Differential Sensitization, Retention, and ... - APA PsycNET

Journal of Comparative Psychology 1984, Vol 98, No 2,119-130

Copyright 19S4 b> the American Psychological Association, lnc

Differential Sensitization, Retention, and Generalization of Habituation in Two Response Systems in the Blowfly {Calliphora vomitoria) Bernard Thon and Annie Pauzie University of Paul Sabatier, Toulouse, France A cardiac disturbance and a motor response was elicited by the same moving visual stimulus in the blowfly .The habituation of these responses developed at a rather equal rate during stimulus repetition. After a rest period, whereas habituation of motor responses was completely retained, a substantial recovery of cardiac responses was observed. The use of distributed trials helped to dissociate the influence of sensitization and habituation processes on the behavioral outcome. Habituation of motor responses, in addition to a longer retention, appeared to be more easily generalized after a spatial displacement of the stimulus. These data support the hypothesis that habituation processes develop independently in different response systems, even if they have the same sensory input. The faster reversibility of habituation of cardiac responses is discussed with reference to a preparatory function for locomotor behavior.

Habituation has often been viewed simply as the decrement of a given behavioral or physiological response to a particular repeated stimulation. Neurobiological studies, which suggest that response waning results from a synaptic depression located in the underlying stimulus-response (S-R) pathway, have encouraged this reductionistic point of view. However, some studies have shown that the repeated stimulus cannot be dissociated from the entire experimental situation (Clark, 1960; Marlin & Miller, 1981) and that habituation is not only the more or less temporary disappearance of a response within a behavioral repertoire but that it involves a reorganization of behavior in an animal faced with a complex situation (Logan, 1975; Melzack, 1961). A number of ethological studies reveal such a complexity in an apparently simple phenomenon (Balderrama & Maldonado, 1971; Ewert, 1967; Peeke, Avis, & Peeke, 1979; Szlep, 1964). This view has given rise to laboratory studies using multiple response-systems approaches to habituation. Differences in habituation propThe authors thank Michel Cambon for his skillful technical assistance. Requests for reprints should be sent to Bernard Thon, ERA CNRS N° 700, Laboratoire de Psychophysiologie, Universite Paul Sabatier, 118 Route de Narbonne, 31077 Toulouse Cedex, France. 119

erties between response systems were interpreted in physiological terms assuming differential mechanisms responsible for response decrement (Leibrecht & Kemmerer, 1974) or from a phylogenetical point of view (Gubernik & Wright, 1979) or with reference to the biological significance of the studied responses (Thon, 1980). Except for some studies, the interpretation of results is often biased because differences in rate of decrement between responses evoked by different stimuli could result from differences in the parameters of the stimulation. This bias is ruled out when the responses under study are actually released by the same sensory input (Goodman & Weinberger, 1973; Leaton, 1976; Scourse & Hinde, 1973; Thon, 1980). Such a model preparation can be found in the blowfly (Calliphora vomitoria) in which cardiac disturbance and locomotor activity can be recorded in response to a single visual stimulation (Thon, 1980, 1982). In a resting blowfly, the main feature of heart activity is the regular alternation of phases of forward beating (mean duration from 6 s in free-moving flies to 15 s in fixed flies) and of phases of backward beating (mean duration of 14 s in free-moving condition and 28 s in fixed condition) (Medioni & Campan, 1967; Thon, 1976; Thon & Queinnec, 1976). Several sensory stimula-

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tions coming from the animal's environment or from motor feedback induce disturbances of this cyclical activity, which are always described as an inhibition of forward beating of the heart. In case of a visual stimulation by a rotating grating pattern in a tethered fly, an arrest of forward beating is recorded in association with an optomotor response. These behavioral outputs can be displayed simultaneously, but in most cases the cardiac response anticipates the motor response (Thon, 1980). Repetition of the visual stimulation is accompanied by a progressive decrement of both responses, but the likelihood of cardiac response remains always higher than the probability of motor response. During acquisition, habituation appears to be less pronounced (more easily reversible) for cardiac than for motor response. The aim of the present work was to carry on this previous analysis by comparing the properties of retention and of stimulus generalization of habituation of these two response systems. Experiment 1 This experiment was designed to study the spontaneous recovery of cardiac and motor responses following previous habituation to a visual stimulus, in order to compare their "memory" of habituation. Method Subjects Animals were 30 adult Calliphora uomitoria of both sexes from 3 to 7 days old. Last stage larvae were obtained from a local supplier and reared in the laboratory at 25 °C. Recording of cardiac and motor responses. Flies under weak ether anesthesia were tethered by the thorax to the tip of a needle. The electrocardiogram was recorded by means of two stainless steel wire electrodes (0.5 mm in diameter) superficially introduced under the cuticle of the second and third abdominal segments and waxed in place. They were connected to an input line of a 4-channel amplifier penrecorder (Alvar Electronic). Motor activity was recorded with a simple set-up which has been previously described (Thon, 1982). The tethered fly was placed above two brass grids separated by a 2-mm space. The leg of the animal contacted the left and right grids. One grid was connected to the positive pole of a battery (1.5 V); the other grid, to one input line of the amplifier. The negative pole of the battery was connected to the other

plug of the same channel. Thus, the electrical circuit was closed by the animal's body, and each movement of the legs resulted in a change in the overall resistance. The variations of the weak current intensity induced by the animal's movements were amplified and recorded simultaneously with the electrocardiogram. Visual stimulation A vertical disk (35 cm in diameter), with 18 alternating black-and-white sectors, was placed on one side of the fly, parallel to its body axis, at a distance of 12 cm. The disk was continuously rotated at 360*/s. The whole experimental set-up being in darkness, the visual stimulation was given by suddenly illuminating the rotating disk. The onset and the offset of the stimulation were recorded by means of a photocell connected to the third channel of the amplifier pen-recorder. In all experiments, the stimulation had a duration of 2 s. Procedure. The experiment began 1 hr after initial operations to allow a complete recovery. The fly was placed in the experimental apparatus and left in darkness for 15 min. Then cardiac and motor activity were continuously monitored. If spontaneous motor activity was recorded, the beginning of the stimulation session was delayed until the animal was motionless for a period of at least 30 s. Each stimulation was applied at the beginning of each sucessive phase of forward beating. Since the duration of backward and forward beating phases showed a within-subjects and a between-subjects variability, the intertrial interval had a different value from one animal to another and also varied for a given animal in the course of the experiment. It had a mean duration of 20 B, with a minimum value of 12 s and a maximum of 30 s. After this acquisition session, the fly was left in darkness for a rest period of 12 min. A second series of 20 stimulations was then given in the same way in order to evaluate the spontaneous recovery of the habituated responses and the rate of rehabituation.

Results and Discussion Response measurements. Cardiac and motor responses were evaluated in an allor-none fashion. We considered that a cardiac response was released if the arrest of forward beating occurred during stimulus presentation or within the two following seconds. In the same way, we considered that a motor response was displayed if motor movements were recorded within the same period of time. Acquisition of habituation. The first visual stimulation induced a cardiac response in all flies, and a motor response in 80% of them (Figure 1). A progressive and rather regular decrement in response probability was observed during stimulus repetition. The levels reached at the end of the session were 30% for cardiac responses and 20%

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Figure 1. Variation of the percentage of elicited responses during acquisition of habituation and retention test after a 12-min rest period.

for motor responses. The overall change of an index of retention was computed for response level within the session is highly each animal following the formula / = (NA significant (Cochran's Q test, p < .01 for - NR)/(NA + NR), where NA is the numboth responses). A linear adjustment can ber of elicited responses during the last five be made between the natural logarithm of stimulations of acquisition session and NR the percentage of elicited responses and the is the number of elicited responses during number of stimulations (N). The equations the first five stimulations of retention test. of best fit lines are log (%R) = -0.020 X N This index takes into account the final + 4.586 for motor responses and log (%R) habituation level. We found average values = —0.017 X N + 4.60 for cardiac responses. of 0.16 ± 0.15 for motor response and -0.26 Neither the slopes nor the two regression ±0.11 for cardiac response. The index of lines differ statistically, which indicates retention is positive for motor responses that the decrement proceeded at the same but not significantly different from zero, indicating no substantial change in rerate for the two responses. Retention of habituation. The first sponse level during the rest period. The stimulation following the 12-min rest pe- index of retention is negative for cardiac riod induced a cardiac response in 46% of responses and different from zero (Stuthe flies and a motor response in 16%. dent's t test, p < .01), indicating a signifiThus, the level of motor responses did not cant recovery from previous habituation. change during the absence of stimulation, The'difference between the index of retenwhile cardiac responses showed an impor- tion of cardiac and motor responses is tant, but not complete, recovery. The dif- highly significant (Wilcoxon matched-pairs ference between response levels persisted test, p .25) nor for cardiac responses (r = .33, p > .15). This point can also be demonstrated by splitting the experimental sample into two groups (n = 15 for each), one group consisting of the animals that displayed a pronounced habituation of both responses during the first session (two or fewer responses during the last five trials) and the other of the animals that showed a weaker habituation (three or more responses during the last five trials). In order to allow a between-groups comparison, the results are expressed in terms of number of responses per five-trial block (Figure 2). A two-way analysis of variance (Winer, 1971) with repeated measures on one factor (blocks of trials), performed separately for cardiac and motor responses on retention test, revealed a significant change of motor response level across trial blocks, F(3, 84) = 4.87, p < .01, but no change for cardiac response (F < 1). The level of previous habituation has no effect on retention performance (F < 1 for both responses). A significant interaction between previous


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Figure 2 Mean number of cardiac responses (black circles) and motor responses (open circles) by five-trial blocks during acquisition and retention test in animals that displayed a strong behavioral habituation performance (left panel) and animals that displayed a low-habituation performance (right panel) during acquisition (Vertical bars indicate SE.)

habituation level and trials blocks is found only for motor responses, F(3, 84) = 2.85, p < .05. So, in spite of a great difference in behavioral habituation during the first session, these animals behaved in the same way during retention test. It can be noticed that the fact that low-habituating animals displayed a lower response level after the rest period than before rules out fatigue as the main factor responsible for response decrement. The lack of correlation between acquisition and retention performances has been reported in some habituation studies (see Hinde, 1970) and could be interpreted in terms of independent mechanisms involved in short-term retention (between two consecutive trials) and long-term retention (over a long period) of habituation. Alternatively, the present results can be interpreted by a sustained sensitization process that lasts for all the acquisition sessions in the low-habituating animals and decays during resting time, a situation allowing the habituation process to be revealed in the second session. In other words, habituation seems to be hidden at the behavioral level by an antagonist incremental process. The

next experiment was designed to study more precisely the relation between these two competing processes in the course of stimulus repetition. Experiment 2 This experiment was designed after Davis's (1972) paradigm which took advantage of the differential retention of habituation and sensitization to dissociate the influence of these processes on the behavioral outcome. The trials were given with a distributed procedure, which provides rest periods between blocks of trials. Method Twenty-five adult flies of both sexes, from 3 to 7 days old, were used. Apparatus for response recording and visual stimulation were the same as in Experiment 1 The general experimental conditions were also identical except for the temporal distribution of trials. Five blocks of 10 trials each were given. The duration of the rest interval between two consecutive blocks, was 5 min. During this time, the animal was left in darkness in the experimental apparatus. Within a single block, the stimulations were given as previously, with a mean interstimulus interval of 20 t,

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Figure 3. Variation of the percentage of elicited responses when a 5-min rest period is provided between consecutive blocks of 10 trials.

for cardiac response (Cochran's Q test, p < .05) but not for motor response (p > .10). The second 5-min rest period between Response measurements were made in the same way as in Experiment 1. The Block 2 and Block 3 is also followed by a results are plotted in Figure 3 in terms of significant drop in motor response level, percentage of elicited responses for each while the percentage of elicited cardiac responses does not change. Stimulus repetivisual stimulation. The changes in response level along the tion results again in a transient response first 10-trial block are comparable to those increment, which appears to be delayed observed during the first 10 stimulations in with respect to the increment observed in Experiment 1. Both cardiac and motor re- Block 2. For Block 3, the overall change is sponses reached the same level of 75% at significant only for motor responses (p < .01). the 10th stimulation. Finally, no substantial changes in reThe percentage of elicited response to the first stimulation following the first 5- sponse level can be noticed, either within min rest period falls to 56% for cardiac or between the last two blocks. So, in this experiment, response decreresponses and to 40% for motor responses. Response level at the beginning of this ments appeared to develop mainly in the block is significantly lower for motor re- absence of stimulation, during the rest pesponse (Cochran's Q test, p < .05). The riods provided between two consecutive difference is not significant for cardiac re- blocks. Such an obvious improvement of sponse (p > .20). When the stimulation is behavioral habituation after the removal of repeated, a transient increment in response stimulation has been reported in some percentage is observed, reaching a maxi- studies (see Peeke, 1969; Peeke & Peeke, mum at the fourth stimulation and followed 1970) and has been interpreted by Lethlean by a progressive decrement until the end of (1965) by the continuation of information the block. The overall change is significant processing during resting time. In that Results and Discussion


sense, habituation processes would be triggered by initial stimulations and would not stop developing when these were no longer given. This concept of habituation was later ruled out (Pearson & Robinson, 1973), and the most adequate explanation of this phenomenon is in terms of a dual-process model (Groves, Lee, & Thompson, 1969; Groves & Thompson, 1970; Thompson et al., 1973), which was put forward by Davis (1972) in a similar study. The basic assumption of this model is that any stimulation results in the development of two antagonist processes within the central nervous system: one incremental process that increases the general level of excitation; one decremental process that is supposed to take place specifically within the involved S-R pathway and tends to weaken subsequent responses to the stimulation. The incremental process, termed sensitization, appears to vanish faster than the decremental process, termed habituation, which has a longer time constant. Thus, during a rest period following a stimulation—or a series of stimulations—the induced incremental process will disappear rapidly, whereas the decremental process will be retained for a longer time. A stimulation given at that time will find the response system in a habituated state, without extrinsic activatory influences from other parts of the central nervous system. The actual response level will be lower than before resting time and will reflect more purely the strength of the underlying habituation process. The reminiscence-like phenomenon found in this experiment would be due in fact to the waning of sensitization over time. As in Experiment 1, habituation of motor responses appears to be better retained over the 5-min rest periods than habituation of cardiac responses. The percentage of elicited motor responses was always much lower than the percentage of cardiac responses, especially for the first trial of each block. Furthermore, no change in cardiac response level occurred during the last three rest periods. Within Blocks 2 and 3, a redevelopment of sensitization is revealed by the typical inverted-U shape of response curves. Since the response peak is delayed from the

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fourth stimulation in Block 2 to the eighth stimulation in Block 3, and does not appear clearly in Blocks 4 and 5, a habituation of sensitization seems to take place progressively during the experiment. The incremental processes would be less and less easily recruited by intrablock iterated stimulations. In order to compare quantitatively the results of Experiment 1 (massed training) and Experiment 2 (distributed training), the performance of each animal was computed in terms of the number of elicited responses within a five-stimulation block (Figure 4). The results are treated by a three-way analysis of variance (Winer, 1971) with repeated measures on two factors, blocks of trials and cardiac versus motor response, the independent factor being the method of training. Because the computational procedure requires equalsized groups, five animals of Experiment 1 were randomly removed, which left 25 animals in each training group. The variance analysis revealed a significant effect of the method of training, F(l, 48) = 4.56, p < .05, a significant change in response level across blocks of trials, F(9, 432) = 22.76, p < .001, and a significant difference between cardiac and motor performance, F(l, 48) = 34.49, p < .001. A significant interaction between training method and trials blocks, F(9, 432) = 3.59, p < .001, indicates that the response curves are not parallel following the method of stimulation. Whereas during massed trials the animals displayed a continuous waning of both responses, during distributed trials much response decrement occurred between the third and the fifth five-trial blocks. After this, the number of elicited responses remains rather constant and finally reaches the same level as the massed-trials group. This would be explained by the suggestion that habituation processes are not really affected by the method of training, at least in these experimental conditions. A distributed method would simply allow these habituation processes to become more quickly unmasked by a regular "washing out" of sensitization during the rest periods (Thompson et al., 1973), whereas sensitization cannot drop in such a way during massed trials.

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Figure 4. Comparison of massed and distributed methods of stimulation during initial acquisition of babituation of motor responses (left panel) and cardiac responses (right panel). (Ordinate: Mean number of responses by five-trial blocks. Dashed lines indicate the 5-min rest periods in the distributed trials group. Vertical bars indicate SE.)

Finally, the nature of the response is not involved in any significant interaction with other experimental factors, a result indicating that the two response systems are affected in the same way by the method of training. Since what differentiates the two methods is the amount of sensitization, this result supports the general idea that sensitization processes are not specific to a response system but affect the whole behavior of the animal. Experiment 3 The preceding results suggest that habituation processes that take place during the repetition of visual stimulation are more strongly established in the visuomotor system than in the visuocardiac system. Another way to compare the properties of these two systems is to test their ability to generalize habituation when some parameter of the stimulation is changed. This experiment was designed to study the effects on a previously acquired habituation

of a spatial displacement of the visual stimulus. Method The general experimental conditions were the same as in the two previous experiments. Two striped disks, rotating at the same speed (360°/ s) were placed at equal distance (12 cm) on each side of the fly. A first series of visual stimulations was given, with a mean intertrial interval (ITI) duration of 20 s, by lighting one of the two rotating disks. During this time, a black screen was placed in front of the opposite disk to prevent any stimulation from this side. The stimulations were carried on until a habituation criterion was reached. This behavioral criterion was set to four no-responses (cardiac and motor) for four consecutive trials. However, if the criterion was not reached within 50 stimulations, the animal was removed and not included in further analysis. Therefore, the animals received different amounts of stimulation, but they reached the same level of behavioral habituation. In the experimental group (n = 20), once the criterion was reached, the next stimulation was given, without changing the ITI, by lighting the opposite rotating disk. During the intertrial interval, the black screen was shifted to the previously used side. A second series of 10 stimulations was then given. In the control group (n = 20), the second series was given without changing the side of stimulation.

DIFFERENTIAL HABITUATION OF TWO RESPONSE SYSTEMS Response measurements were made with the same method as in Experiments 1 and 2.

Results and Discussion Eighteen animals did not reach the criterion.

The response curves of acquisition of habituation being synchronized with respect to the last stimulation (and not to the first, as previously) present a different shape when compared with these obtained in Experiments 1 and 2 (Figure 5). The level of

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Figure 5 Generalization of habituation of cardiac and motor responses (In both panels, the left part of the curve shows the percentage of elicited responses during the first 10 and last 10 stimulations of initial acquisition of habituation. In the top panel, the arrow indicates the first stimulation following the spatial displacement of the visual stimulation. In the control group [bottom panel], the stimulus was not moved.)

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motor and cardiac responses dropped abruptly just before the criterion trials. The disappearance of the responses was not progressive. This phenomenon could be due to the discontinuous method (all or none) of response measurement. The mean numbers of stimulations to reach the criterion were 26 in the experimental group (± 12) and 24 in the control group (± 9). They do not differ statistically (Mann-Whitney U test, p > .30). In the experimental group, after the disappearance of both responses, the spatial displacement of the visual stimulus resulted in a partial recovery of motor responses, up to 25%, and a great enhancement of cardiac responses, up to 65%. In the control group, for the corresponding stimulation, motor response level was 5% and cardiac response level was 15%. The difference between response levels of experimental and control groups was not significant for motor responses (Fisher's exact probability test, two-tailed, p > .18) and highly significant for cardiac responses (p < .0003). When the new visual stimulation was repeated in the experimental group, no change in motor response level was observed (Cochran's Q test, p > .30) while cardiac responses waned significantly (p < .01). In the control group, no significant change occurred in motor or cardiac response level. The values of the correlation between the number of stimulations necessary to reach the criterion and the number of elicited responses during the 10 stimulations of generalization test are r = .32 for motor responses and r = .35 for cardiac responses (p > .05). When we take into account only the performance to the first stimulation of the generalization test (which is more discriminative), the animals that displayed a cardiac response at that trial reached the criterion after a mean number of 28 (± 13) stimulations, and those that did not show a response reached the criterion after 24 (± 9) stimulations. The difference is not significant (Mann-Whitney f/test,p > .20). Thus, the extent of generalization of habituation appears to be greater for motor responses than for cardiac responses. This

differential generalization is mainly revealed by the first trial following the spatial shift of the visual stimulus, because cardiac response tends rapidly to reach the same level as motor response when the new stimulation is repeated. So, the generalization of habituation of cardiac responses is revealed by a saving in rehabituation rate after the reappearance of the response to the new stimulus. General Discussion The present results reveal that the two response systems, which have the same sensory input, display different properties of retention and generalization of habituation. This finding provides support for response-specific habituation—that is, S-R intrinsic models of habituation processes— because S-R extrinsic and unique mechanisms such as those suggested by Sokolov (1963) or Stein (1966) can hardly account for differential habituation of responses to the same actual stimulus. Habituation appears to take place independently and with different "strength" in various response systems. The dual-process model of Groves and Thompson (1970) provides a satisfactory framework to account for the observed behavioral results. However, it is not clear whether differential habituation proceeds from different basic mechanisms or from different synaptic plasticities in the underlying pathways. Moreover, the lack of correlation between acquisition rate and the retention of habituation suggests that different mechanisms within a given response system could be involved in short-term and long-term retention of habituatory response decrement, as previously suggested by Wagner (1976, 1979). Another general conclusion that can be drawn from this study deals with the need to be careful in using behavioral criteria to infer the extent of the underlying processes. The variations of the observed behavioral output during stimulus iteration are not faithfully representative of a unique mechanism. The involvement of at least two antagonistic processes with different temporal dynamics prevents the prediction of the retention performance of an individual


from its previous habituation performance during acquisition. Habituation is a very popular test in research on behavioral plasticity, because such experiments are easy to perform and the observed performance is believed to be weakly loaded by complex mechanisms of information processing. However, the multicomponent feature of the underlying processes has to be kept in mind when interpreting behavioral results from a neurobiological point of view. In particular, experimental designs using retention tests (even after a short rest period) allow sensitization effects to vanish during resting time and lead to a better assessment of the underlying habituation than a simple acquisition paradigm does. Finally, these results can be discussed with reference to the functional significance of the studied responses. Many studies have been devoted to the analysis of sensory-induced cardiac disturbances (Campan, 1972; Medioni & Campan, 1967; Queinnec & Campan, 1976) and their habituation (Queinnec & Thon, 1981; Thon & Queinnec, 1976). All the sensory stimulations that have been used as well as the locomotor movements (Thon 1976, 1980) induce an inhibition of forward beats of the heart. Moreover, these forward beats appear to be less favorable to the release of motor activity. It has been shown that the latency of a motor response to a moving visual stimulus is significantly shorter when the stimulation is given during a phase of backward beats than during forward beating of the heart (Thon, 1982). Thus, the arrest of forward beats by a sensory cue appears to have a "preparatory" function with respect to locomotor behavior. Because this preparatory function is not specific of a given behavioral pattern, the cardiac responses have to recover rapidly after habituation in order to become available again if a motor behavior, such as escape response, is needed to be quickly released. This fast reversibility of habituation seems to be a general feature of "warning" behaviors, such as orientation responses (Precht & Freytag, 1958). These responses are generally not competing with other behavioral patterns, whereas stimulus-specific responses, such as optomotor

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Received March 29, 1983 Revision received October 4, 1983 •