A M . ZOOLOCIST, 12:455-469 (1972).
Invertebrate Strategies in Comparative Learning Studies
WILLIAM C. CORNING AND ROBERT LAHUE
Division of Biopsychology, Department of Psychology, University of Waterloo,
Waterloo, Ontario, Canada
SYNOPSIS. Despite the overwhelming variety and abundance of invertebrate species, the
contribution of invertebrate studies to our understanding of the behavioral and
physiological bases of learning has been minimal. Although anthropocentric biases may
be responsible for the inordinate number of studies performed with the usual
laboratory animals, clearly a vigorous extension of the comparative approach in the
behavioral sciences is demanded. Several features of the comparative approach are
outlined and suggestions are made which minimize any of its inherent difficulties. A
multi-level and polythetic approach is proposed which considers multiple characteristics supplemented by evidence obtained at other levels to establish a meaningful
behavioral taxonomy. Controlled systematic variation may be used to analyze the
functional relations of the performance of different species on the same behavioral
task. Another strategy compares simplified and complex versions of the same system in
order to assess the quantitative and qualitative relationships between complexity and
capacity. The structure of many invertebrate species renders them ideally suited to
such analysis. Data on habituation obtained in Limulus polyphemus employing such a
paradigm is discussed. The relationships between electrophysiological habituation and
levels of neural complexity are clearly demonstrated. Future contributions from this
preparation as well as from other invertebrate species are also discussed.
The forgotten majority
tion that derive from the "simpler" animal
model gain validity only through extenInvertebrates comprise approximately sive comparative analyses.
1.1 o£ the 1.2 million existing species in
In spite of the precedents set in the biothe animal kingdom and for that reason logical disciplines, invertebrates remain the
alone — because they exist — a case could forgotten majority in the behavioral
be made for doing research on them. sciences. Since 1950, in the American PsyThere are, however, more compelling rea- chological Association Journal of Comsons. In the physiological and medical dis- parative and Physiological Psychology, less
ciplines, the use of invertebrate data has than 5% of the papers have been concerned
been extensive and has contributed heavily with the invertebrate. This actually repto general concepts of organization and resents a decline from the period 1911function and to our knowledge of patholo- 1948 where 9% of the articles in what
gical processes. Ideally, the general strategy is billed as a "comparative" publication
behind a comparative approach is to take used an invertebrate preparation. There
advantage of physiological variation to ar- are some probable reasons for this disrive at basic concepts (Van der Kloot, crimination. Psychology retains a strong
1967). By studying the diversity of oper- anthropocentrism. Perusal of introductory
ation, mechanisms are frequently more textbook chapter headings supports this,
clearly understood; similarities and differ- e.g., we see chapter headings like "emoences are specified and hypothesized struc- tion," "motivation," "cognition," etc. Analture-function relationships are put to a ogies of these processes are readily seen in
critical test. Frequently, a basic law or con- the rat, pigeon, and primate. Whether they
cept is modified and made more powerful. are homologous with human processes has
The assumptions about higher organiza- yet to be clearly determined, but the popularity of the laboratory subject is probaPreparation of this paper and most of the au- bly dependent upon its ability to display
thors' research reported herein was supported by some sort of human-like behavior. There is
National Research Council grant APA 0351.
455
456
WILLIAM C. CORNING AND ROBERT LAHUE
nothing really wrong with this except that
it is limiting. The conceptual structure
and the categories of inquiry are biased by
the anthropocentrism.*
The lack of a vigorous comparative approach in psychology may account for
some of the vapid definitional schemes.
There is, for example, considerable phylogenetic variation in the capacity to adapt
to environmental perturbations, yet the
learning "laws" fail to clearly distinguish
between levels; most of the basic paradigms are successfully applied at the level
of the flatworm although there are attempts to provide data that qualitatively
differentiate animal groups (Bitterman,
1965). The comparative approach requires
extension and elaboration in the behavioral sciences.
2. The special reaction or bioassay.
Many systems have developed, specific and
highly sensitive reactions to certain stimuli
or agents. To assay for a transmitter
found in invertebrates and vertebrates, the
clam heart is an exceptionally sensitive
system, responding to 10- 12 M acetylcholine in the perfusate. The spider web
of the orb-weaver may turn out to be
useful for screening drugs or assaying for
metabolic products in organisms.
3. Structure-function similarities and
differentiations. Neural systems and other
systems undergo structural and functional
changes during evolution; by examining
the functional capacities of systems that
differ in morphological characteristics, correlations between structures and capacities
may be obtained. There are many examples of this type of comparative approach
General comparative tactics
in vertebrates. For example, Beritashvili
(1971) has recently used this strategy to
There are several reasons for an em- draw correlations between the appearance
phasis upon an essentially comparative ap- of certain structures and certain learning
capacities with particular attention to
proach:
1. The special advantage strategy. To "image-driven" behavior. In invertebrates,
obtain greater control, to apply special there are marked differences in the learntechniques, or to gain more information, ing capacities of coelenterates and flatan animal model or preparation is selected worms and the superiority of flatworms
because of some special advantage. There may be attributable to the appearance of a
are many examples of this strategy in in- concentrated, anteriorly located mass of
vertebrates. Ionic mechanisms in axons neural tissue or brain. There are emergent
were first delineated in the squid giant interests in structure-function correlations
axon, as were the effects of toxins and within certain invertebrate lines —for exother agents on ionic diffusion and trans- ample, the role of the corpora pedunculata
port processes. Presynaptic and postsynap- in the integrative capacities of arthrotic events accompanying reflex commit- pods.
ment and the pharmacology of these
4. Complementary taxonomic data. Freevents can be followed in the giant cells of quently the behavior of a species as well as
molluscs, leeches, and others. Identifiable morphological data can be used to assist
cells that are readily penetrated with elec- in the grouping of species and in tracing
trodes for stimulating and recording make evolutionary derivations. The ethologists,
intercellular integrative and relational of course, have been strong proponents of
properties more easily studied. Optical this view. In the invertebrate, an excellent
properties, transducer mechanisms, and example of how behavioral data aids clasperipheral sharpening processes can be fol- sification can be found in the spider where
lowed in the large lateral eye of IAmulus.
the gross morphology is less differentiat• Tavolga H969) argues that ". . . anv attempt ing between some species than the web
to interpret the behavior of an insect with concepts characteristics.
and methods based on human
psychology
5. Special finding — universal applicabilwould be as ridiculous as attempting a Freudian
ity. An infrequent but always possible ocpsvchoanalvsis of a cockroach (p. 21) ."
INVERTEBRATES AND COMPARATIVE LEARNING
currence in research on organisms is the
discovery of a mechanism or agent that has
some universal application particularly
with respect to understanding and perhaps
preventing some pathological pattern.
This is always a possibility at any level of
research. A recent demonstration of this
possibility has occurred in a less advanced
organism of phylum Schizophyta, E. coli.
Attempts to produce an orientation in an
electrical field and to determine whether
the orientation would persist after current
cessation were unsuccessful; the organisms
did, however, display incomplete mitosis
and grew to great lengths (Rosenberg,
1971; Rosenberg et al., 1969). Cell division
inhibition was traced to a platinum salt
being formed in the medium and subsequent investigations have shown this salt
to be an effective anti-tumor agent in
mammals. Potential therapeutic agents
may also be found in invertebrates or in
the by-products of invertebrate activities
(Nigrelli et al., 1967).
Definitional problems: mulli-levelpolythetic analysis
One of the major difficulties in a comparative approach to behavior is determining whether what appears to be the same
overt behavioral change observed in species of different phyla represents an homologous or an analogous process. As we have
pointed out earlier, the anthropocentrism
in psychology has led us to search for human-like processes in animals. Both the
protozoan and the mammal show the ability to learn, but clearly, the modifications
must be analogies. In researching the
learning capacities and the substrates of
learning in animals, comparisons and
equations of groups always entail the risk
of involving analogies.
Guided by developments in biological
classification as put forth by Sokal (1966),
the idea of a polythetic approach to behavioral classification has been proposed (Jensen, 1967). Rather than rely upon a single
or a few unifying characteristics to define a
particular behavioral category (a mono-
457
tlietic approach), it is argued that a
meaningful behavioral taxonomy is possible only when multiple characteristics are
considered. This provides more information and permits a more quantitative evaluation of similarities and dissimilarities
between animals. For example, if a response decrement observed in two different
animals is to be defined as "habituation,"
the animals are not equated on the basis of
two or three criteria (response decrement,
recovery, dishabituation, etc.). Multiple
characteristics should be considered including the nine that are listed by Thompson and Spencer (1966). Comparisons between species that are based on many dimensions and involve the consideration of
many variables, would lead to a sounder
behavioral taxonomy. This reduces the
probability of the facile equation of one
levels with another with respect to a behavioral process, the error ". . . of calling a
fish whatever swims in the sea . . . and
the error of generalizing from the blood of
a beet to the blood of man because both
are red" (Jensen, 1967, p. 54).
There are some problems with a polythetic approach to behavioral classification particularly if the dimensions of analysis are all derived from one level. The
behavioral data must be supplemented by
evidence obtained at other levels. As an
example of how analogies may prevail in
spite of a multi-dimensional (but single
level) approach, we can point to the rapidly accumulating literature on habituation and mechanisms of habituation in
vertebrates and invertebrates. In Table 1,
a number of different preparations are
listed, all of which demonstrate "habituation." Using some of the generally accepted criteria of habituation as discussed
by Thompson and Spencer (1966) and
Horn and Hinde (1970), it would appear
that all animals possess the same capacity
and that habituation is a process characteristic of all phylogenetic levels. However,
analysis of the mechanisms (or deduced
mechanisms) underlying the response decrement indicates that these are analogous
processes at the various levels, that habitu-
458
WILLIAM C. CORNING AND ROBERT LAHUE
TABLE 1. Habituation criteria* and mechanisms in various species.
Levels
PROTOZOA
Spirostomum
ambiguum
Stentor
coeruleus
Behavioral
criteria*
1, 2, 3, 4,
5, 8,10
A passive intra-cellular diffusion of
ions uncouples contraction from sensory stimulation.
1, 2, 3, 4,
5,8
A recordable electrical prepotential
based in the sensory apparatus diminishes and thus fails to elicit contraction.
COELENTERATA
Hydra
1, 2, 3, 4,
5,8
ANNELIDA
Lumbricus
terristris
1, 2, 3, 4,
5,8
iVereis
pelagiea
1, 2, 3, 4,
7
MOLLUSCA
Aplysia
1, 2, 4, 5,
Limnea
stagnalis
1, 2, 3, 4,
7, 8,11
.LoM^o
vulgaris
1, 2, 4, 5,
8
ARTHROPODA
Procambarus
ciarfcii
1, 2, 8
Procambarus
clarhii
1, 2, 3, 4,
8
Schistocerca
gregaria
1, 2, 3, 4,
8
Gastrimargus
1, 2, 3, 4,
8
VERTEBRATA
eat
1, 2, 3, 4,
5,8
1,2,3,4,
5, 6, 7, 8
* 1.
2.
3.
4.
5.
Possible mechanisms
(Applewhite et al., 1969; Applewhite and Gardner, 1971;
Kinastowski, 1963; Wawrzynczyk, 1937).
1972;
Wood,
(Harden,
1970a,6; (1971).
in motor
pacemakers
Activity
changes, but the modulating mechanism is not known.
(Rushforth, 1965, 1971).
Synaptic failures occur at
sensory to giant and giant
junctions.
Synaptic failures occur at
sensory to giant and giant
junctions.
both the
to motor
1958;
Gardner,
(Kuenzer,
1968; Roberts, 1962).
both the
to motor
(Evans, 1969; Clark, 1960;
Horridge, 1959).
Motoneuron EPSPs decrease in amplitude due to changing excitatory
synaptic efficacy; the decrement
could result from either a decrease
in transmitter release or a decrease
in postsynaptic receptor sensitivity.
Actively incrementing, hyperpolarizing influences upon synaptic efficacy
(inhibition).
Failure of postsynaptic potential to
reach threshold due to an uncoupling
from presynaptie excitation probably
due to decreased mobilization or
utilization of transmitter.
(Pinsker et al., 1969; Kupfermann et al., 1969; Castellucci
et al., 1969).
Decreased transmitter release from
the first presynaptie terminals of the
/3 sensory-lateral giant synapse.
At motor giant to muscle synapse,
labilities in the presynaptie membrane potential or safety factor; unrelated to loss of transmitter.
Tritocerebral visual unit; decrease
thought due to progressive reduction
of available transmitter.
Auditory unit, active collateral inhibition cited as responsible, at least
in part.
(Krasne, 1969;
Krasne, 1969).
A polysynaptic analogue (at inhibitory synapses) of post tetanic potentiation.
An interaction between incrementing
and decrementing influences mediated
by separate neuronal pathways.
(Wickelgren,
1970).
habituation demonstrated
spontaneous recovery
potentiation of habituation
frequency effects
intensity effects
6.
7.
8.
9.
10.
(Holmgren and Prenk, 1961).
(Horn and Wright, 1970).
Wine
and
(Bruner and Kennedy, 1970).
(Horn and Rowell, 1968).
(Rowell et al., 1969).
1967a,6;
Wall,
(Groves and Thompson, 1970).
below zero habituation
stimulus generalization
dishabituation
habituation of dishabituation
missing stimulus
INVERTEBRATES AND COMPARATIVE LEARNING
ation in Spirostomum is apparently different than habituation in the cat. Thus,
while the overt "phenotype" looks to be
the same, the substrates are different.
It is possible that behavioral homologies
may exist across phyla. The development
of particular types of neural networks may
permit the same type of stimulus association and classical conditioning in the planarian as well as the cockroach. The equation of these two different animals can
only be accomplished when there is sufficient information concerning the structure
and the function of relevant systems. Atz
(1970) has provided a most interesting discussion of the problems of applying the
notion of biological homology to behavior
noting that, "The extent to which behavior can be homologized is directly correlated with the degree to which it can be
conceived or abstracted in morphological
terms. Nevertheless, no morphological correlates have ever been found, either in the
nervous system or peripheral structures by
which the homology of behavior can be
established." Current efforts at providing
insights into the "structure" of habituation
may provide a primitive beginning for the
homologizing of behavioral categories.
Phytogeny, complexity, and learning capacity
Phyletic comparisons that reflect true
differences in capacities between organisms
of differing levels are difficult to establish.
Animals differ in sensory and motor apparatus, motivational levels or contingencies that influence behavior are highly
variable across species, and endogenous
factors such as diurnal periodicities and
hormonal production are different; in
short, how is it possible to "equate" animals in a learning task and assess learning
differences? Is it possible to compare meaningfully a reptile and a rat? The approach
taken by Bitterman (1965) promises to be
a useful comparative strategy. Instead of
trying to compare animals on the basis of
such numerical measures as trials to criterion, per cent savings scores, etc., Bitter-
459
man conducted comparative analyses of
functional relations. For example, in a
spatial reversal task it is possible to construct similar capacity tests for both a rat
and a fish. Both animals can be trained to
go to the right or the left side of a twocompartment chamber in order to obtain
some reinforcement. Upon successive reversals of the reinforced side, rats will
demonstrate a decline in the number of
errors while fish maintain a consistent inability to improve performance. It can be
argued that this demonstration of a capacity difference between two species is due to
motivational factors or to other uncontrolled factors. However, one can persist
with the fish for several trials and still fail
to obtain reversal learning. Possible differences in motivation can also be ruled out
by what Bitterman terms control by systematic variation. If hunger, for example,
is critical then there should be a level of
food deprivation that should begin to influence performance. By varying hunger
levels over wide ranges, motivation could
be ruled against and the conclusion drawn
that the difference between a fish and a rat
in spatial reversal learning represents a
qualitative difference in capacity.
Bitterman's research has shown that
there are qualitative differences appearing
with increased phyletic complexity and organization. Another strategy, which permits both quantitative and qualitative assessments of the relationship between complexity and capacity, is to compare simplified and complex versions of the same
system (Lahue and Corning, \97 la,b).
There are many invertebrate species where
this is possible, particularly in the arthropods where ganglia are readily definable
and surgical isolation of various levels of
the central nervous system is easily accomplished. This type of preparation does not
permit any comparisons to be drawn between what are considered less advanced
and more complex phyla but it does permit some assessment of the relationship between neural complexity for degree of
possible neural relationships) and plasticity. The problem of equating different spe-
460
WILLIAM C. CORNING AND ROBERT LAHUE
cies with respect to stimuli, motivation,
and environmental factors is avoided.
Since the receptors and various levels of
neural organization are all within the same
system, inputs can be assumed to be constant for simplified or complex versions of
the system.
The latter approach is possible at all invertebrate levels, including the protozoans.
It may be possible, for example, to compare the habituation characteristics and retention spans of colonial ciliates using
colonies of varying sizes. It is surprising
that more research hasn't been done on
the behavior of colonial protozoans, particularly in light of the earlier findings of
Jennings (1906) and Plavilstchikov (1928).
Jennings demonstrated habituation in
Carchesium to mechanical stimulation
and noted a gradual localization of contraction. At first, when a single subject
was stimulated, the entire colony was observed to contract but as stimulation was
continued more localized contractions were
produced. Plavilstchikov reported associative conditioning in Carchesium. By pairing a change in light wavelength (CS)
with a tactile stimulation (US), Plavilstchikov found that after 100-200 trials, the
responsivity to the light change was increased. Transplantations were carried out
to determine if the altered light responsivity could be "transferred." A portion of
a "trained" colony was grafted to a naive
Intact
Isolated
Ganglion
Half
Ganglion
c:
FIG. 1. Preparations of varying "complexity" in Limulus habituation studies (Lahue and Corning,
} Ventral
Cord
1971a,6).
INVERTEBRATES AND COMPARATIVE LEARNING
461
GROUND
SUCTION
ELECTRODE
AIR
FIG. 2. Arrangement of stimulus (air puff) and suction electrode in Limulus.
host, left for 7-22 days, and then removed.
The remaining "host" was then tested for
any transfer effects and was found to maintain a heightened sensitivity to the light.
Although Plavilstchikov did not incorporate a number of obvious controls in these
studies, they remain a potentially useful
finding that should be replicated. Details
of these and other protozoan learning
studies are available elsewhere (Corning,
1971, 1972; Corning and Von Burg, 1972).
We have recently attempted to assess the
relationship between neural complexity
and the acquisition and retention of a simple form of plasticity in Limulus (Lahue
and Corning, 1971a,fc). The large segmented nervous system of Limulus is easily
dissectable and most ganglia can be readily
localized for lesions or stimulation (Corning and Von Burg, 1968; Corning et al.,
1970; Von Burg and Corning, 1969, 1970).
Since the nervous system is enclosed in an
arterial sheath, perfusion of specified segments is readily accomplished by inserting
a cannula into the sheath and tying it
(Von Burg and Corning, 1971). The
chronic monitoring of heart activity and
nerve activity is also possible, and a simple
chronic cannulation of the pericardial
sinus permits the injection of drugs and
other agents in a relatively unrestrained
intact preparation (Corning et al., 1965).
Interest in the ability of Limulus to
demonstrate some form of behavioral plasticity has only recently developed but
efforts have not been too successful
462
WILLIAM C. CORNING AND ROBERT LAHUE
INTACT (n=14)
100 .
80 .
\
ACQ.
4MIN. RETEST
(•)
\
(A)
60.
\
40 •
\
\
\
S \
•
V
20 ,
Ul
a
Ul
u
80.
\
cc
\
Ul
\
-12 MIN. RET.
(A)
ACQ
(•)
\
\
60 .
\.v
\
40 .
- —
\ .
\l
20.
^•—
\
ulator outputs, and there are both cardioinhibitor and cardioaccelerator units. The
ventral nerves mediate tactile input as well
as gill efferents. Tactile stimulation of the
gill surface will produce a marked increase in dorsal nerve output and a transient inhibition of heart rate. To monitor
dorsal nerve activity, suction electrodes
were used that had a tip opening of 10-15
m/x. Four surgical preparations, schematically portrayed in Figure 1, were used. In
the Intact group, recordings were made in
dorsal nerve units in preparations with a
completely intact central nervous system;
the Ventral Cord group consisted of animals in which the higher brain influences
were removed; in the Isolated Ganglion
group, recordings were made in a single
ganglion isolated from the rest of the system; the fourth group, the Half Isolated
Ganglion, consisted of animals in which
the single isolated ganglion was divided
medially.
•
4
16
28
40
52
' 60 '
160
260 360
VENTRAL(n=15)
00
TRIALS
FIG. 3. Per cent change in unit counts of the
Intact group during acquisition (ACQ) and during
the 4-min and 12-min retests. Single units were
followed in the multiunit recording by using a
Tennelec Window Discriminator to select particular
pulse heights. The per cent change is corrected
for base-line changes. The response to the maximal initial air puff is given a value of 100%.
60 .
\
ACQ.---4 MIN. RETEST
\
(•)
60 •
40 .
(A)
s.
\
\
(Makous, 1969; Smith and Baker, 1960;
Wasserman and Patton, 1969). Previous
work had demonstrated the occurrence of
habituation in light reflexes in intact
preparations, but there was considerable
variability in performance and the procedure took several days (Corning, unpublished; Corning and Von Burg, 1968).
To achieve better control over input
and output modes and to arrive at a
preparation more amenable to the exploration of the physiological mechanisms of
habituation, we have explored the electrophysiological concomitants of habituation
in simplified and complex versions of the
Limulus abdominal ganglia. Each of these
ganglia has two pairs of nerves: dorsal and
ventral. The dorsal nerves carry cardioreg-
20.
\
o
z
x
i-
z
in
o
DC
Ul
. 0 .
a
\
60 .
40 .
20 .
ACQ.
(•)
K
v:
-12MIN. RET.
(A)
\
V..
\
52
60
160 260 360
TRIALS
FIG. 4. Per cent change in unit counts in the Ventral Cord group.
463
INVERTEBRATES AND COMPARATIVE LEARNING
00
ISOLATED (n=14)
80 ,
\
60 .
40 .
V\
\\/
\
ACQ.----4MIN. RETEST
(•)
(A)
^.
20 .
ACQ.- 12 MIN. RET.
(•)
(A)
\
-v\
;\
4
16
28
40
52
60
160 260
all four groups during the first 60 trials
when compared to the same period in the
acquisition phase (Intact, p < .01; Ventral Cord, p < .05; Isolated Ganglion, p <
.05; Half Isolated Ganglion, p < .01).
The initial responses were lower and the
rates of diminution were greater for all
groups during this first retention assessment. In the 12-minute test there was a
slight increase in spike counts in all groups
during the first 60 trials. Comparison of
the counts obtained during acquisition and
those obtained during the first 60 trials of
the second retention test yielded significantly lower scores for the Intact and Ventral Cord groups (p < .02; p < .05, respectively), but the Isolated Ganglion and
Half Isolated Ganglion groups were returning to levels observed during the initial acquisition.
Comparisons between the four groups at
each of the stages are presented in Figures
7 through 9. Statistical tests indicated no
360
HALF [n = 18)
TRIALS
FIG. 5. Per cent change in unit counts in the
Isolated Ganglion group.
Stimulation was effected by delivering a
light puff of air at a specific point on the
gill book surface every 0.73 sec (Fig. 2).
Each preparation received three blocks of
stimulation with 360 puffs delivered during
each block. The first block is designated
as "acquisition," the second as the "4-minute retention test," and the third as a
"12-minute retention test." At the completion of each block, the stimulated point
was given one of three dishabituation stimuli (a drop of water, a stronger puff of
air, or a touch with a blunt probe).
In Figures 3 through 6, comparisons of
the per cent change in unit responsiveness
during the three stages are presented. All
per cent changes are calculated on the basis of the maximal initial response to the
puff and are corrected for base rate shifts.
From these data, it can be seen that most
of the response decrement took place during the first 60 puffs. During the 4-minute
test, there were significantly fewer spikes in
\
ACQ.—-4 MIN. RETEST
(•)
(A)
\
\_.
\\
"' V^K
X
O 100
BO.
\
ACQ.- --12MIN.RET.
(A)
(•)
\
60.
-s
40 .
20.
4
16
2B
40
52
SO
100
260
360
TRIALS
FIG. 6. Per cent change in unit counts in the Halt
Isolated Ganglion group.
464
WILLIAM C. CORNING AND ROBERT LAHUE
ACQUISITION
HANGE
100.,
• — • Intact y
• — • Ventral
-.05
° — ° Isolated
a—°Ha|f
>-
80
-.002
O
LU
60
PER
o
111
40
20
-f-
4
i
16
28
40
52
—i
60
TRIALS
FIG. 7. Comparisons o£ groups during the acquisition phase o£ habituation.
significant difference between the Intact,
Ventral Cord, and Isolated Ganglion
groups during the acquisition phase. However, the Half Isolated Ganglion group did
differ significantly from the Intact (p <
.05) and Ventral Cord (p < .002) groups.
In general, it appears that all but the Half
Isolated Ganglion group were equal with
respect to the initial acquisition of the
habituation. During retention, the more
complex preparations (Intact and Ventral
Cord groups) demonstrated superior retention.
Immediately following the completion
of 360 puffs, a dishabituation stimulus was
applied. This produced dorsal nerve responses that equalled the spike counts obtained when the gill surface was first stimulated ruling against dorsal nerve fatigue
as an explanation for the response decrement. Recordings made from ventral nerve
fiber branches mediating tactile input
show that the repetitive stimulation did
not result in any afferent nerve decrement.
These findings demonstrate that there
is some relationship between neural complexity and retention of an habituated response. Limiting the neural network appears to have less of an effect on acquisition than on retention although the Half
465
INVERTEBRATES AND COMPARATIVE LEARNING
4-MINUTE RETEST
100
•—" Intact
•—'Ventral
UJ
o
Z
-.05
o—o isolated
o—oHalf
80
X
o
\z
60
UJ
o
OC
UJ 40
0.
IUJ
16
28
40
52
60
TRIALS
FIG. 8. Comparisons of groups during the 4-min retest phase.
Isolated Ganglion group was poorer on acquisition. Research can now expand along
vertical (multi-level) and horizontal (polythetic) dimensions to determine whether
habituation in Limulus represents a process that is analogous or homologous to
that observed in other preparations. For
example, recent analyses (Lahue and Corning, unpublished) of frequency effects on
the habituation process have uncovered
another dimension of habituation that others have reported — the "sensitization"
component (Groves and Thompson, 1970;
Hinde, 1970). At higher frequencies, there
appear to be two processes, the first is a
short-lived response increment and the second is the response decrement or habituation. We have also found that deletion of a
stimulus in the train of puffs does not
result in a dishabituation (the "missing
stimulus" effect of Voronin and Sokolov,
1960) suggesting that our decremental process may be different from that in mam-
malian cortex.
We can also readily test certain assumptions about the mechanisms of the decrement to determine the multi-level similarities and dissimilarities with other preparations. Applewhite (Applewhite and Gardner, 1971; Applewhite et al., 1969) has
suggested that in protozoans, acquisition
of the response decrement is due to the
passive diffusion of some ionic species (perhaps Mg2+), whereas recovery from the
response decrement is due to an active
metabolic process. By varying temperature
it was possible to demonstrate that low
temperature did not affect rate of response decrement and that high temperatures speeded recovery. By perfusing the
abdominal ganglia with sea water held at
different temperatures, this particular theory can be tested in Limulus. Other pharmacological agents can also be applied to
the system to assess presynaptic and postsynaptic involvement in the habituation.
466
ivf C. CORNING AND ROBERT LAHUE
12-MINUTE RETEST
100,
•—• Intact
LU
•—• Ventral
(5
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<
>|
.002 X
o—o Isolated
80
a—D Half
X
O
y
gO 60
cc
LU
Q. 40
<
o
LU
20
16
28
40
52
60
TRIALS
FIG. 9. Comparisons of groups during the 12-min retest phase.
out the invertebrate phyla. In protozoans, there are now a substantial number of studies that definitely support the
conclusion that protozoans can habituate. Current polythetic and multi-level analyses offer the hope of a meaningful behavioral and physiological taxonomy for
this phylum. Demonstrations of associative
learning have been controversial and
several paradigms, such as that of Plavilstchikov's, need to be replicated. At the
level of the coelenterate, there is again
little doubt that habituation occurs. The
recent
investigations of Rushforth (1965,
Invertebrate learning: a general outlook
1971) demonstrate this capacity in Hydra
A recently completed invertebrate learn- pirardi and H. viridis, and the rapid acing review (Corning et al., 1972) em- cumulation of electrophysiological and biphasizes the ubiquity of plasticity through- ochemical knowledge of the contractile
We know from preliminary analyses that
certain dorsal nerve units can be specifically affected by certain agents (Von Burg
and Corning, 1971). Acetylcholine appears
to selectively activate cardioaccelerators
whereas picrotoxin releases cardioinhibitors from inhibition. By accelerating or interfering with the effects of presumed
transmitters in the system, a clearer picture
of interneuronal events during the habituation acquisition and retention is possible.
INVERTEBRATES AND COMPARATIVE LEARNING
467
ogy to behavior, p. 53. In L. R. Aronson, E.
mechanisms in Hydra will permit multiTobach, D. S. Lehrman and J. S. Rosenblatt
level comparisons with other species.
[ed.], Development and evolution of behavior.
There is also some evidence that associaW. H. Freeman, San Francisco.
tive conditioning is possible (Ross, 1965).
Beritashvili, J. S. 1971. Vertebrate memory. Plenum
Press, New York.
It is in the phylum Platyhelminthes that
most of the basic learning paradigms of Best, J. B. 1965. Behaviour of planaria in instrumental learning paradigms. Anim. Behav. Suppl.
psycho log)' are demonstrated. Planarians
1:69-75.
have the ability to associate light (CS) Biuerman, M. E. 1965. Phyletic differences in learnwith shock (US) and to differentiate being. Amer. Psychol. 15:709-712.
tween a cue that is associated with shock Brunei-, J., and D. Kennedy. 1970. Habituation:
occurrence at a neuromuscular junction. Science
(CS-)-) and one that is not (CS—). For
169:92-94.
example, Jacobson (1967) trained planariCastellucci, V., Ff. Pinsker, I. Kupfermann, and E.
ans to differentiate between light and viKandel. 1969. Neuronal mechanisms of habituabration, pairing one or the other with a
tion and dishabituation of the gill-withdrawal
reflex in Aplysia. Science 167:1745-1748.
shock stimulus. Planarians can also learn
to negotiate maze discriminations, acquir- Clark, R. B. 1960. Habituation of the Polychaete
Nereis to sudden stimuli. I. General properties of
ing discriminations between black and
the
habituation
process.
Anim.
Behav.
white alleys, rough and smooth surfaces,
8:82-91.
and right and left choices (Best, 1965; Cor- Corning, W. C. 1971. Recent learning demonstrations and some biochemical correlates in planarining and Ratner, 1967; Corning and Ricans and protozoans, p. 101-119. In E. Adam
cio, 1970; McConnell, 1966; McConnell
[ed.], Biology of memory. Plenum Press, New
and Shelby, 1970). Operant training tasks
York.
are also successful with the planarian Corning, W. C. 1972. Conditioning and "transfer of
(Best, 1965; Lee, 1963; Crawford and
training" in a colonial ciliate: a summary of the
work of N. N. Plavilstchikov.
Skeen, 1967). A planarian will learn to
enter a tunnel (thereby breaking a photoe- Corning, W. C, J. A. Dyal, and A. O. D. Willows
[Ed.]. 1972. Invertebrate learning. Plenum Press,
lectric beam) in order to turn off a noxNew York. (In press)
ious overhead light. In higher phyla such Corning,
W. C., D. A. Feinstein, and J. H. Haight.
as Annelida, Arthropoda, and Mollusca,
1965. Arthropod preparation for behavioral, electrophysiological and biochemical studies. Science
the demonstrations are equally convincing.
148:394-395.
The basic learning demonstrations and Corning, W. C, R. Lahue, and R. VonBurg. 1970.
a plethora of useful preparations that perEndogenous and exogenous influences on Limuhis heart rhythm. Amer. Zool. 10:303. (Abstr.)
form well in various learning paradigms
are available for multi-level and polythetic Coining, W. C, and S. C. Ratner [Ed.]. 1967. The
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analyses. Thus the raw material for a viaCorning, W. C, and D. Riccio. 1970. The planarian
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tive strategy in invertebrates exists and, as
Molecular approaches to learning and memory.
Academic Press, New York.
evidenced by the progress that is occurring
in various laboratories (for example, that Corning, W. C, and R. VonBurg. 1968. Behavioral
and neurophysiological investigations of Limulus
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Coining, W. C, and R. VonBurg. 1972. Protozoan
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