locus t, recorded with wires manipul,l ted into the largely eviscerated thoracic cavity of a locust. The top record is of downstroke muscle potentials, which are repea ting ,It the wing-beat frequency. The bottom record is of a sensory (stretch) receptor
from one wing, firing one or two times per wing beat. [Wilson, 1968.J
upon enteri ng the eNS, would be adeq uate to trigger and control the events of
th e next cycle. Appa rently, however, it
does not even signi fi can tly affect the next
cycle. In spite of th is rich detail of information a bout wing position, there is
li tt le input/output correlation except a
relatively long-termed one relati ng average input frequency in th e stretch receptofs to average wingbeat freq uency
•
and ampli tude. Th e ganglion integrates
and smooths the input over several
wingbeat cycles, thereby almost bu t not
quite los ing the phasic informa ti on. The
fil tering process is analogous to th e
smoothing and integration in a resistance-capacitance electrica l net work.
In su m, locust fli ght reaffercnce primarily plays a role in con trolling the average
excitation of the motor p.l t1ern genera tor,
278
Chapter 7
integrdti OI1 at the intennedidte levels
thus affecting wing beat frequency and
power. It has a very we<lk effect on
wingbeat phase.
An impo rt.l llt lesson to be Je.1!"ned
from this exam ple is thai, even though
one can demonstrate that proprioceptive
input in a rhythm ic syste m fits the requ irements for a refl ex feedback model,
that input may not be necessary for th e
normal pa ttern, and significant information parameters for the peripheral
hypothesis may not even be used in the
normal operation of intact anima ls. They
may be discarded in a filtering process.
to produce th e swimmeret beat command, and the output of a deafferented
or isolated preparation is normal in both
frequency a nd segmental phasing (Fig.
7.29). The known proprioceptive reflexes
cannot even modulate these parameters.
They do, however, modulate th e force of
each st roke, affe cting the velocity a nd
amplitude by influencing the number
and repetition rate of motor impulses
during each cycle-in other words, the
magnitude of the motor discharge.
Swimming ill Slzarks. When many fi shes
swim, the longitudinal musculature of
the two sides contracts in alternate
metachronal waves. If a shark is curarized to the point of total paralysis, motor
output in the segmental nerves may still
result when the anima l is stimulated, but
since no movement occurs there can be
no correlated proprioceptive feedback . In
th is circumstance, bursts of impulses still
issue alternately through contralateral
nerves, but at unusually low frequency.
Proprioceptive input may, as in locusts,
be necessary for ton ic excitation of central state. But in sharks, compMison of
the outputs on the same side in different
segments shows them all to be synchronous. The metachronicity is lost. On
the basis of presently available evidence,
it appears that proprioceptive feed back
is necessary for the phasi ng of outputs in
proper segmental seq uence as well as for
the ma intenance of normal frequency
(see Fig. 10.63).
A superficially quite different category of
centra lly scored pattern is that called up
by com nl.1nd cells, actually just the e nd
of a spectrum of mechanisms that occur
in all degrees. Command units, first
discovered in crayfish, are now known in
many arthropods, annelids, molluscs,
and vertebrates (see Box 7.3, p. 274 ).
Com mand units, or redundant clusters of
similar units, may turn out to be q uite
general. The concept and the term come
from the observation that certain single
un its, upon sti mulation, are capab le of
causing actions rese mbl ing major pieces
of normal behavior. Some c<luse static
postu re, others phasic sequences. In
higher invertebrates, in which they Me
prob<lbly all potentially identifiable, nonidentical s ubsets of com mand cells may
act together to determine the form of the
behavior. Th ey are presumed to trigger
or release the action, not to instruct the
motor neurons in the te mporal patte rn of
their firing; that pattern is alre.1dy preformu lated by other neurons.
The best-known command fi bers in
cf<lyfish are not of extraordinary size, are
not motor neurons themselves, and in
general do not even synapse d irectly on
motor neurons. They are high er-order
Crayfisl! find Lobster Swimmerei Beal. The
abdomina l appendages of decapod
crustaceans also have a metachronal
rhythmic beat. The completely isola ted
abdominal nerve cord can be stim ulated
B. Command Cells
279
interneurons that run through several
ganglia or even the whole length of the
neuraxis. They excite whole motor
systems, small or large, controlling posture or locomotion (Fig. 7.28). They are
found repeatably in different anima ls.
Each is uniquely characterized by position in the nerve cord, axon diameter,
output function, and other properties.
The pattern of output does not depend
much upon command fiber frequen cy or
pattern, and the output may continue
well after the stimulation of the command fiber has ceased.
The command fibers are obviously
labeled lines. The temporal pattern of
activity in each is relatively unimportant.
What is important is which command
fibers are active, since they drive diverse
behaviors. Each command fiber controlling posture of the crayfish abdomen
seems to have unique but overlapping
output fields. Perhaps the severa l fibers
commanding swimmeret beat are also
unique and produce somewhat different
outputs (Fig. 7.29). Whether they do or
not, swimmeret movements can be
differentially controlled by combining
the action of fibers driving the OScillatory
mechanis m with those affecting posture.
Command fibers m.1Y turn motor
system s on or off or bias them for purposes of steering or orientation.
Some giant fibers (see Box 7.3) are
command units- namely, those that are
not motor neurons but interneurons receiving from many small cells. They are
specialized for prompt, synchronous, and
brief action s that do not continue after
the giant fiber stops firing. local sites in
the hypothalamus of mammals, where
stimulation rather reliably triggers characteristic behavior, may represent a
cluster of cells acting as a kind of command cente r (pp. 316-319).
•
CJ
62 /
,
CM10
1
60
0", ,
'
--"\ --7,. . . ---}- -,
- r 63 ,
L. __ ,.
4 1 65 "\ - - ;
66
'75
,; ;
~; 1
74
61
, 67 , , , 73 ,
,, /69 , 71 '>' 72
--.J ~,
68
70
A
B
Figure 1.28
A. A comm and fibe r for posture. This fiber, called CMlO, travels in area
75 of th e circ um eso phageai conne cti ve of the cray fi sh. Wh en stimul ated at
a minimum of 20 sho ch per sec, it release s the "defensive postu re"
shown in H, invol ving stereotyped positions o f all appendage s. This is one
of the stati c, postura l respo nses trigge red by anyone of a small numbe r
(3-5) of sp ecifi c co mmand neu rons; othe rs are dynam ic, rh ythmi c movement s, such as swimmere! beat ing (e). [l'art A, Wiersma, 1958.J
280
Command neuron
Ch"pter 7
Inte gration at the Inte rmed iate Levels
Coordinat ing neuron
~~r-,--~(--___~
~
Fig ure 7 .29
Circu it for swimmer,,! beating in crdyfls h. T he segmentally repeated circuit is connected
both by th e multisegmental command neuron dnd by the intersegmental coordirMt ing neuron tha t controls the ,lelual time relatio ns 0( the wave of beating. [Stein, 1971.]
What sets off a command cell? In
general, we do not knolV, but an informed guess might be that it usually
requires a number of backgrou nd conditions plus some triggering input. This
means it is highly integrative, acts as a
recognit ion un it (p. 236) to detect these
criteria, a nd is therefore a decision unit
(p. 238) in a significant sense. The input
it requires may come fro m sense organs,
but in some cases it seems likely that
centrally a risi ng changes in mood or
re.ldiness might do the same th ing (see
vacuum activity, p. 315, central sponta neity, p. 325).
C. Hierarchical Structuring
of Molor Systems
If rhythmic motor output can be driven
by nonoscillatory impu lse trains in the
command fibers, where does the oscilla-
tion arise? Cou ld it be due to interactions
between the motor neurons? Several
sorts of motor neuron interaction a re
known . Mutual excitation and reciprocal
inhi bition between motor neurons in the
stomatogastric ganglion of crabs and
lobsters are respons ible, at least in part,
for the way in which the output pattern
of that ganglion rein forces a nd ad justs a
spon taneous rhythm or command fi ber
response (p. 279). Some motor neurons
exciting the same muscle in insects are
electrotonically coupled and tend to fire
together. The sa me is true for contralaterally paired inhi bitory motor neurons
in nervati ng the a bdominal postural
muscles in crayfi sh . Motor neu rons innervati ng th e same flight m uscle in certain flies inh ibit each other. Synergistic
motor neurons in vertebrate spina l cords
are a lso inhibitorily lin ked, throug h
known short-.lxon inte rne urons, the Renshaw cells (p. 269).
281
If interaction between motor neurons
were genera lly responsible for thei r
rhyth mic activity, one might expect that
ant idromic stim ulation of sets of motor
neurons could reset or modify the output
of the whole network. In genefil!, this is
not true. At a more detailed level of
analys is one wou ld expect to find th.lt
intracellular stimu lati on of one motor
neuron would give rise to synaptic potentials in functionally related ones, but
aga in this is not generally true, or else
the effects are quite weak. Current
thought on the matt er is that motor
neuron interactions are usually inadequate to account for the patterns of
output in motor systems.
This concl usion leaves us look ing for
a process, or even a structure, that
mediates between the com mands and the
motor d ischarge itself. The search ison for
interneurona l pacemaker cells or networks th"t produce rhythmicity(Fig. 7.29}.
Cons istent with the notion that there
is a hierMchy in molor systems, with
input co mmands driving osci ll ators that
drive motor neurons, is the fact that the
same set of motor ne urons ca n be used
in more tha n one behavioral pattern.
Frogs swim or jump with synchronous
ou tput to homologous cont ralateral
muscles, bu t alterna te them d uring
walking. Insects use some of the same
muscles to move the wings and legs, but
they do so according 10 different
synergistic/ antagonist ic
relationships,
depend ing upon whether the com mand
says "walk," "jump," "sing," or "fly."
We are pu shed into thinking th"t even in
the lower ga nglia or s pina l cord there is
a mu ltiplicity of p"Uern gener.ltors or
oscillators that can each be turned on or
off or be modul.1ted in frequen cy or .1mplilude by command input, and thai
these pattern generators each converge
upon identical or overlapping pools of
motor neurons. Thus the motor neurons
Me, to use Sherringlon's phr,1se, the
"final com mon paths" transm itting to the
muscles signa l piltt em s th"t are produced at a higher level.
If we turn from a preoccupat ion with
the genesis of rhythm to the question of
how alternative motor patterns that involve higher level switching are selected
and programmed, we have to dea l
mai nly with conce ptual models that
seem compatible with principles of
physiologica l organization.
The rather wide ly accepted notion
today is that actions commanded by
higher centers are not specified in detail
by those centers, nor primarily determined by peripheral stimuli, but triggered in a preprogrammed language
ca lling up combinations of elementary
acts in a hierarchy of levels. The highest
command, as well as the lower-level
instructions to still lower levels, may
simply specify the sequence, strength,
" nd duration of the nex t lower components, finally elicit ing moveme nts as
though the adequate periphera l stimuli
had occurred that can reflexly elicit
them . Ana lysis of six ga its of horses
s hows that they could be produced
simply by ca lling up components eq ual
to certain loca l spinal and long spinal
reflexes in formulat ed sequences and
durations, given a few fixed rules
(Easton, 1972). Whether the horse
actually works this W,lY, we ca nnot tell,
but the !'ul es are simple, and the model
might work. Of course, superimposed on
wha tever "c" lIing up" the bra in initiates,
proprioceptive input as well as visual
and s01llesthelic ]'eafference (sensory
input c"used by one's own actions) wi ll
be important in shaping and correcti ng
the centrally patterned prograJll, by
Section VI
Sco<('d Bth~Yior'
In S p~c ... ~nd Timt
C~"'tr.l.lly
r~tt (' rnlng
2.2
l
!'DI---==+.-----...----''-<G)I----==- L""".
Comma nd
Ton ic
Depressors
Ph asic
(campanlfo rm
se nsi ll a)
E)tci lalory
Inhibitory
A
Feeding
pacemaker
Com po nen ts 01
intri nsic
program
ConUllcUon
c~' ..'''~~
j
S tress ing 01
mechano receptor,
~j,,.;..,
+ .,....
An tagonist
inhi bi tion
Mechanore<:ep tor
activity
B
I-
J
Ret ra cti on 01
buccal mass
Destressi ng 01
mechan'o recepto rs
~
----~~---Delayed nega tive l eedback loop
ending mechanoreceptor bu rst
Positive leedback
loop sustaining
re tra cto r burst
283
s imple adjustments of strengt h and
ph.1Se of pdrticular components.
Motor patterning systems have been
so incompletely s tudied that we kn ow
vel·Y little of th eir actua l mechanisms.
Parti,ll models with some s upporting
evidence ca n be made in many cases.
(Examples are s hown in Figure 7.30 and
in the figure in Box 7.3, p. 275; see also p.
333.) Since it has been so diffi cul t to
ma ke an ana lys is of even relatively sim ple motor syste ms in terms of individual
neuron activities, perha ps we shou ld expect 10 fin d eventua lly Ihat presen lly
un known concepts of neural function are
involved.
D. Centrall y Scored Pattern
by Sensory Tape
Another possible mecha nism of central
programming, besides the motor score,
has been suggested by Hoyle. He calls it
a sensory la pe, or 10 use the phrase of
the ethologists, a sensory templa te (sec
p. 309). Sensory tapes or templates have
not been demonstrated, though strongly
inferred for the control of some bird
song. T he idea is worth more discuss ion.
Suppose the CNS contained an instruction tha t sa id, " Produce a motor output
that results in a s peci fi ed feedback from
Figure 1.30 (f~,iQg ,.~gt )
Circu its for inso:><:t w,ll k ing (A I and sn~i l feedi ng (8). A. Hypothetic .. 1 scheme for the ob5erved d is·
charge pdUerns of levator (5 and 6) and d epressor motor axon s (D). A bursting interneuro n (bi) is
excited by the comm~nd neuron and in lurn excites the levators whi le inhibiting depressor motor
neuron s. The comm,md nber is believed to exc it e the depressor, so t h ~1 ~n incre,lse in command
input decreases int erburst inte rvdl while producing ~ less marked decru se in burst durdtion. Ce rl.lin
se nsory in put toniCollly (.. cilitates the bi ~ nd inhibi ts D; other input ph ..sic.Uy excites D dnd in hib its
bi. [pe.. rson .. nd lies, 1913. 1 D. Diolgr.. m showing the funct iondl interco nnec tions that give rise to Ihe
tempor.. 1 re l.. tions o( dCl ivity in the retr.. ctor .. nd protr.. ctor elements o f the 2S pairs of lIIust tes res ponsible fo r feed ing in the s n.. il Ht/isortllf. The neu rons of the p.Ktm"ker generdte dn .l utonomous
rhythmic output th~t olppeMS with differen t "mounts o f ph ..se shift in the \'o1rio us motor neuron s.
The rhythm is symbo li ~ed by the saw tooth Wolve ~ nd the two represen t,ltive populations of mo tor
neuro ns at the lop of the di,lgr,lIn (upper bra ce, right -hand side of diagram). T he retrdcto r neurons
drive the retractor mu scles. Co nt ract ion in th ese mu scles exo: it es mech~norece ptors, ~nd their ou lput
is fed back pos itively 'lid exc it atory syna pses on the retractor motor neuron s. T his posi tive- feedba<:k
loop (Io\ve r br ..ee, righ t-ha nd side) sust" ins the re tr.. cto r bu rst. Contrdction o f the retractor muscles
p rod uces, ..fter .. de l.. y (due 10 exci t.. tion-contract ion coupling .. nd the Vi5Coel.. ~ic .. oo inert i.. 1 properties of the system), .. retrol("t ion of the bucc.. 1 mdSS. W hen it is retr.acted, cont r.. ction of Ihe muscles
no longe r stresses the mech,Uloro:><:eptors, .. nd th ese shut off; Ihis series of events constitu tes a negati ve-fCi'dback loop wi th deldY, ,md it limit s th e retrdctor burst by ope ning the positive-feedbd ck loop
,1(ler relra ction is comple le (low brdce). The protra clo r motor neurons and mu scles dre excited 011 Ihe
op pos ite phase of the cycle from Ihdt o f retractors. They fire un til in h ibited by inpu t (rom mecl1dIlO.
re cep tors, whi ch Me stretched by the contracting re tractor muscles. This accomp lishes a unidlrec·
Uondl ,m tdgon ist in hibition with de lay, wh ich .. lIows the protract ion ph .. se to be sustained u nt il retr.. ctor tension is developed. Ant.agonist inh ib ition in the re\"('rse d irect ion (i. e., protr.actors in hibiting
retr.lctors) is absent, ~nd thi s allows the O\"erlap ping activity in the two groups of muscles .It the
beginning of the retraction phdse. (Kater and Ro well, 1913.1
,
Se(tlo n VI
Cen trall y Scored Dehulor:
Patterning in Sp.ce a nd Time
264
MOlor ta pes
SenlOlY tapes
In ternal stal e ,..'--''--',
Tape
leleC lo r
Compare
Genera!
d river
Compule ' rom
Specillc
driver
Propriocep tive
afference
Spec ilic
driver
Othe r
"","U
Xp".,
2nd- o rder
driver
Extenso r
A
Jo int
"clues"
-
di fference
285
proprioceptors or other sense organs."
This ins tructi on would not lead inevitably to a sing le s tereotyped motor output, as from a molar score ge nerator, but
it could guide motor out put to achieve a
goal (Fig. 7.31). Ou tput might at first give
in correct results, but feedb<1Ck cou ld
modulate th e output on successive cycles
of loop operation . Consistent with th is
notion of central progra mming by comparison of sensory feedback with a
centrally slored goa l pattern is the fa ct
that diverse motor oUlputs may be associated wit h a pparently identical leg
movements during walk ing in insects. In
some cases the flexors and extensors
alternate. In others, one muscle contracts
tonically whil e the other oscil lates. The
resulting movemcnt is thc same.
T he only reasonably strong case of a
sensory template is found in bird song
control (see Fig. 8.18). In the invertebrate
cases in wh ich a sensory principle may
be operat ive, it seems to be supe rimposed upon a motor score type of
central generator. Insect fli ght is basically
programmed by .1 motor score, but ex teroceptive as well as proprioceptive
inputs can modify that score for purposes of s tability, s teeri ng, or com pensation for inherent error or damage to bod y
paris. Perhaps in these systems the no-
tion of a sensory template n~ ally redu ces
to reflex modulation of a motor score.
E. Coordinated Movement to Gross
Stimulation of the Brain
A clear progression is ev ident if one
compa res the responses to crude electrica l stimulation of s tructures at successive neural levels. Ventral roots give a
segmental, loca l contraction closely related to the duration and strenglh of
stimula tion. Lower motor centers in the
cord or bra in stem give little more,
though the d istribution m.1Y be mOfe
functional (e.g. flexion of certain joints).
The responses relevant to this section are
the quite normal actions involving
sequences of 'movements, s uch as ca n be
elicited from the hypothalamus of
mammals (p. 471). These are so natural as
10 suggest a centra l pattern, si nce the
stimuli are like lightning bol ts. A pocket
mouse may s tuff invisible seeds inlo its
cheek pouches at a high rate, a cal may
arch its back, hiss, unshealh its claws,
erect its hair. The value for our purposes
is the same whether we assume that the
stimuli trigger motor patterns or sensory
" hall ucinations": the patterns are cenlral
and need only an adequate trigger.
Figu re 1.31 Ullting ,111<')
Two types of cont rol by centrally determined seq u('nces. A. System dri ven by sequellces Ih ~t determine motor outp ut directly. Driving comm ~ nds c~n be gener~ 1 or s pecific to dny degree of det.!il,
,md .It a lower level th ey Cd ll be modified by prop ri ocepto rs. B. System drive n by tdpes of se nso ry
feedbdc k th .. t must be expected. A com pd(~to r m .. kcs th e dctl1~ 1 (OIllIllJnds on the bdsis of the
differences between the proprioce ptive dfferenee dnd the inst ruction from the tJpe. Th ere c.. n dlso be
proprioceptive (onlrol lower down, ..s before. Thi~ syslem is more "d"ptdble, bu t requires much
more circui try in dddit ion to d COlll pd ril tor ~nd .. COlllllldnd center, which th('m~I"es musl produce
high ly compleK .Id.l lJlil'e sequences of impulses. Most inverlebr.lte responses inveSlig" tcd usc .I n " inline'" syslem, ,15 in A. IHoyle, 19M. 1
Seell a n VI
Celltrd ll y Score.! Beha vior:
r dtt ern ing in Sp.lce ~ nd Ti me
286
Box 7. 4
Chronology and Background of Ideas on Ihe Ph ysiology of Ihe Nervous System
We present here i\ selection of highlights in the history
o f ide,IS, from the ('.Hlies! till1es up to 1929. The inte rpretation of the brain in terms of cells is highlighted in
Box 3. 1, p. 102. The roots of bra in chemistry, membrane
bio physics, ph,umacology, sensory and psychophysiology, .md be havioral a nalys is arc not attempted
he re.
The redder is urged to look furthe r, fo r more balance
a nd adcquille representation. Some useful, more-or- Iess
conde nsed accounts aTC by Nordcns kiold (1935),
Dampier ( 1948), Singe r (1959), Brazier (1961). Sirks and
Zirkle (1964), Gard ner (1965), Clarke and O'Millley
(1968), and McHe nry (1969). Specia l as pects are dealt
with in FeiHing (1 970), Brazier (1961), and Swazey and
Worden (1976).
1700 B.C. An Egyptian document, transl,l ted centuries later ,lnd published ,lS The Edwin Smi th Surgicdl
Papyrus, includes 13 Cdse descriptions of head injuries.
Aphasia, paralySiS, and seizures were descri bed, and
suggested the fun ct ions of the brain. Nevertheless,
diseolse continued to be generally oltiributed to suprdnaturoll influences olnd whims of the gods.
800 B.C. Homer's works and the flowering of Greek
iHt and intellectua l life led slowly and incomple te ly to
the idea thilt the world is knowilble.
500 B.C. Alcmaeon performed the first recorded
d issection of ,l human body. He p,l id some ,ltiention to
the brain and discovered the optic nerves. His teache r,
Pythagoras, tilught th.t t the brain is conc::erned wi th
reasoning. In the next century more dissections and
similar speculations were made by others.
400 8.C. Hippocr,ltes of Cos countered the mys tics
and the entrenched supranaturalists to introduce rationa l medicine. This requ ired the systematic accumulation of cl inic::al experience, and his desc::ription of
e pilepsy went unsurpassed un til the work of H ughlings
Jackson. However, Hippocratic teaching was dominil ted
by the idea tha t fun ction derives from the combination
of four humors; blood, phlegm, ,lnd black and yellow
bile. The brilin is the org.tn of intelligence .md d re,lms,
but it a lso secretes phlegm OWd cools the blood. Even in
the Gold en Age the Greeks- d id no l easily fo llow his
exam ple. The lack of .lutopsies de l'lyed progress.
340 B.C. Aristotle syste molt k.llly pursued compar,llive an.t to my and in his 19 books set a high wolter mark
of natura l knowledge thilt l.lsted until the RenaisS.lnce,
but he did litt le to change ideas on the bra in.
300 8.(;.
Herophilus and the greilt school of
Alexandria in Egypt dissected many cadavers Jnd really
founded anatomy. He distinguis hed sensory and mo tor
nerves and sho wed tha t they connect from spinal cord
to periphery.
250 8.C . Erisistrat us postulated a mechanis m of the
brain function: blood and two kinds of air arc carried in
the veins, arteries, and nef\'es; air is changed to vita l
spi rits in the hear t and these to animal spirits in the
brain ventricles, whence they go via the nerves to
distend and sho rte n the muscles.
-.
200 6 .C. Galen culminated the classic period, writing
more than 400 works that were dennitive for a
mille nium. By now much of the naked-eye anatomy of
the nervous system had been d iscovered, including
most of the cranial nerves. Among the few advances in
the unde rstanding of function were t he descriptions of
symptoms fo llowing section OInd hemisection of the
spi na l cord in lower mammol ls.
400- 800 The D.uk Ages lasted more than 12
generat ions. Greek knowledge WolS forgotten in Europe.
Men did not ask to unde rstolnd themse lves or nature but
to be told the supra natura l or religious meanings of
things.
600-1200 Islam s pread from Asia minor to Spain,
carrying Gree k knowl edge unknown in the Christian
wo rld. Jewish tfolders introduced Arabic transla tions to
Europe. Long-lost Latin versions of Greek writings were
rediscovered in monastery storeroo ms. Men d id nol ye t
ask abou t nature but Jbout thei r heritage.
]200- 1300 This interest in book learning and the
new wave of ideas induced schol.lSticis m, which in turn
287
110x 7.4
(n",'hilltd)
brought on huma nis m as a redetian. Univers ities sprang
up widely du ring the last period of thc crusades.
HOO- 15OO The inve ntio n of movable ty pe stimula ted p rinting. Voyages o f ex plo ra tion expressed the
new .ttti tud c IOWo1rd d iscovery.
1478 Mo ndino represents the height of dassicill,
dulhoritar i.J[l (Ga lenic) anatomy. His manual, illustra ted
crudely and ascribing func tions such as f,l1l tasy to the
anterior part of the la teral ven tricle, was little influenced
by actual d issection. Nevertheless. it WdS used for 200
fr,Kture sho we d a s ustained para lys is of a rm and leg;
the pOlrOl lysis disappe.ued promptly after surgical removal of iI spicule of bone.
1.730 StE'p hE'n Hales openE'd the d oor to reflex
physiology by noling that the legs of a decapitated frog
would withdraw upon pinching but that s uch "reactions" d isappeared whe n the spinal cord was destroyed. T he terms "stimu lus," "response," "reflex,"
"afferent," a nd "efferent" came into use by the 1770's.
Rohert Whytt (175 1) played an important role in the
drama.
Y C<lTS.
1500 l eonardo da Vinci manifested the new curiosity by making his own dissections and drawing more
accurately th,1n anyone before; but, fai li ng to publish,
he had litt le influence on the progress of .-millomy.
1543
Vesalius broke wilh the tradition of
Aris totelian J nd c..lenic .Julhority, inaugu rating the
mode rn id e.J of the a utho rity of o rigina l observations.
His landmark work, Dr H uma'ii Corporis Fllb rica, conta ins many plates of brain dissectio ns showing nume r·
ous fe.Jture s fo r the fiTst ti me.
1608 Ha rvey WJS the first to reason that the blood
circul.Jtes. He multiplied the c.Jpolcity of the heMt (with
its o ne-w.JY va lves) by the heart rate, both long-known
q uantities. T he met hod of inductive reasoning, lost
since the G reeks, was re-established .
1662 Descartes, the lCiider of 17th-century physio logical thoug ht, crude ly conceived the idea of reflex
action powered by a Galenic mechanism. He broke new
g round also in the mind-body pro ble m, placing the seat
of the soul in the pineal.
1664 T ho mols W illis published o ne of the first
separate wo rks o n the brain, the most complete and
accura te so far, introduci ng several of our current terms.
He suggested tha t the cerebrum presides over voluntary
motions and the cerebellum over involuntary moveme nts; he manipu lated the cerebellum in a living
m.Jmm.J I itnd no ted tha t the hE'oIrt s to pped.
1691 Ro be rt BoylE' pointed to the existence of a
motor cortex. A kn ight suffering a depressed skull
]740 Swede nborg conside red the basal gitl\glia the
seat of primary sensibility of bod y and soul and the
route of "all determinations of the wilL" He d istinguished u pper and lower motor cen ters a nd co rrectly
subdivided the mo to r cortex.
1791 Galvani starled electrophysiology by il\adve rten lly stimula ting the muscles of d issected frog
legs when they completed a circuit with two d issimilar
metals. Volta used the d iscovery of a source of electric
potentia l to develop the battery and voltaic pile.
Ga lvani, mistake nl y believing tha t the poten tial came
from t he tissue, wen t o n to discover bioelectricity by
observing tha t a ne rve is excited when it completes a
circuit betwee n an injured and an un in jured tissue. The
use of a nerve-muscle preparation as a biological
de tecto r, amplifier, and ind icator was an ingenious
physiological tech ni(IUe that permitted the d iscovery of
mi llivolt level bioelect ricity many years before the
g<1lvanometer was invented. Elect ricity came just in ti me
to fill the gap as improved anatom y excluded the
hyd raulic mo del of ne rves and the new physics and
che mistry ra ised do ubts about "a nima l s pirits." T he
s t<1ge was set fo r a r<1tiollal, mechanistic physiology.
·1809 Rolando removed the cerebellum in fish, reptiles, and mamma ls and saw disturbances in volun tary
move ments witho ut influencing sensa ti on .
1822 Francois Magendie made fi rm an eMlie r claim
by Charles Be ll that do rsa l roots are sensory a nd a lso
s howed unequivoca lly that ventral roots are moto r. like
a ll s uch experiments in these pre-anesthesia days, his
work was based on vivisection.
(ColllillJlfd QII
II fXl l!IIg~.)
288
UOI( 7.4
(rOlllj'HIt<I)
1823 Pierre Flourc ns showed that vision depends on
th e cortex; ablatio n on one s ide in pigeons, T,lbbits, and
dogs was found 10 cause contrali1ter,l l blindness.
1826 Johannes Mli ller, wide- rangingGcrmilll natu ra l
philosopher, sensory phys iologist, and ("omp,-u .ltive
anatomist, enunci,lied the " law of specific nerve
energies," which s tates that each sensory nerve gives
rise to its own charilderistic sensatio n, however it is
s timul<l ted . For example, electrical, mechanicdl, or
chemical stimulation of the optic nerve (.luses a sensation of light.
1833 Marshall Hall recogniled segmcntill, intcrsegment<ll, and s uprasegmenlal reflexes. '1"he spinal
cord is a chain of segments whose function.ll units iH C
sep.H.lte reflex arcs which interact with o ne another and
with the highe r centres of the nervous system to secure
coo rdina ted movement" He recognized the tempor.uy
de pressio n of reflexes below a spinal transection and
c,tl le d it s pinal shock.
1848 Du Bois Reymond showed that activity in a
nerve is invMiably accomp.mied by an e lectrica l change
(" negative v<lria tion"). He described the properties of
neurOlnuscul<lr transmissiOn and opposed the prevailing doctrine of vitalism.
1850 Helmho ltz measured the velocity of conduction in nerve tissue and began what would become a
continuing effort to improve the instruments of electrophysiology.
1651 CI.lude BernMd de veloped the la ndm.uk concept tha t the body maintains a consta nt inte rnal e nvironment for the ce lls by means of the extracellular
fluids . Among other things related to sympa thetic function, he described the vasomotor ne rves, which pldy a
ke y part ill this regulation, late r ca lled ho meostas is. An
en thus ias tic e xperimen talis t, he wrote influentially o n
the experilllentdi method, advocating rigo r, con tro ls,
and fo rm uldtion of testable pred ictions.
1861- 1898 H ughlings Jackson, British neu rologist,
developed concepts on the underlying principles of
brain function from cl inica l observa ti ons. One was the
concept of "release" to olccount fo r va rio us signs of
in jury to higher p.uts of the brain, s llch itS s pasticity,
thai a rc more pos itive th,ln negative; the resulting
OVC I·act ivi ty of the s urviving lower centers bespeaks .1
normal restrolint imposed by the higher. A seco nd
co ncept lVds that although e \'olution has been a process
of increased differentioltion and he terogcneity, wi th
integration keeping pace, d isedse reverscs this, such
that higher parts go first and the lower take control. A
th ird concept, growing out of intense stud y of patien ts
with speech d iso rders, those wi th sensory, motor, or
psychic epilepsy ilnd hemiplegi.Js, was that the cortex
has Illany locollized func tions.
1863 Sechenov stud ied " reflexes of the brol in,"
me.lning cerebrol l activity thai .lTises from sensory
st imulat io n and med iates psychic experience and causes
volun tMy action, s ubject to modulation by other bra in
cente rs, incl ud ing inhi bition by the midb rain. This he
obtained by placing salt on the optic lobes. He recognized temporal s ummation of subth reshold stimuli; also
muscle sense, later ca lled proprioception . He emphas ized the physicochemiCdI anollysis of metolbolism and
excitoltion. Trained with CI,lude Bernol rd in Paris dnd Ou
Bo is Rcymond in Be rl in, he is reg.lTded as the father of
Russian physiology.
1865 Pfluge r systcmoltically investi g~t ed inhibition,
mol inly vid a utonomic nerves. Searching fo r inhibitory
nerves to skele ldl muscle, Pa ylov (1885) found the m [n
the fres h-water mussel, AIIQdQrlili. a biva lve mollusc;
Biedermann (1887) found them in the crayfish. They ~re
still unknown in vertebrJ.tes.
1870 Gudde n's find ing th itt s pecific thalamic nuclei
degencrate when certilin areas of the cerebral corte x arc
dcstroyed was a milestone in experimental anatomy, as
well as col iling attention to retrograde degenera tion and
o pening the mode rn period of stud y of the thalamus.
t874 Bartholow, in the U.s.A., stimu),lted and
mapped the motor cortex in man. He fo und, incidenta lly, ihat the brain itself is inse nsitive to manipulolt ing
and cutting.
1875 Richard Caton, in Engl.lIld, observed clec tr ic~l
waves from t he exposed brains of rolbb its dnd monkeys;
289
80)( 7.4
(Wllf;,mrd)
his finding was overlooked, but the waves were rediscovered later in Russi,1 (1877), Poland (1890), .lnd
Austria (1890). Caton IV.lS looking for action potcnti,ll s
ill the ur,lin, inspired by Du Bois Reymond's in nerve,
hoping they would provide a Inelhod for loc.tl izing
sensory arCilS. [n this he succeeded, d iscovering evoked
potentiolls and, inddenlally, DC s hifts with activity, as
well as the ongoing EEG
1898 Lmgley introduced the term "autonomic" ilnd
7 yc,lrS lale r, "sympathetic" and " p.Holsympathelic."
1902 Pavlov, investigating the phys iology of d igestio n, saw clearly the rOild he would follow for 34 years,
analyzing the psychologica] propert ies of conditioned
reflexes. His influence on neurophysiology was "" Imost
nil" (Fu lton, 1949) until recen t yeMs.
1903 Brodm,lnn, Vogt, and Ca mpbell e<1ch made
their first communiutions on the archi tectonics of the
cerebr<1l cortex, m<1pping the dist ribu tion of d ifferent
types of cortiC<11 struclure. It lYas some ye.us, however,
before the 6-layered str<1tificoiltio n lYas fully exploited;
then its embryologic<11 origin lYoiIS e mphasized. By 1929
Ariens K<1ppers and others had ildded a n evolutionary
origin from a primitive 3.I<1yered mantle. Enthusiasm
for the 6·Ja yered structure long delayed a concern for
the neurona l organ iz.ltion and connecti o ns.
1906 Sherrington, in England, published his land·
m.uk treollise, Thf IlIlfgrali vt ATlioll of illt Navolls 51/SItIII,
in which he systematic.llly .malyzed holY the nervous
system works, by close eXolm inoltion of si mple a nd
compound reflexes. Primarily he used mechanical re·
cording of cont raction of individual muscles. Most of
thc ideas on pp. 271-27Z M e his.
1909 Karplus .Ind Kreidl beg.ln the first experi.
ment.ll study of the hypothalamus, their resu lts .lppe.u·
ing in iI long series of papers. Many othe rs joined in,
including Ihe ce lebr.lIed surgeon Harvey Cush ing, who
in 1912 discovered that removal of the pituit.uy or
merel y tr<1nsecting its st.llk c.luses an adi posogenit<11
dystrophy. Nevertheless. the modern period of re·
seMch, in IYhich the hypotha lamus is related to
"utonomic, emotio nal, a nd instinctive functions and the
,
control of the pituitary, did not really begin until the
1930's.
19"1"1
Henry Head and Gordon Holmes, using
psychologic" l concepts ilnd testing, studied sensory
deficits after clinical lesions. They were more concerned
lYi th thc [ldture rather than the locus of cortical sensory
processes in man. They s holYed th.l t the cortex is
especi.,11y involved in discri minat ive "nd higher as pects
of perception. Head is remembered a lso for severing a
nerve in his own ,J.rm to stud y the loss "nd return of
sensation with rcgener,J. tion.
1917 Keith Lucas firmly established the all·or· none
law and quantitative relations in exci tation, such as the
minimal s lope of a slowly riSing current necessary for
excitation.
1924 Kato, in J"P<1I1, sett led a con troversy by show·
ing nondecremental conduction in nerve.
1924 G,J.sser and Erlanger, in the U.s.A., used the
cathode fay osci lloscope to describe the components of
the compound action potential of the whole nerve.
1924 Rudo lph Magnus published his la ndmark
monogrdph on post ure. Starting his investigations 16
years before with Sherrington, he edrly realized the
importa nce of twisting the head on the neck, IYhich
reduces the tonus of posturalmusde and thei r reAexes
o n the side of the forward car in the human or the lower
ear in the dog.
1926 Adridn and Zo\terman recorded from si ngle
scnsory nerve fibe rs and found Iha t, as in motor fibers,
the repet ition rate of impulses is graded. Stronge r
stimuli result in a g reater frequ ency of s pikes.
1929 Denny. Brown recorded from a single motor
neuron ,lctivdled by a n0T1n~1 reflex stimu lus; he used
the stre tch reflex in a decerebrate Cdt.
[929 Berger reported that brJin W.lVes could be
recorded through the skull in humans. After" general
scepticism. this was confirmed by Adri.ln in England
and t,lken up by Davis and othe rs in the U.s.A.
290
Chapler 1
Inleg ra tion al the Inter mediate Levels
SUGGESTED READI NGS
Autrum, H., R. Jung, W. R. Loewenstein, D. M. MacKay, il,o.d H. L Teuber. 1911. Hllndboak of
5'"50/,y Ph ysiology. Sp ringer-Ve rlag. New York. fProjectea to make up e ight volumes, some
in paris, th is will be a comp rehE'ns ive treatise.]
Bach-y-Rita, P., C. C. Collins, and j. E. H yde. 197 1. Tht (,mlral of Eyt MClllfllltIJ/S. Academic
Press, New York. [A symposium on a system es pecial ly favo rable for revea ling principles.
Other mo re recent symposia and reviews can be fou nd on this system. ]
Gr,mit, R. 1970. TIl t BlI5is of M olor Conlro l. Academi c Press, New York. [A systematic ana lys is
from sensory receptors to higher cerebr'!l level s controlling motor neurons.]
G rod ins. F. S. 1963. CD lli rol Tlltory ,wd BitJlogiltl/ SyS/lm $. Colum bi(l Univ. Press, New Yo rk. [A
compact textbook, useful both as an introduction to this (lp prO<lc h a nd to some ins ightfu l
exa mples, which .ue partly neur.ll.!
Horridge, C. A. 1968. 'll/mlll.rou s. W. H. Freeman and Company, S.lIl Francisco. [A collection
of diverse exa mples of neuf;11 mec ha nisms that involve interneurons a t several levels of
analysis. ]
Reiss, R. F. 't964. NlUrtll TlltDI'y ami M odtling (Proc. t962 Ojai Synlpos ium ). Stanford Univ.
Press, Sta nfo rd. [A sym posium combining ex peri me ntal a nd theore tical trea tmen ts o f
examples of sensory and motor beh.lvior. [
""'Schmi tt, F. 0 ., and F. G. Worden. 1974. Tlt t N furDsrinl(fs: TI,jrd Stu dy PrDgrll lll . (See Suggested
Read ings in C hap ter 8 fo r comments on this and two preced ing volumes in the series.]
Stein, It 8., K. G. Pe.lTSOn, R. S. Smith, ,m d J. B. Redford. 1973. CO Il/rol of pos/u,-e alld LOCDrIl O/iDli .
Plenum Press, New York. ]A symposium includ ing invertebrate and vertebrate sensory,
ccntr,ll, reflex, and rhy thmic control.!
St.uk, L 1968. NfrfrDIDgirlll CDII/ ru/ Sys/rllls: Slrulits ill BiolHgillrniag. Plenum Press, New York.
[Exemplary ,111,l lyses from an engineering ilpproach o f some subsystems controll ing
seei ng and manipulating.]
Wiener, N., and J. P. 5chad~. 1965. Cybmltiirs of Olt Nrrvolls 51/51t lll (Progress in the Br.l in
Resea rch, vol. 17). Elsevier Pu blishi ng Company, Amsterdam. IA lt ho ugh ma n y cha pters
(Ire d ated or mainly of historical interest, the collection exe mplifies how d iverse are the
problems and stages o f p rogress under this rubric. Many modern symposia and articles
are read ily fo u nd, in addition to the journ.l ls whose ti lles Cil rry Wie ner's term.)
Wie rs nlol, C. A. G. 1967. IIII'tr/tbral, Nuvcllts SysltJIl5; Tluir SigllifiCIIll ft fDr MllmmR/iali Nfur".
Vll 1/sivlQgy. Un iv. Chicago Press, ChicJgo. [A sym posium deal ing a t many levels wi th
results relevan t to Ill<lmma li,11l neuro physiology.]