J. exp. Biol. (1978), 73. 29-46
With 10 figures
29
Printed in Great Britain
INTERSEGMENTAL REFLEX COORDINATION BY A
SINGLE JOINT RECEPTOR ORGAN (CB) IN
ROCK LOBSTER WALKING LEGS
BY F. CLARAC, J. P. VEDEL AND B. M. H. BUSH*
Institut de Neurophysiologie et Psychophysiologie du C.N.R.S. - INP. io,
31 chemin Joseph-Aiguier, 13274 Marseille cedex 2
{Received 2 June 1977)
SUMMARY
In the decapod Crustacea, Palinurus vulgaris and Jasus lalandii, the reflex
influences of one particular proprioceptor organ, the coxo-basal chordotonal
organ (CB), on all the muscles operating the proximal and distal joints of the
same leg, have been analysed. The distal end of CB was clamped in fine
forceps mounted on a servo-controlled stretcher, and CB length changes of
2 mm were applied. Motor unit activity of the different muscles was recorded
as electromyograms (EMGs).
1. Two types of proprioceptive reflex evoked by CB length changes have
been investigated: (a) resistance reflexes of the two levator and two depressor
muscles of the same leg segment, the coxopodite, i.e. ' intrasegmental
reflexes', (b) 'intersegmental reflexes' induced in the muscles operating the
proximal (T-C) joint of the same leg, and in all eight muscles of the limb
segments distal to CB.
2. Both levator muscles respond reflexly to imposed CB stretch (which
normally occurs with limb 'depression'), while both depressors respond
during CB shortening (or passive ' elevation' of the leg).
3. Intersegmentally, CB stretch reflexly activates the M-C extensor
muscle, and sometimes facilitates the T-C remotor and C-P bender muscles.
Shortening of the single CB organ of a leg excites one or two tonic motor
units of the T-C promotor and M-C flexor muscles, and also facilitates the
remotor, I-M reductor, and the single stretcher-opener excitatory motoneurone.
4. Some of these muscles, particularly the M-C flexor and extensor
muscles, are also influenced intersegmentally by the resting length of CB,
usually but not invariably in the same direction as for the corresponding
dynamic reflexes.
The role of the CB chordotonal organ is discussed, with particular consideration of its intersegmental reflex influence on the posture of the entire
leg, and on the more complex motor behaviour of locomotion, where it may
be specially significant in coordination of the limb in lateral walking. A
complex picture of both tonic and dynamic, intra- and intersegmental reflex
regulation of the positions and movements of the limb segments, thus
emerges.
• Present address: Department of Physiology, University of Bristol, School of Veterinary Science,
Bristol BSi 5LS, England.
2
KXB 73
30
F. CLARAC, J. P. VEDEL AND B. M. H. BUSH
INTRODUCTION
In relatively complex behaviour involving jointed limbs, all the segments of a limb
operate together. Accordingly, the neural activity patterns underlying such behaviour
presumably comprise more or less synchronous motor commands to several muscles
in different segments. For example, during lateral walking in decapod Crustacea like
the rock lobster, levation of the leg at the coxo-basal (C-B) joint, flexion at the merocarpopodite (M-C) joint, and adduction ('closing') of the most distal (P-D) joint (see
Fig. i), commonly occur together in a trailing leg, and usually in conjunction with
depression, flexion, and P-D abduction ('opening') in the contralateral, leading leg
(Clarac & Ayers, 1977).
Intersegmental relationships are clearly important in such behaviour. Reflex interaction between different segments of a limb has been suggested by experiments
involving joint immobilization during locomotion in crabs (Clarac & Coulmance,
1971). If, for instance, the M-C joint is fixed in an extreme position, the movements
occurring at the C-B joint in the same leg during sideways walking are altered.
Another, more specific, proximally directed, intersegmental reflex action has been
briefly reported in crayfish walking legs (Moody, 1970). Bending or stretching the
carpo-propodite (C-P) joint influences the tonic discharge frequency of a motoneurone innervating the thoracico-coxal muscle receptor, and of others supplying the
coxal promotor muscle, of the same leg.
Recently Ayers & Davis (1977) have demonstrated in the lobster, Homarus atnericanus, that several leg muscles are excited phasically by passive movement of individual
joints in the limb. These reflexes involve almost all walking leg joints, and they distinguish between ' resistance' and ' distributed' reflexes. Resistance reflexes have been
extensively investigated in decapod crustacean limbs (e.g. Bush, 1962ft; Barnes,
Spirito & Evoy, 1972; Vedel, Angaut-Petit & Clarac, 1975). They are mediated by
chordotonal organs at each joint and also the M-C myochordotonal organ (Bush,
1965; Evoy & Cohen, 1969; see also Mill, 1976), and by the single thoracico-coxal
muscle receptor of the basal leg joint (Bush & Roberts, 1968; Bush, 1976, 1977). Like
the analogous vertebrate stretch reflexes, these resistance reflexes tend to resist
passively imposed joint movements, by reflex excitation of motoneurones innervating
the stretched muscles.
The term 'distributed reflex' is used by Ayers & Davis to refer to reflex interaction
between different segments of the same leg. For this type of reflex we prefer the term
'intersegmental reflex', in contrast to the resistance reflex which is an 'intrasegmental
reflex'. These two more general, complementary and essentially morphological,
categories of proprioceptive reflex within individual limbs, can then be used to
encompass other leg reflexes arising from different types of proprioceptor, including
apodeme tension receptors (Macmillan & Dando, 1972) and cuticular stress detectors
(Clarac, 1976). Thus each type of leg receptor mentioned above has now been implicated in intersegmental as well as intrasegmental reflexes (Clarac, 1977). Furthermore,
as will be suggested below (see Discussion section 26), certain mtersegmental reflexes
may be regarded as having a postural role comparable to the homeostatic action of the
more extensively studied 'resistance reflexes'. The latter term, therefore, though
Inter segmented reflexes in rock lobster legs
31
generally used hitherto to denote a particular kind of intrasegmental reflex, should in
future preferably be thought of in a wider functional context.
The present paper, then, reports on an experimental study of both intrasegmental
and intersegmental reflexes, proximally and distally directed, in walking legs of the
intact rock lobster. The widespread reflex influences of one particular proprioceptor
organ, the coxo-basal chordotonal organ (CB), on all the muscles operating the
proximal and distal joints of the same leg, have been analysed. Preliminary accounts
of these intersegmental reflexes have been presented previously (Bush & Clarac, 1975;
Vedel, Clarac & Bush, 1975).
MATERIALS AND METHODS
The rock lobsters Palinurus vulgaris and jfasus lalandii were used in this study. The
animal was strapped with rubber bands dorsal side up in a Perspex dish. This was
filled with cooled sea water, which was maintained throughout the experiment at
about 10 °C by means of a Peltier effect cooling element.
Experiments were usually performed on the fifth (posterior) or fourth pereiopod or
sometimes on the third. The chosen leg was fixed horizontally so as to allow access to
the coxo-basal chordotonal organ, CB, from the dorsal articular membrane of the
coxo-basal (C-B) joint. This soft cuticle was dissected away to expose the receptor
strand distally, where it inserts onto the proximal rim of the coxopodite, between the
anterior and posterior levator muscle tendon insertions.
Before severing the distal attachment of the strand, it was clamped in the points of
fine forceps mounted on a servo-controlled stretcher. This apparatus (Clarac & Vedel,
1971) allowed calibrated sinusoidal length changes to be applied to the CB strand.
Usually CB length changes of 2 mm were applied, this being about 16-20% of the
normal resting length of CB (about 10-12 mm), and well within the normal physiological limits (8-5-16-5 mm in a 700 g Palinurus; our specimens ranged from about
600 to 800 g). The monitored length changes are represented in the bottom trace of
each record, increased C-B length (stretch) being indicated by upward deflexion.
For each reflex studied we repeated the following sequences of CB length changes
(see figures): (i) a single stretch or a single release (sinusoidal function) to compare
two steps of CB length; (ii) a single complete sinusoidal movement, starting with CB
stretch or release, to further characterize the effects of direction of onset of the CB
movement; (iii) four sinusoidal movements to observe the effect of a repeated stimulation.
Motor unit activity was recorded as electromyograms (EMGs) in the muscles, or in
occasional fortuitous instances as impulses in the motor axon (e.g. the flexor response
in Fig. 6). A bipolar needle electrode was inserted through a hole in the hard cuticle
into the appropriate muscle, careful positioning being necessary to obtain good
(differential) recordings. In most cases EMG recordings were made from two muscles
simultaneously, in different combinations, though in some experiments three muscles
were monitored simultaneously.
F. CLARAC, J. P. VEDEL AND B. M. H. BUSH
Dorsal view
Meropodite
Propodite
Coxopodite
T-C
CB
Ant. & post.
lei:
prom
Ant. & post.
dep.
red.
ace. flex:
stret.
open.
bend.
clos.
Fig. i. General disposition of the different segments (upper drawing: dorsal view) and joints
(middle drawing: anterior lateral view) of a left third walking leg of the rock lobster, Palinurus
vulgaris. The lower diagram is a schema of the muscles; the joints are represented by rectangles and the fulcra as black dots. Abbreviations of muscles (in this and subsequent figures):
rein. = (T-C) remotor, prom. = promotor; lev. = (C-B) levator, dep. = depressor; red. =
(I-M) reductor; ext. = (M-C) extensor, flex. — flexor; ace. = accessory; stret. = stretcher
(C-P retractor), bend. = bender (= C-P protractor); open. = opener (i.e. P-D extensor or
abductor), clos. = closer (P-D flexor/adductor).
RESULTS
Each walking leg of the decapod Crustacea incorporates six joints (except in the
Astacura which possess a seventh one between the basipodite and the ischiopodite).
They move mainly in two perpendicular planes (Fig. i): movement of the distal
segment of the joint occurs primarily in an antero-posterior direction at the thoracicocoxal (T-C), ischio-meropodite (I-M) and carpo-propodite (C-P) joints, and in a
dorso-ventral plane at the coxo-basal (C-B), mero-carpopodite (M-C) and propodactylopodite (P-D) joints. At the majority of joints the presence of two condyles
limits the movement of the distal segment to one plane only. However, in the rock
lobsters used in these experiments, the C-P joint is also able to rotate slightly (see
Wales et ah 1970).
The different muscles of the leg were systematically investigated. We will first
consider the muscles of the same joint as the CB chordotonal organ, next the proximal
muscles controlling the thoracico-coxal joint, and then all the leg muscles distal to the
CB joint.
Intersegmental reflexes in rock lobster legs
4UW
post lev.
ant. lev.
33
urn
CB
iiiumim
post. dep.
_|_l
ant. dep.
CB
D
+>r-\—hill
3s
Fig. 2. Electromyographic activity recorded in two different preparations of Palinurus,
(A, B) from the two levators (posterior and anterior), and (C, D) from the two depressor
muscles, during reflex activation by imposed length changes of the CB chordotonal organ
strand. (A, C) Four sinusoidal CB length changes; (B, D) one CB stretch (B) and one release
(D), CB length being maintained constant for the remainder of each record. In this and
subsequent figures, stretching of CB is indicated by upward deflexion, releasing by downward
deflexion of the lower traces.
(i) The coxo-basipodite (C-B) joint
This joint is controlled by the limb levator and depressor muscles, which lie predominantly within the coxa but whose proximal portions of the anterior levator and
anterior depressor continue into the thorax (Fig. i). The coxo-basal chordotonal
organ, CB, runs from its distal insertion on the rim of the basipodite between the
anterior and posterior levator insertions, to a special endophragmal peg inside the
dorsal, proximal end of the coxa (Whitear, 1962). It is therefore stretched by limb
depression (at the C-B joint), and shortens with levation.
All four coxal muscles in Palinurus respond to passive, imposed length changes of
the CB receptor strand with classical 'resistance reflexes', similar to those previously
described for the crabs, Carcinus (Bush, 1965) and Cardisomaguanhumi (Moffet, 1975).
Thus both levator muscles respond reflexly to passive stretch of CB, while both
depressors respond during CB release, i.e. shortening (Figs. 2, 3). That is, the functionally synergistic muscles are synchronously excited by CB strand stimulation,
antagonistic muscles being modulated in opposition.
Levator muscles. The number of motoneurones supplying the two levators has been
much discussed because of the role of these muscles in autotomy (Clarac, 1976). This
number appears to vary with the species studied. Bush (1965) and McVean (1974)
F. CLARAC, J. P. VEDEL AND B. M. H. BUSH
3s
Fig, 3. Electromyographic activity recorded from the anterior depressor, posterior levator,
and promotor muscles during reflex activation by CB strand movement in Palinurus vulgaris.
(A) Four sinusoidal CB strand movements; (B) two single sinusoidal movements in opposite
directions; (C) one CB releasing followed by one stretching movement.
described three axons to the anterior levator of the shore crab. In a recent paper
McVean & Findlay (1976) distinguish clearly in these crabs two parts in each levator
muscle: ALM 1 and ALM 2 for the anterior levator, PPLM and RPLM for the
posterior levator. They recorded at least two motoneurones in the rotator part
(RPLM) and two in the PPLM, but one is common to both parts. In Cardisoma
Moffett (1975) described nine units in the anterior levator and two in the posterior
levator. In the rock lobster, the anatomical organization of the levator muscles does
not seem as complex as in the brachyurans. By CB stimulation we have been able to
distinguish only two excitatory units in each levator muscle.
An electrode in the posterior levator records a low-frequency tonic discharge, particularly with CB held stretched (Figs, 2, 3, 9). This resting motor discharge was
strongly modulated by changes in CB length, being increased during stretching and
decreased by release. The posterior levator EMG burst is sometimes at a higher
frequency at the onset of the stretch movement (Figs. 2 A and B), while sometimes it
reaches a maximum frequency in the middle of the stretch curve (Fig. 3). This leaves
open the question of whether the reflex response frequency depends (primarily) upon
the velocity of CB stretch (but cf. Bush, Vedel & Clarac, 1978). A fairly pronounced
facilitation of the EMG response occurs, in close correspondence with the frequency
of discharge (Figs. 2, 3). Most of the time only the tonic unit is recorded; however, if
the animal displays a high level of activity, as indicated by a high discharge rate of
the tonic unit, a second, phasic unit often also becomes active, and this too is modulated by mechanical stimulation of the CB strand.
The anterior levator shows a similar response, but usually at a lower and more
Intersegmental reflexes in rock lobster legs
35
rem.
ant. lev.
CB
D
illlllllMIIIIWJllllllllHlllllllllllllUI
Ill
3s
Fig. 4. Electromyographic activity of the remotor and anterior levator muscles during reflex
activation by CB strand movement. (A) Four sinusoidal CB strand movements; (B) two opposite sinusoidal movements; (C) one CB stretch followed by a CB releasing when T-C is in a
mid-position; (D) one CB stretch followed by a CB releasing with T-C completely promoted.
variable frequency, sometimes with little or no resting discharge (cf. Figs. 2, 4). The
anterior levator discharge is not always completely inhibited by releasing CB (Fig. 4),
though it is always excited by CB stretch. Despite these small differences between the
two levator muscles, it is evident that their reflex activation by CB is nearly identical.
Depressor muscles. Again both anterior and posterior depressor muscles respond
qualitatively similarly to each other, but in opposite sense to the two levator muscles
(Figs. 2C, D; 3 and 5). In contrast to the levators, both depressors showed two active
units, that with the larger EMG spikes being more phasic. Occasional discharges in
additional units were also sometimes seen. In each species studied (Jasus lalandii and
Palinurus vulgaris) the depressor units recorded all responded strongly to CB shortening, and any tonic activity present was greater at the shorter lengths. The larger unit
of both depressors commonly discharged at its highest frequency at the beginning of a
release movement, though in Palinurus (Fig. 3) this was still at a much lower frequency
than the smaller unit. Sometimes the response does not last the full duration of the
movement, particularly after several repetitions (Fig. 3 A).
(2) The proximal, thoracico-coxal joint (T-C)
In Palinura (rock lobsters) the T-C joint is controlled by a single promotor muscle
and two remotors, all situated within the thorax (Fig. 1). The exact number of motoneurones innervating each of these muscles has not yet been clearly determined. There
36
F. CLARAC, J. P. VEDEL AND B. M. H. BUSH
III Mill I
II 111 II I
1
n
i
I I
3s
Fig. 5. Electromyograms from redactor and posterior depressor muscles during various CB
strand movements (as indicated in lower traces).
is also a single muscle receptor organ in this segment, the T-C MRO, lying in parallel
with the promotor muscle (Alexandrowicz, 1967). Stretching this MRO in the shore
crab, Carcinus, causes a reflex discharge in from 1 to 9 motor units of the promotor
muscle (Bush & Roberts, 1968; Bush & Cannone, 1973; Bush, 1976, 1977). In the
present work on rock lobsters, it has not been possible to identify as many motor units
as this in the promotor muscle. Nevertheless several units in the promotor and remotor
muscles are sensitive to CB stimulation.
Promotor muscle. Releasing CB evokes an increase in discharge frequency in at least one
unit of the promotor muscle, while CB stretch completely or partially inhibits this discharge (Fig. 3). A clear modulation is evident when (four) successive sinusoidal CB length
changes are applied (Fig. 3 A). The discharge frequency during releasing is somewhat
variable, and depends markedly upon the direction of the first movement, i.e. whether
this is a stretch or a release (Fig. 3 B). The tonic effect of CB length on this unit is also
much less consistent than that on the motor units of the levator and depressor muscles.
We have occasionally encountered other promotor units sensitive to CB movement
(not illustrated), and in general their frequencies are also accelerated on releasing CB.
Remotor muscle. The number of motoneurones innervating this muscle is not well
defined. Nevertheless one unit is clearly modulated by mechanical stimulation of the
CB strand (Fig. 4), albeit much less prominently than that of the promotor muscle.
Its discharge frequency is enhanced during both stretching and releasing CB. Sinusoidal movement evokes only a small modulation (Fig. 4 A), and appears simply to
cause a general activation of this unit. The influence of CB alone on this unit is in fact
relatively slight, and seems also to depend strongly upon the position of the T-C joint.
When the joint is completely promoted, for example, the remotor unit discharges at a
high frequency, due to the T-C resistance reflex. CB then modulates the remotor
Intersegmental reflexes in rock lobster legs
37
ace. flex. n i ,
II
II
I I I II
I ill
I I
. i
II
I
I I I 11
III
II I
I
1_ 1
1 _! I. l_l 11 II!!! I I J.I
LLJ
III
_ I
iilllnHiliin IIIIIIIIU.... i
I I I II
I
I I I III I
Illl
III
I
I I I II I
11
l
II
I
D
U .|-1 lilllli II • 11 T| | J | r M i l ,
il I IIIII mum HIli
ii iiiiiiinii in inunIIM i
3s
Fig. 6. Simultaneous recordings of electromyograms from accessory flexor, extensor, and main
flexor muscles, during one sinusoidal CB strand movement in opposite directions (A and B),
and during a single CB stretch (C) and release (D). (Note that the single extensor unit was
fortuitously recorded with the same electrode as the accessory flexor unit.)
activity more effectively, facilitating the unit when released and inhibiting it when
stretched (Fig. 4D). Thus, as in the other segments of the limb, the intrasegmental
resistance reflex and the intersegmental reflexes combine to provide a complex regulatory control mechanism.
(3) Joints distal to C-B
The ischio-meropodite joint (I-M)
Only a single muscle (with several muscular heads) controls this joint, the reductor
muscle, which moves the meropodite posteriorly on the basi-ischium (Fig. 1). The
effect of the CB receptor on this muscle is slight, and the resting length of CB does
not appear to influence the reductor motor activity consistently. However, CB shortening usually causes some excitation of a small reductor motor unit, while any tonic
discharge is transiently inhibited by stretching CB (Fig. 5). When, as often occurs in
a lively preparation, the other legs move slowly and rhythmically from the thoracicocoxal joints in an antero-posterior direction, a large phasic reductor unit commonly
discharges in the (stationary) leg under observation. The discharge of this unit,
however, is not modified by CB movements.
The mero-carpopodite joint (M-C)
The meropodite is the longest segment in the leg, and contains the large main flexor
and extensor muscles of the limb and in addition the small 'accessory flexor muscle'
38
F. CLARAC, J. P. VEDEL AND B. M. H. BUSH
A
flex.
111 111 11 I I K I ) | | I | | ( | I I I
i
mi i n II
h d I 111II III I 111 I I I I I Illl I I III 111 1 '
CB
~
m in|in i
' ' ' " "''
Ml
'
|||i||
i
. 11 n II I I
' > ' ' ' ' 'I HI I I i n I II I 1 1 III I I i I I
a
,,niiii h n
i MI 111 i n in
111 inn I i H I inlillillllll I III
i i ii n mi t li mil
l i I n i illlllllllllll M I I H I
r
I I i ii i i i «i i ii Ml ill ililll in i mi hi i n i II mill i in il i inn tin i iiii i'
I I ill I I
I I
I I
I l l l
I
I I II ll 1 I
I I I
I
11 I 1 I I I
I I
3s
Fig. 7. Simultaneous electromyograms from flexor and bender muscles. (A) Four CB strand
sinusoidal movements; (B) two single sinusoidal movements; (C) a single CB release.
(Fig. 1). All three muscles show pronounced reflex responses to CB length changes,
being much more clearly influenced by CB than any of the other limb muscles apart
from the ' intrasegmental' levators and depressors. CB stretch elicits phasic discharge
in a single extensor unit (Fig. 6), while releasing CB excites both the flexor (Figs.
6-8) and the accessory flexor muscle. Stretching the receptor generally also inhibits
the flexor units, while the extensor is inhibited by CB release. These reflexes are
described in more detail in the following paper (Bush, Vedel & Clarac, 1978).
The carpo-propodite (C-P) and propo-dactylopodite (P-D) joints
The muscles of these two joints are much less strongly or consistently influenced
by the CB chordotonal organ. Any reflex effects of CB on these muscles are dominated
and often completely overridden by the much stronger reflexes from the chordotonal
organs of their own joints, and to a lesser extent also by the M-C joint receptors. With
these two distal joints well stabilized, however, the most commonly recorded reflex
influences of CB upon their muscles are illustrated in Figs. 7-8.
The bender muscle (propodite productor) is innervated by two excitatory motoneurones, a 'fast' and a 'slow' unit (Wiersma & Ripley, 1952). The slow unit commonly discharges tonically. Other factors being constant, its tonic discharge frequency
is somewhat greater when CB is stretched than when it is relatively relaxed (Fig. 7).
Rapid CB length changes inhibit this bender unit, CB release being rather more
effective in this than stretch. When the bender discharge is weak, it may sometimes
be completely suppressed by a series of CB movements.
The shared stretcher-opener motoneurone is the only excitatory motor innervation of
these two muscles (the propodite reductor and dactylopodite extensor, respectively),
though each of them receives a separate peripheral inhibitory motoneurone (Wiersma
& Ripley, 1952). Again the influence of CB on this excitor unit is small and variable.
There is usually little effect on its tonic discharge frequency, though this may be
Intersegmental reflexes in rock lobster legs
39
stret.
open,
l l - l l l
flex.
illinium 1
1 mini
- — —
CB
1 1II
1
| 11 [ | 11
II II
—
1II 1 1 1 I I
- I I I Illlllllll
1 1 1 i 1 1 i
•
1 I I I 1 1 11
B
1
*-
! l _ l
J
i
c
iiii
D
1 1 11
1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 11 1 1
II
3s
Fig. 8. Electromyograms of opener (-stretcher) and M-C flexor during CB strand mechanical
stimulation. (A) Four sinusoidal movements; (B) one sinusoidal movement; (C, D) a single
releasing and a single stretch.
11111111111 11111 1 mi
post. lev. -I-UIUIUIUII-U
clos.
CB
||
A
I
3s
Fig. 9. Simultaneous recording of electromyogram for posterior levator and closer muscles,
during (A) one sinusoidal movement of CB; and (B) a single CB release.
slightly greater with CB stretched. Releasing CB, however, sometimes produces a
small but definite excitation of the stretcher-opener unit, whereas stretching CB has
an inhibitory influence (Fig. 8).
The closer muscle (dactylopodite flexor), like the bender, receives both a 'fast' and a
' slow' excitor. As with the bender, there is a tendency for any tonic discharge of the
slow closer unit to be inhibited by CB length changes, in either direction, and also to
be slightly greater when CB is held stretched than when it is relaxed (Fig. 9).
(4) Other legs
All the intersegmental reflexes described so far have been in muscles within the
same leg as the CB organ stimulated. Several recordings from legs other than the
F. CLARAC, J. P. VEDEL AND B. M. H. BUSH
Table i. Summary of CB chordotonal receptor organ influences on the muscles
of a walking leg of Palinurus vulgaris
( + , Excitatory reflex; —, inhibitory reflex effect; ?, no obvious, consistent reflex effect
observed. Numbers of symbols roughly indicate relative intensity of reflex effects.)
Movement of CB
Position of CB
t
Joint
Muscles
T-C
Remotor
Promotor
Levators:
Ant.
Post.
Depressors:
Ant.
Post.
Reductor
Extensor
Flexor
Ace. flexor
Bender
Stretcher
Opener
Closer
C-B
I-M
M-C
C-P
P-D
Stretching
Releasing
CT-
IP
~~
Stretched
j
Released
j
XX+
---
++ +
-
i
+
;
?
-??
(+>
?
r
(+>
stimulated one have not revealed any inter-leg reflex influences of CB. Thus, for
example, CB movement in one leg does not appear to influence either the C-B levator
and depressor muscles, or the M-C flexor and extensor muscles, of the contralateral
leg, or of the next anterior or posterior legs. It may tentatively be concluded, therefore,
that the reflex influences of the coxo-basal chordotonal organ are restricted to the
muscles of its own leg.
DISCUSSION
The present study has shown that both the resting length (position) and change of
length (movement) of the coxo-basal chordotonal organ can modulate the tonic
motoneurone activity of all the muscles of the same limb. Fig. 10 and Table i summarize the reflex actions of CB established in this paper. This constitutes the first
demonstration of multiple intersegmental reflexes mediated by an individual proprioceptor organ in Crustacean thoracic limbs.
(i) Technical constraints
The relatively simple experimental techniques employed in this investigation were
adopted because they offered the possibility of simultaneously monitoring the activity
of two or more muscles with minimal interference to the whole animal. More sophisticated procedures will be required to elucidate the underlying neural mechanisms, and
to establish, for example, whether the CB organ makes direct, mono- or poly-synaptic
connexions with the ' intersegmental' motoneurones, or only indirectly influences
them via secondary reflex loops. Nevertheless, some attempt at interpreting the
present results is warranted, provided certain technical limitations, noted below, are
borne in mind.
Intersegmental reflexes in rock lobster legs
mil. let:
post. lev. 1 1 1
prom.
Fig. 10. Summary of typical electromyographic responses of all the muscles of a rock lobster
walking leg during reflex activation by single sinusoidal movement of the CB strand (CB
stretching indicated by upward, releasing by downward deflexion of monitor traces). Muscle
and joint representation as in Fig. 1.
(a) ' Silent' motoneurones
Extracellular records of motoneurone activity obtained, as here, either indirectly
from the muscles (EMGs) or directly from the motor nerve, clearly give no indication
of any subthreshold influences upon non-discharging motoneurones. The absence of
overt activity in a portion of the excitatory innervation of most of the limb muscles
studied, therefore, cannot be taken to indicate a total lack of influence of the CB
chordotonal organ upon these other, more phasic motoneurones. Some contribution
of this sensory input to the excitability of these other motoneurones seems quite
likely, at least in active, freely moving animals. However, intracellular recordings
from the motoneurones within the ganglia will be necessary to establish this.
(b) Peripheral inhibition
The present experiments also provide no information about the activity of the
peripheral inhibitory motoneurones known to innervate the distal limb muscles of
decapod crustaceans (see Wiersma & Ripley, 1952). This is because it is very difficult
to infer anything about their behaviour from extracellular EMG recordings (but cf.
Bush, 1962 a). It is possible that some of the variation in excitatory junction potential
(e.j.p.) amplitudes encountered in the present experiments was a consequence of
partial suppression by peripheral inhibitor impulses (i.e. a-inhibition: Katz & Kuffler,
1946). However, in most of the present records, the e.j.p. amplitude variation is
broadly explicable in terms of variation in degree of facilitation, due to the manifest
fluctuation in discharge frequency. Nevertheless it remains quite possible, indeed
42
F. CLARAC, J. P. VEDEL AND B. M. H. BUSH
probable, that peripheral inhibitor discharge frequencies are also modulated intersegmentally by CB movement (and by other chordotonal organs in the leg), as in the
intrasegmental resistance reflexes (Bush, 19626).
(c) CB movement compared with joint movement
The CB stimulation imposed by means of forceps is analogous to that elicited by
C-B joint movement when the leg is levated or depressed. In our experiments the
stimulation is limited to the CB organ; the other coxo-basal receptors, namely the
levator and depressor receptors (Alexandrowicz, 1967), and the cuticular stress
detectors, CSD 1 and CSD 2 (Clarac, Wales & Laverack, 1971), are not stimulated.
This (and/or the species difference) could explain the difficulty in reconciling certain
aspects of our results with those of Ayers & Davis (1977) in the astacuran lobster,
Homarus americanus. They found, for example, a positive feedback influence of C-B
joint movement on the levator and depressor muscles. In our experiments on the rock
lobster, however, an inhibition of the motor output to the two depressor muscles
occurs when CB is stretched, and conversely of the levator activity when CB is
released. In some atypical records we observed that the tonic unit of the anterior
levator is not inhibited during CB release, though on the other hand no facilitation of
the discharge was evident either. In Ayers & Davis' preparation, the combined effect
of all the C-B receptors could evoke such a response. Accordingly, the functional
summary presented here (Fig. 10) is not as complex as the relationships described by
these other authors would indicate. This difference might, therefore, be explained by
our much more specific proprioceptor stimulation.
(d) Secondary reflex effects
There exists the further possibility that additional reflex loops may be influencing
the motor responses recorded here. In the experimental arrangement employed, the
leg was clamped in a more or less natural position, with the meropodite roughly
horizontal and the distal segments either fixed or, in some cases, free to move to some
extent. Consequently the motor facilitation or inhibition elicited by CB might, for
example, produce isometric tension changes in some muscles or, as was sometimes
observed, overt movement of the unrestrained M-C (and occasionally more distal)
joints. Such reflex movements could clearly cause secondary resistance reflexes in
these muscles, though these would probably tend, if anything, to reduce the direct
reflex effect of CB.
However, careful comparison of the various intersegmental reflex responses to CB
length changes when the M-C joint moved with those when no overt movement
occurred, shows no significant difference. Furthermore, in several control experiments, the tendon of the accessory flexor muscle was cut, thereby eliminating the
possibility of any secondary reflex loop by this route. Again, the intersegmental
reflexes resulting from CB movement were identical with those obtained when the
accessory flexor was intact. It can therefore be concluded that, in the present experiments, secondary reflex effects via the accessory flexor and associated myochordotonal
receptors did not influence the intersegmental reflexes evoked by CB length changes.
Intersegmental reflexes in rock lobster legs
43
(e) Possible influence of other receptors
Whether the apodeme tension receptors (Macmillan & Dando, 1972) or the
cuticular stress detectors (Clarac, 1976) could also have secondary reflex effects in
these conditions is as yet unknown. Intersegmental reflex influences from chordotonal
organs are certainly known to impinge upon the thoracico-coxal muscle receptor
(Moody, 1970) and the myochordotonal organ (Bush & Clarac, 1975; Bush, Vedel &
Clarac, 1978), so that these two proprioceptors might also contribute secondary reflex
effects. Probably any such actions would be relatively slight, since the observed
intersegmental modulations of motor discharge evoked by CB were on the whole
relatively 'weak' (see below), compared to the intrasegmental reflexes. The possibility
cannot, however, be excluded, and further experiments are needed to clarify this
issue, including, if possible, denervation of the musculature with recording directly
from the motoneurones, or even complete de-afferentation of the limb. Unfortunately
such operations are not only technically very difficult, particularly the latter, but would
probably also be so traumatic as to substantially reduce reflex responsiveness.
(/) EMG recordings and reflex strengths
Comparison of the relative strengths of reflexes cannot readily be made purely on
the basis of electromyograms, since the forces involved depend upon the type of
motor unit activated and the mechanical properties of the joints, as well as upon the
discharge frequencies of the active units. Ideally the muscular forces exerted and their
mechanical effects upon the joints should be measured, but such complex procedures
would undoubtedly seriously impair reflex responsiveness and viability. Moreover,
comparison of the absolute forces exerted by different muscles of radically different
size, shape and power would be of limited value, as these forces could not alone define
relative strengths of the reflex actions of one receptor organ on the different muscles
and joints. A more meaningful comparison is between the reflex actions of different
proprioceptors upon the same muscle - or between the intrasegmental resistance
reflex and other, intersegmental reflex responses of the same muscle (or motoneurones). And since in any one muscle the same one, or two, tonic motor units were
generally the only ones to respond in these reflexes, it seems reasonable to argue that
their discharge frequencies do indeed reflect, at least qualitatively, the relative
intensities, or 'strengths', of the different reflex influences impinging upon that
muscle. This assumption is implicit in the ensuing discussion.
(2) CB receptor influences
(a) Proximo-distal CB control
A priori, it seems likely that CB should affect the muscles of its own joint more
strongly and consistently than those of the other joints of the leg. The present results
are not incompatible with this prediction, although, recognizing the reservations
noted above, they cannot be taken as conclusive evidence for it. Further, CB influence
appears in general to be greater on the next distal joint than on the proximal one:
that is, T-C is evidently less ' strongly' affected than M-C. Moreover, joints moving
in the same plane as C-B are on the whole more affected by CB stimulation than
joints moving in a perpendicular plane: M-C and (to a lesser extent) P-D muscle
44
F. CLARAC, J. P. VEDEL AND B. M. H. BUSH
activity is more modified by CB length and movement than T-C, I-M and C-P. Thus
the predominant intersegmental influence of CB would appear to be upon the M-C
muscles. Furthermore, CB evidently has an antagonistic action on flexor and extensor
muscles, since quite often in these experiments a change in CB length elicited a
clearly observable movement of the M-C joint. In contrast, the reflex effect of CB on
the T-C or C-P joints is not altogether an antagonistic one: the remoter and promotor
muscles are both facilitated on releasing CB. The bender and stretcher muscles seem
to be affected rather more tonically, by CB length, than by its movement: their discharge is in both cases slightly greater when CB is stretched than when it is in the
released condition.
(b) Postural action of CB
As a rule CB affects predominantly the tonic units of the various muscles. It has an
influence on the phasic units, e.g. those of the coxal muscles, only when these are at
the same time involved in a resistance reflex within their own segment. This would
suggest that these intersegmental reflex influences of CB on the other joints of a leg
may be of particular importance in postural control. It is therefore important to
distinguish between the static and dynamic components of these presumed regulatory
reflexes. In the static condition CB is evidently able to regulate the position of all the
joints of a leg. This is not surprising if we consider the location of this chordotonal
organ in the whole limb. It is clearly necessary to have a general adjustment of all the
leg segments in relation to any given position of the C-B joint. A very small modification of the C-B angle evokes postural modification of all the more distal joints. A
strong static reflex connexion between C-B and M-C would therefore seem eminently
appropriate to help maintain a correct posture. The basipodite depressor and meropodite flexor are both anti-gravity muscles, supporting the leg's share of the weight of
the animal. Accordingly they are both influenced in the same (i.e. synergistic) way by
CB position: that is, both these muscles are more excited by CB release (which occurs
with limb levation) and inhibited, centrally at the motoneurones, by CB stretch. These
static, intersegmental reflexes can therefore be considered as an extension of the
intrasegmental resistance reflexes, serving in part to maintain an efficient load distribution between segments, and hence a stable overall posture of the leg.
(c) CB activity and walking
The dynamic reflexes observed may be useful during locomotion. When the animal
is walking sideways, the trailing leg alternately levates and flexes together, then
depresses and extends (Clarac & Ayers, 1977). In this case, the intersegmental reflex
seems efficient (in contrast to the intrasegmental one): CB shortening (which occurs
during levation) reflexly increases the flexor muscle discharge, and CB stretching
(which occurs during a depression movement) increases the extensor muscle discharge. Thus the centrally determined linkage of the motor commands during both
the power stroke (depression-extension) and the return stroke (elevation-flexion) in
the trailing leg is reinforced by the intersegmental reflexes originating in the coxobasal chordotonal organ. For a leading leg, however, levation is synchronous with
M-C extension, and depression withflexion.In this case, the inter- and intrasegmental
reflexes elicited by CB act together, and may possibly strengthen the coupling
Intersegmental reflexes in rock lobster legs
45
between sequential bursts. For example, when the leg is completely elevated there is
facilitation of both the depressor and the flexor muscles by CB, and this could help to
initiate the onset of the powerstroke at the end of a return stroke.
(3) Proprioceptive reflexes and motor patterns
The role of proprioceptive reflexes in motor behaviour has been discussed several
times (e.g. Barnes et al. 1972; Barnes, 1977; Vedel & Clarac, 1975; Clarac, 1977;
Ayers & Davis, 1977). It appears that during a centrally driven movement, the whole
reflex organization is arranged to facilitate it, the opposing neuronal activity being
repressed. If we pursue this hypothesis, the CB reflex interactions in trailing legs
during lateral walking appear more important than those elicited in the leading legs,
except for its possible role in the latter at the end of the return stroke, suggested above.
On the other hand, CB action during backward and forward walking appears less
useful - or at any rate not so readily interpreted in functional terms.
A similar intersegmental reflex, initiated by the receptors of the M-C joint and
controlling the C-B joint, has been described in crabs (Clarac & Coulmance, 1971).
Imposed M-C extension increases the rhythmic variation in discharge of the levator
muscle of a trailing leg, while at the same time extension inhibits the levator motor
discharge of a leading leg. This reinforces the very close functional connexion of these
two joints, C-B and M-C, seen in the present study, and also emphasizes the complexity of the regulatory influence of this class of proprioceptive feedback upon central
motor patterning.
Finally, it must be emphasized that during walking, or any other motor behaviour
involving limb movements or postural adjustments, proprioceptors of all the various
types known in crustacean appendages are presumably activated together. These
include not only the 'pure' chordotonal organs like CB, but also the myochordotonal
organ and T-C muscle receptor, the apodeme tension receptors, and the cuticular
stress detectors (see Barnes, 1975; Clarac, 1977). Further, each of these sense organs
evokes its own characteristic type of reflex, whether from passive or active movements
or force changes. Considering all the reflex interactions demonstrated here or inferred
from previous work, therefore, a highly complex picture of both tonic and dynamic,
intra- and intersegmental reflex regulation of positions and movements of the segments of a limb emerges. These reflex, regulatory controls can be modulated or, in
appropriate circumstances dominated or totally overridden, by central 'commands'
or extrinsic stimuli.
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