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Laboratoire de Psychophysiologie, Université de Caen, 14032 Caen Cedex, France; C.R.E.C., 14530 Luc-sur-Mer, France
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ABSTRACT |
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 TOP ABSTRACT ResultsDiscussionMaterials and MethodsREFERENCES |
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;
Benjamin et al. 2000;
Zhang et al. 2003;
Brembs et al. 2004;
Crow 2004). However, there is
a need for other models, with a more complex central nervous system (CNS),
suited to cellular, molecular, and network analysis. For a comparative
analysis of this kind, cephalopod molluscs (cuttlefish, squid, octopuses) are
ideal models: They have developed the most sophisticated CNS of all the
invertebrates and exhibit unexpected behavioral abilities that are sometimes
equal to those of lower vertebrates
(Packard 1972;
Fiorito and Scotto 1992;
Boal 1996;
Boal et al. 2000).
Cuttlefish actively prey upon shrimp and capture them by shooting out their
two tentacles for a strike. This behavior is visually driven in the cuttlefish
(Messenger 1968). It has been
extensively studied in laboratory conditions: A shrimp is placed in a glass
tube in the middle of an experimental tank. The cuttlefish then attacks its
prey but does not obtain it (Messenger
1971,
1973;
Chichery and Chichery 1992;
Dickel et al. 2000). Under
these conditions, Sepia officinalis promptly learns to inhibit the
predatory motor pattern, i.e., the number of capture attempts (tentacle
strikes) decreases with stimulus presentations. Messenger
(1973) clearly demonstrated
that this waning was not the result of motor fatigue or of a temporary
incapacity to make a tentacle strike, and Agin et al.
(1998) showed that it was not
due to nonspecific effects such as stress or "contextual fear"
induced by the manipulation of the experimental apparatus.
Nonassociative learning (habituation), or associative learning (passive
avoidance learning), could contribute to the regulation of the waning of
capture attempts. Habituation is classically defined as the relatively
persistent waning of a response as a result of repeated stimulation that is
not followed by any kind of reinforcement
(Thorpe 1963). Conversely, the
decreased response to repeated stimulation observed in passive avoidance
learning is due to the association of this behavior with consecutive,
aversive, painful stimuli. Messenger
(1973) demonstrated that the
level of striking was significantly lowered when negative reinforcement was
enhanced, and was significantly raised when negative reinforcement was reduced
or when positive reinforcement was given. Because of this, Messenger
(1973) suggested that the
waning of the response of cuttlefish to prawns in a glass tube cannot be
habituation but is, rather, an example of what Thorpe
(1963) terms associative
learning. There are numerous and various sensory receptors in the suckers of
the tentacles (Graziadei
1964). Therefore, the tentacles striking the tube may deliver a
"pain" message to the brain. This pain would then be associated
with the prawns in the tube. However, it could be argued that we are dealing
with a mixture of associative learning and habituation. In fact, cuttlefish
whose tentacles had been removed exhibited a slight waning of attacks. This
could be considered as the result of pure habituation, but we cannot exclude
the possibility of a pain input from the tentacle stumps at every
pseudo-strike. Because the "prawn-in-the-tube" procedure is now
being used to explore the cellular and molecular correlates of behavioral
plasticity (Agin et al. 2001,
2003;
Bellanger et al. 2003), the
precise nature of the task used in cuttlefish should be made clear. One
critical test to distinguish between passive avoidance learning and
habituation, which has not previously been done, concerns a fundamental
empirical characteristic of behavior undergoing habituation, i.e.,
dishabituation, the ability of a strong, extra, or different stimulus to
reverse the habituated response (Groves
and Thompson 1970). In this study, the first three experiments
examine whether the acquired response in the course of training could be
dishabituated. For this, we used two different training procedures and two
different dishabituatory stimuli. The fourth experiment examines whether or
not the repeated application of a brief visual prawn stimulus, one that is
terminated before the cuttlefish can strike, extends attack latency.
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Results |
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TOPABSTRACTResultsDiscussionMaterials and MethodsREFERENCES |
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A schematic view of the experimental procedure is given in Figure 1. Figure 2 shows that the level of striking declined with time. Indeed, the Friedman test revealed that the number of strikes declined with each successive 2-min block (Fr = 27.425, P < 0.001). The Wilcoxon signed-ranks tests confirmed that the number of tentacle strikes declined significantly between the first and fifth 2-min block (Z = -2.539, P < 0.05). These results show a good acquisition of the task at the end of the first five 2-min blocks. By the end of the 10th minute of presentation of the glass tube, the cuttlefish had significantly acquired the task, and so they were given the arousing stimulus (crab). When shown the crab, they promptly exhibited typical characteristics of predatory behavior: prey detection, orientation, chase, frontal positioning with respect to the prey accompanied by ocular convergence, and attempts at prey capture (the crab was removed just before they could seize it). Thirty seconds after the presentation of the crab, the training phase began again with the glass tube. There was no increase in response after the introduction of the crab (2-min blocks T6-T10) compared with the response during 2-min block T5 (Friedman test, Fr = 2, P = 0.849). This means that the additional event did not produce dishabituation of the attenuated response.
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Experiment 2 (spaced training)
A schematic view of the experimental procedure is given in Figure 1. As can be seen in Figure 3, the level of striking declined in the course of training. Indeed, the Friedman test revealed a significant decrease in tentacle strikes at each successive presentation of the glass tube (group E2-1: Fr = 43.231, P < 0.001; group E2-2: Fr = 24.302, P < 0.001; group E2-3: Fr = 23.469, P < 0.001). Post hoc tests confirmed that progressive acquisition of the task occurred over the course of the first six presentations of the glass tube (group E2-1: Z = -3.183, P < 0.01; group E2-2: Z = -2.666, P < 0.01; group E2-3: Z = -2.371, P < 0.05). Since the task had been significantly acquired by the end of the sixth presentation of the glass tube, the arousing stimulus (crab) was introduced into the experimental cuttlefish's tank 29 min 30 sec before the start of the seventh presentation of the glass tube for group E2-1, 15 min before for group E2-2, and 30 sec before for group E2-3.As previously described, cuttlefish that were shown the crab tried to attack it within a few seconds. After the presentation of the crab, cuttlefish from the three experimental groups showed no significant increase in response to the prey enclosed in the tube compared with their response in the previous phase of training: Comparison of the number of tentacle strikes of the sixth, seventh, and eighth training sessions revealed that the presentation of the crab did not produce dishabituation of the inhibition of predatory behavior (Friedman tests, group E2-1: Fr = 1.077, P = 0.584; group E2-2: Fr = 2.722, P = 0.256; group E2-3: Fr = 0.929, P = 0.629).
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A schematic view of the experimental procedure is given in Figure 1. Figure 4 shows that there was a decrease in the number of strikes in the course of the first 10 min (Friedman test; Fr = 23.657, P < 0.001). Significant acquisition of the task was indeed present at the fifth 2-min block (Wilcoxon signed-ranks test; Z = -2.375, P < 0.05). As in Experiment 1, experimental cuttlefish were given the arousing stimulus (flashing light) after the end of the 10th minute of the training phase. In this case, all the cuttlefish showed changes of color over the entire body, with pronounced opening of the pupil, which demonstrated that the flashing light was an effective stimulus. Nevertheless, the number of attempted attacks on inaccessible prawns during 2-min blocks T6-T10 was not greater than in 2-min block T5 (Friedman test, Fr = 9.531, P = 0.09). Therefore, despite the use of an arousing stimulus of another modality, we were unable to produce dishabituation of the inhibition of predatory behavior; for this reason, we did not try the spaced procedure with the flashing light.
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A schematic view of the experimental procedure is given in Figure 1. When shown the shrimp (56x over eight periods of 3 min each), all the cuttlefish tried to capture it within a few seconds (Fig. 5); the shrimp was removed just before they could seize it. Surprisingly, attack latencies gradually decreased from the beginning to the end of the experiment (Fr = 16.592, P < 0.05). The Wilcoxon signed-ranks tests confirmed that the attack latencies declined significantly between the second and eighth period (Z = -2.191, P < 0.05). This experiment showed that removing the prey from the tank immediately after an initial attack did not prevent the cuttlefish from attacking the prey in the 55 subsequent presentations.
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Discussion |
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TOPABSTRACTResultsDiscussionMaterials and MethodsREFERENCES |
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;
Mongeluzi and Frost 2000;
Aoyama and McSweeney 2001). So,
the absence of dishabituation in our experiments cannot be due to chosen
dishabituatory stimuli (crab, flashing light) because an increase in the state
of arousal of the cuttlefish was universally observed with the two stimuli.
Moreover, experimental cuttlefish systematically seized and ingested
accessible shrimps that were offered at the end of the tests. Consequently,
the inhibition of predatory behavior after the arousing events cannot be
attributed to surprise or fear of these stimuli. Second, the difficulty in
demonstrating dishabituation might be due to the point at which the arousing
stimulus is presented in the course of training and subsequent testing
(re-exposure to trained stimulus). In studies with rats, Groves and Thompson
(1970) trained animals to
inhibit startle response to repeated acoustic stimulation, presenting 17
habituation stimuli at 1-min intervals; they reported that the rats showed
recovery of the response immediately after a novel stimulus (flashing light)
given between the 14th and the 15th habituation trial. Rats given a 30-min
session in a running wheel each day over a 20-d training period
(Aoyama and McSweeney 2001)
showed dishabituation immediately after a brief extra event (the application
of a brake or a flashing of the house light) lasting 5 sec, given 20 min 55
sec after the beginning of a free running session. In Aplysia, Marcus
et al. (1988) obtained an
increase in siphon withdrawal reflex 90 sec after the administration of an
arousing stimulus (mild tactile stimulus) given just after habituation (20
habituation stimuli at 30-sec intervals). In Tritonia, dishabituation
of the number of swim cycles (seven habituation sessions, at 4-h intervals, in
which a salt stimulus was delivered to the tail every 2 min) was demonstrated
with a single dishabituatory salt stimulus to the head applied 5 min before
the seventh session (Mongeluzi and Frost
2000). However, in the same organism, massed procedure failed to
produce dishabituation (12 tail stimuli, 10-min intervals, with a
dishabituatory salt stimulus to the anterior body 2 min before the 11th
session (Frost et al. 1996).
In a cephalopod, the squid Lolliguncula brevis, Long et al.
(1989) trained animals to
inhibit the number of escape jets and the production of a chromatophore ring
pattern in response to brief (5-sec) presentations to models of predators.
Dishabituation was examined after habituating the squids to a model shark for
15 trials (1-min intervals) and then presenting a threat stimulus (waving a
hand near the squid) followed by 15 trials of the same shark presentations.
Dishabituation was partially demonstrated. In fact, after presentation of the
threat stimulus, the squids showed elevated ring pattern responses (ring) to
the next several presentations of the model shark, but the effects for escape
jets were not statistically significant.
These studies give us no indication of an optimal time for the presentation
of a novel stimulus and re-exposure to trained stimulus in the cuttlefish. For
this reason, in our experiments, the time at which arousing stimuli were
presented was varied according to conditioning. It is unlikely, therefore,
that presentation of the arousing stimulus and testing were not carried out at
the right time. Finally, the inability to produce dishabituation in our
experiments might be explained by interference of simultaneous sensitization
induced during training. In fact, Mongeluzi and Frost
(2000) reported that
dishabituation was difficult to demonstrate in Tritonia because of
the presence of short-term sensitization induced during habituation training
(Willows and Dorset 1975;
Frost et al. 1996). The
simplest explanation for the occlusion of dishabituation by sensitization is
that the two processes share common underlying mechanisms
(Groves and Thompson 1970).
Could sensitization mask dishabituation of the inhibition of predatory
behavior in cuttlefish? In our opinion, it is highly improbable: Our spaced
training protocol, with a rest period between each training session, allowed
us to test dishabituation when the inhibition of predatory behavior has been
acquired but after recovery from a hypothetical short-term sensitization.
Moreover, several studies have concluded that the processes underlying
dishabituation and sensitization are completely separate
(Rankin and Carew 1988;
Erlich et al. 1992;
Wright et al. 1992;
Sahley et al. 1994). In
Experiment 4, the repeated application of a brief visual prawn stimulus, one
that was terminated before the cuttlefish could strike, did not extend attack
latencies, as expected if habituation were occurring. Instead, these stimuli
decreased attack latencies. This last control, combined with the other
experiments, significantly strengthens the idea that habituation is not a part
of the decrease in responsiveness observed during the prawn-in-the-tube
procedure.
In conclusion, the findings of this study, with those of Messenger
(1973), strongly argue for
associative learning and, more precisely, for instrumental conditioning as a
process of this learning: Acquired behavior is the result of pairing capture
attempts with aversive consequences (tentacle strikes on the glass tube)
(Messenger 1973). And in fact,
the data show a definitive correspondence between the inhibition of tentacle
strike and passive avoidance learning, where the cuttlefish learns to suppress
its predatory behavior in order to avoid punishment. In addition, the fact
that experimental cuttlefish readily seized and consumed accessible shrimp at
the end of the experiment suggests that cuttlefish could tell the difference
between accessible and inaccessible prey. Are the cuttlefish progressively
able to discriminate the glass tube? Could this learning be contextual?
Further work will be required to test these ideas.
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Materials and Methods |
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TOPABSTRACTResultsDiscussionMaterials and MethodsREFERENCES |
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Adult cuttlefish (218-262 mm dorsal mantle length) of both sexes were collected by trawler several miles off the coast of Ouistreham (Northern France). They were, thereafter, housed in individual tanks (80 x 60 x 40 cm) with circulating seawater maintained at a temperature of 15°C ± 1°C. They were fed daily ad libitum with live shrimp (Crangon crangon) and crabs (Carcinus mænas). Cuttlefish showing external scars or not eating regularly were discarded. After an acclimatization period of 3 d, cuttlefish were assigned at random to six different experimental groups. All the cuttlefish were naive at the outset, and each was used only once. Good ethical standards have been followed in the care, housing, and use of the animal subjects in our study.
Procedure
The object of the first three experiments was to discover whether the inhibition of predatory behavior shows dishabituation when using an arousing stimulus in the course of training.
Apparatus
The experimental apparatus was identical to that described by Messenger
(1971,
1973). To allow presentation
of the prey to the cuttlefish for the timed training sessions, a glass tube
containing the prey (five shrimp) was concealed within an opaque plastic tube
and placed in the tank 4 h before the start of the experiment. Training
sessions could then be timed by the gentle removal and replacement of the
plastic cylinder, a process 3-4 sec.
Training paradigms
Two different training paradigms
(Messenger 1973), massed and
spaced, are usually used to study retention of the task in cuttlefish
(Chichery and Chichery 1992;
Dickel et al. 2000; Agin et
al. 2001,
2003;
Bellanger et al. 2003). It is
well known in psychology that spaced training, interposing a rest interval
between multiple training sessions, produces stronger and longer-lasting
memory than does massed training involving the same number of training
sessions (Hintzman 1974;
Tully et al. 1994;
Menzel 1999). We use these two
different procedures (Fig. 1)
to produce first acquisition of the inhibition of predatory behavior and to
examine afterward dishabituation of the response. The spaced procedure was
used to dismiss the effect of a possible short-term sensitization that could
interfere with attempts to produce dishabituation
(Frost et al. 1996;
Mongeluzi and Frost 2000).
Dishabituation stimuli
A novel stimulus, of the same or of another modality than the habituation
stimulus, involving an increase in the state of arousal can be considered as a
candidate for dishabituation (Groves and
Thompson 1970). In cephalopods, the only arousing stimulus
previously used was "waving a hand near the squid"
(Long et al. 1989). We
rejected this stimulus on the grounds that it cannot be consistently repeated,
and that there is a risk of unintentional cueing. We therefore experimented
with two other stimuli: the presentation of a crab (which is specific to the
cuttlefish, since it is among its natural prey) and a flashing light.
Predatory behavior varies depending on the prey, although the first phases of
the attack are the same for both crab and shrimp: visual prey detection,
orientation, chase, frontal positioning with respect to the prey accompanied
by ocular convergence, and attempt at prey capture. With shrimp, prey capable
of a rapid escape, capture is achieved by projection of the two tentacles; in
the case of less mobile prey, such as crab, capture is achieved by jumping on
the prey (Messenger 1968). In
our experiments (Experiments 1 and 2) (Fig.
1), however, the live crab was tied to a thread and, in each case,
was removed just before it could be seized by the cuttlefish. The flashing
light employed as a dishabituatory stimulus in Experiment 3
(Fig. 1) might be considered as
an unspecific dishabituatory stimulus, since it has been widely employed on
different models (Groves and Thompson
1970; Post and von der Emde
1999; Aoyama and McSweeney
2001), but we know that visual modality is much used by cuttlefish
(Messenger 1968).
Experimental design
The final form of the experiment involved five dishabituation protocols,
with different intertrial intervals for the training stimulus, different
intervals between the training stimulus and the novel stimulus, different
intervals between the novel stimulus and the test stimulus, and differences in
modality of the arousing stimuli. In the first experiment
(Fig. 1), we chose the massed
procedure: The opaque plastic cylinder was removed for a single period of 20
min, during which time the prey was visible to the cuttlefish and the number
of strikes was counted. Earlier experiments have shown that the inhibition of
predatory behavior is an acquired response and is stable at the end of the
10th minute of the training phase (Agin et
al. 2003); the chronometer was therefore stopped at the end of the
10th minute, and the cuttlefish (group E1, n = 8) were given the
arousing stimulus (crab). Thirty seconds after the presentation of the crab,
the chronometer was started up again for the last 10 min of presentation
period of the prey in the glass tube; the number of strikes was recorded to
assess the evidence of dishabituation.
In the second experiment (Fig.
1), the spaced procedure was used. The glass tube was presented
eight times, for a period of 3 min, each presentation being separated by a
rest interval of 30 min. During each presentation of the tube, the number of
capture attempts (tentacle strikes) was counted. In earlier studies, we showed
that the inhibition of predatory behavior is an acquired response and stable
at the end of the sixth presentation of the glass tube
(Chichery and Chichery 1992;
Agin et al. 2001). The
experimental cuttlefish were therefore given the arousing stimulus (crab)
between the sixth and the seventh presentation: the first group (group E
2-1, n = 13) exactly 30 sec after being exposed to the training
stimulus (i.e., the sixth presentation of the glass tube), the second group
(group E2-2, n = 9) 15 min before being re-exposed to the training
stimulus (i.e., the seventh presentation of the glass tube), and the third
group (group E2-3, n = 7) 30 sec before re-exposure. In the third
experiment, cuttlefish (group E3, n = 7)
(Fig. 1) were tested with the
same training procedure as in the first experiment, except that in this case,
the arousing stimulus was a flashing light (10-msec duration, 300 lux,
Vareclar M, Alvar Electronic). Because the proposition that habituation could
be related to the visual stimulus presentation per se cannot be excluded, we
tested, in a fourth and last experiment (group E4, n = 10)
(Fig. 1) whether the repeated
application of a brief visual prawn stimulus, one that is terminated before
the cuttlefish can strike, extends attack latency. A live shrimp attached to a
thread was presented to the cuttlefish and systematically withdrawn just after
an initial attack signified by frontal positioning with ocular convergence.
The shrimp was presented seven times at 30-sec intervals over a period of 3
min, followed by a rest period of 30 min. This routine of presentation and
rest periods was continued until eight presentation periods had been
completed, making a total of 56 presentations of the live shrimps. Attack
latencies were recorded throughout the experiment.
Analysis of behavioral data
Experiments 1-3
To verify the acquisition of the task before the presentation of the
arousing stimulus, the acquisition performances within groups were first
evaluated. For Experiments 1 and 3, the number of tentacle strikes was plotted
in 2-min blocks (T1: min 1 + min 2; T2: min 3 + min 4; etc.), and the number
of tentacle strikes was compared within the first five 2-min blocks (T1-T5).
For Experiment 2, the number of tentacle strikes for each 3-min presentation
of the glass tube was plotted, and the number of tentacle strikes was compared
within the first six presentations. Friedman tests were used for multiple
comparisons (Siegel and Castellan
1988). In significant cases, Wilcoxon signed-ranks tests for
matched samples were performed as post hoc tests
(Siegel and Castellan 1988).
To examine a possible dishabituation of the acquired inhibition of predatory
behavior, we tested the amplitude of response to prawn in the glass tube after
the presentation of the arousing stimulus. The number of tentacle strikes
observed after the presentation of the crab (Experiments 1 and 2, blocks
T6-T10 and seventh to eighth presentation of the glass tube, respectively) or
the flashing light (Experiment 3, blocks T6-T10) was compared with the number
observed just before its presentation (Experiments 1 and 2, block T5 and sixth
presentation of the glass tube, respectively; Experiment 3, block T5).
Friedman tests were used for multiple comparisons. In significant cases,
Wilcoxon signed-ranks tests for matched samples were performed as post hoc
tests.
Experiment 4
To verify whether the repeated application of a visual prawn stimulus
extends attack latency, attack latencies were compared within the eight
periods of 3 min. Friedman tests were used for multiple comparisons. In
significant cases, Wilcoxon signed-ranks tests for matched samples were
performed as post hoc tests. Data analyses were conducted with the Systat
software package (version 5.02).
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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1 E-mail veronique.agin{at}unicaen.fr; fax 33-1-31565600.
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