- Email: [email protected]
Observational learning of duration discrimination in rats (Rattus norvegicus)
Behavioural Processes 41 (1997) 97 – 105
Observational learning of duration discrimination in rats (Rattus nor6egicus) F. Simons a,*, H. Lejeune b b
a Cogniti6e Psychology Laboratory, Uni6ersity of Lie`ge, 5 bd du Rectorat, B32, 4000 Lie`ge, Belgium Psychobiology of Temporal Processes Unit, Uni6ersity of Lie`ge, 5 bd du Rectorat, B32, 4000 Lie`ge, Belgium
Received 31 October 1996; received in revised form 25 April 1997; accepted 6 May 1997
Abstract Hungry ‘observer’ rats watched at trained conspecific ‘demonstrators’ performing a duration discrimination (1 vs. 8 s sound) before being themselves exposed to the same task. Performance of ‘observer’ rats was compared with that of naive control rats who learned the same task without observing a demonstrator. Statistical analysis showed that observing a trained demonstrator significantly contributed to the rapid discovery of the relationship between a particular duration and its related response patterns or stimuli, increasing learning speed with regard to the control animals. © 1997 Elsevier Science B.V. Keywords: Duration discrimination; Imitation; Observational learning; Rat; Social learning
1. Introduction Scientists have long been interested in observational learning, and several early cases were reported both in the wild and in laboratory settings. For instance, in 1871, Darwin (Galef, 1988) commented the difficulty of trapping or poisoning a wild animal which had seen conspecifics poisoned or trapped (see also Logue, 1988). In 1884, Romanes (Galef, 1988) considered that observational * Corresponding author. Fax: + 32 436 62859; e-mail: [email protected]
learning was responsible for the continuity of behavior schedules and the perfection of instinct. In fact, these reports did not describe what would have been regarded as true social imitative learning (Robert, 1990; Heyes, 1994). Indeed, learning can occur without the presence or the influence of a conspecific, as animals submitted alone to a same environment may develop the same new behavior. In such cases, learning does not derive from the social environment and can be labeled ‘single stimulus learning’ or ‘asocial learning’. Categories of asocial learning can be distinguished on the basis of the type of experience (S, S–S or
0376-6357/97/$17.00 © 1997 Elsevier Science B.V. All rights reserved. PII S 0 3 7 6 - 6 3 5 7 ( 9 7 ) 0 0 0 3 9 - 9
98
F. Simons, H. Lejeune / Beha6ioural Processes 41 (1997) 97–105
R – S) which causes a change in the organism, and the type of behavior that is the signature of this change. Social learning, on the other hand, supposes, first, that a demonstrator plays a role in generating matching behavior and, second, that this behavior will be produced later on in the absence of the demonstrator (Heyes, 1994). Without claiming to be exhaustive, we may firstly illustrate asocial learning and mention local enhancement, which can be defined as ‘an apparent imitation resulting from directing the animal’s attention to a particular object or to a particular part of the environment’ (Thorpe, 1963, p. 143). For instance, a rat finding food in a hole will draw the attention of a nearby conspecific to this location in the environment (Galef and Clark, 1971). The conspecific’s behavior may then develop by trial and error, but not by imitation of a demonstrator’s behavior. A less restrictive definition was proposed by Spence (1937), and further expanded by Heyes (1994), under the label stimulus enhancement: learning may occur ‘when observation of a demonstrator (or its products) exposes the observer to a single stimulus (rather than a relationship between events) at t1, and single stimulus exposure effects a change in the observer detected, in any behavior at t2’ (Heyes, 1994, p. 216). Social facilitation or contagious behavior, i.e. the increase in the intensity, frequency or initiation of behaviors present in the repertoire of the animal (Clayton, 1978) is another case of single stimulus or asocial learning. To occur, social facilitation requires the presence of conspecifics engaged in the same behavior (for instance, satiated chickens start eating again if they are placed together with eating conspecifics). However, contagious behavior is not a case of social learning, because the effects are detected only in the presence of conspecifics (at t1) and not in their absence (at t2). Second, a process similar but more sophisticated than stimulus enhancement was described in chimpanzees (Pan troglodytes). Common chimpanzees and 2-year-old children were presented with a rake-like tool and an attractive but out of reach food item. In each group, half of the subjects saw a demonstrator using the tool in one
way and the other half observed a demonstrator using the tool in another way. As they had to retrieve the food item, chimpanzees in both conditions displayed an identical use of the tool, whereas children did what the demonstrators did: they faithfully reproduced the demonstrator’s behavior. Thus, children imitated the demonstrator’s behavior whereas chimpanzees did not (Tomasello et al., 1987; Nagell et al., 1993). They only learned functional relationships within the task, such as the tool–goal relationship, but they did not precisely learn how the demonstrators behaved. This learning process has been described as emulation, a label borrowed from research on social learning in human development (e.g. Wood, 1989) Finally, animals may specifically imitate the behavior of a conspecific. These cases are labeled imitative social learning. For instance, monkeys observing a conspecific’s fear in response to the presence of a snake will exhibit the same behavior when exposed to the same stimulus (Mineka et al., 1984). In other respects, the famous potato washing by Japanese monkeys (Macaca fuscata) (Kawai, 1965; Itani and Nishimura, 1973) rather seems to be a case of stimulus enhancement instead of imitative social learning (see Galef, 1990). Second, budgerigars (Melopsittacus undulatus) which observed a conspecific using its feet to remove a flat cover from a food cup were more likely to use the same appendages than birds which observed a demonstrator using its beak. This effect was, however, fragile and transitory, as the observer birds switched to a beak response after just a few trials (Galef et al., 1986). Third, rats which had the opportunity to push a joystick for food immediately after observing, from an adjacent compartment, a conspecific demonstrator moving this lever in front of them, 50 times either to the right or to the left, pushed the joystick in a direction opposite to the observed one (Heyes and Dawson, 1990). The plausibility of imitative social learning was furthermore strengthened by a transfer test, the axis of the joystick having been rotated 90° between observation of a model and testing sessions (Heyes et al., 1992). Later experiments conducted by the same team proved that the activity of a conspecific
F. Simons, H. Lejeune / Beha6ioural Processes 41 (1997) 97–105
demonstrator was indispensable for imitative learning to occur. Rats having observed a joystick moving automatically, either in the presence or the absence of a passive conspecific, did not show observation-consistent responding (Heyes et al., 1994). As was the case for asocial learning, instances of social learning can be classified according to the underlying mechanisms (Heyes, 1994). Snake fear is a case of observational conditioning or S – S learning, which depends upon a pavlovian conditioning mechanism. Indeed, in the first part of the process, the observer was exposed to the unconditioned fear response (UCR) of a conspecific facing a snake (S1). Exposure to this association changed the UCR into an unconditioned stimulus (UCS) eliciting, in the absence of the conspecific, a matching fear response to the snake stimulus. Observational conditioning involves unconditioned behavior, and not a topographical novel response, as is the case in the two last examples listed above (cover lifting in budgerigars and joystick pushing in rats). In these cases, the observer’s behaviors were instances of observational learning of an R – S relationship, i.e. a subset of the instrumental response – reinforcer (R – RF) conditioning process. Observers learned a positive relationship between a demonstrator’s novel response and an appetitive reinforcement and, subsequently, produced the same novel topographically matching behavior. Procedures designed to analyze observational learning basically resort to one of three categories: the ‘duplicate cage’ procedure, the ‘non-exposed control procedure’ and the ‘pattern control procedure’. In experiments using the ‘duplicate cage’ procedure, a demonstrator and an observer are kept in separate but identical experimental enclosures fitted with identical response and reinforcement devices. Demonstrators and observers thus remain in sight of each other as demonstration and imitation attempts go on (as in the above described emulation case). In experiments using the ‘non-exposed control’ procedure, observer animals watch models perform from a separate and ‘nude’ enclosure, whereas controls are not exposed to demonstrators, but only to the apparatus operations. With the ‘pattern control’ procedure,
99
one manipulandum is present, as in the second procedure, but this manipulandum has particular properties: it can be used in two or several ways. Pushing a joystick in one or the other direction, as in the bi-directional control procedure of Heyes and Dawson (1990), is a good example. Whereas the second procedure does not provide a control for local or stimulus enhancement (learning rate may increase by autoshaping of the response or because the attention of the observer was attracted to a particular feature in the environment), the third does: the response device must not only be manipulated, but the nature of the behavior (lift the cover with the beak or the paw) or its directional patterning (push to the left or to the right) are determinant. The experiment described hereafter addresses for the first time the social learning of a measure of time. Living organisms do not have a time ‘sense’ and time is a dimension of every phenomenon or event. However, it might happen that only their durations can allow organisms to discriminate between two events which otherwise share common features, and it is commonly argued that time discrimination is indispensable to survival. It thus is reasonable to assume that living organisms possess mechanisms specifically devoted to measuring time (for classical animal data, see Richelle and Lejeune, 1980; Gibbon and Allan, 1984; more recent perspectives and human data are discussed, for instance, in Block, 1990; Macar et al., 1992; Lejeune and Macar, 1993; Helfrich, 1996). In particular, the role played by attention in time estimation has been highlighted in animals and humans (Meck, 1983; Macar et al., 1994). Methods have long been developed to test temporal accuracy and sensitivity of animals or humans to time. One of them, the temporal discrimination procedure, was used here (Church et al., 1976). Demonstrator rats were trained to listen to a short or a long sound, before two retractable response levers (‘A’ and ‘B’) where simultaneously introduced in the experimental enclosure. If the sound stimulus had been short (1 s) food reinforcement followed a press on lever ‘A’; if it had been long (8 s), a press on lever ‘B’ was reinforced, and vice versa. Thereafter, ‘naive’ rats
100
F. Simons, H. Lejeune / Beha6ioural Processes 41 (1997) 97–105
observed from a ‘nude’ adjacent compartment a conspecific model performing with high efficiently (94 – 100% correct presses, depending upon the session or the subject). The demonstrator was then removed and the observer rat was put in the demonstration compartment for a series of discrimination trials. With regard to the procedure categories distinguished above, the experimental design followed here can be included within the non-exposed control category. The possible influence of stimulus enhancement, autoshaping or incidental learning was reduced by shaping observer and control rats on both levers, prior to their exposure to the experimental conditions. As the observer rats already mastered the leverpress – food (R–RF) relationship (which was not the case in the series of experiments by Heyes and collaborators), the one and only relevant information was the demonstrator’s strategy with regard to the short and long sounds. Previous leverpress training, indeed, potentially increased the likelihood of true imitative social learning in the explanation of observer rats’ time discrimination behavior.
2. Materials and methods
2.1. Subjects Sixteen naive 5-month-old male Wistar albino rats were randomly assigned to the ‘observer’ or ‘control’ groups. Five other male rats (10-monthold) were the ‘demonstrators’. All animals were maintained at 85% of free-feeding weight and had free access to water in their home cage. They were kept on a 12-h light/dark cycle (lights on 06:30 h).
be protruded in the chamber or retracted in 0.75 s. Retractable levers were used to prevent responding before the end of the sound signal. Neither response devices nor food cup were located in the observation compartment. Observer or control rats were thus not reinforced while watching the model or the operation of the apparatus. A loudspeaker was placed 350 mm above the food dispenser. It delivered a 4000 Hz, 40 dB tone (Kelly and Mastreton, 1977) of 1 (short signal), or 8 s (long signal). Results were collected on an 8086 PC.
2.3. Procedure 2.3.1. Training of the ‘demonstrator’ rats The five demonstrator rats had an experimental history on a Fixed-Interval 60-s schedule. Errorless discrimination training took place over five consecutive 40-trial sessions (1–5). In these sessions, the 1 or 8 s sounds were delivered and followed by the presentation of the correct lever. The left lever was arbitrarily associated to the 8 s signal for three demonstrators, and to the short signal for the remaining two. The correct lever remained accessible until the first response was given or a maximum delay of 60 s. This errorless procedure was maintained until each sound stimulus was followed by a leverpress. On the next 25 days, both levers were simultaneously presented after each stimulus duration and rats were exposed to 60-trial sessions twice a day (sessions 6–54). A correction procedure was used: each error was followed by the same trial until a cor-
2.2. Apparatus Animals were trained and tested in a long perspex chamber (80 ×40 ×40 cm) with an aluminum grid floor, as shown in Fig. 1. This chamber was divided in two compartments of equal size by a transparent partition. In the left compartment, two identical retractable levers were located at 7 cm on either side of a food tray, and 5 cm above the floor. Each lever required a 20-g force to be depressed. These two levers could
Fig. 1. Perspex test chamber.
F. Simons, H. Lejeune / Beha6ioural Processes 41 (1997) 97–105
rect response was recorded. Sounds were randomly scheduled, with the restriction that a same duration could not be presented three times consecutively (except in the correction mode). Each trial was followed by an Inter-Trial-Interval (ITI) of 10–20 s. From session 22, a ‘spectator’ rat was placed in the observer compartment to accustom the demonstrator to the proximity of a conspecific. During the next four sessions (23 – 26), demonstrators were influenced by the spectators, as the response latencies increased. Thereafter, habituation to the presence of a conspecific developed and demonstrators performed with short response latencies and an efficiency of 94 – 100%, depending on the session and the subject.
2.3.2. Training of the ‘obser6er’ and ‘control’ rats Observers and control rats underwent a hand shaping procedure to leverpress for food pellets. Half of the animals of each group were shaped on the left and the other half on the right lever. After shaping and to avoid any lever preference, the location of the inserted lever was changed from one session to the next. In the first four training sessions (session 1– 4) the lever was protruded into the chamber before the animal went in and was not retracted. Each leverpress was reinforced and this training stopped after 30 food pellets were earned. At the end of these four sessions, each animal readily pressed both levers with a response latency less than three seconds. They were then accustomed to the lever movements. On sessions 5–8, the rats were introduced into the chamber before a lever was presented. The lever remained accessible until 30 responses were made (as previously, each response was reinforced). Thereafter, in the same session, the lever was briefly retracted before being presented again until 15 responses were made. It was then again retracted after ten and eventually five responses were produced by the rat. During this phase, the inserted lever was changed from one session to the next, as previously. Finally, both levers were presented simultaneously during two sessions of 40 trials each (11–12). At the end of training, observers were assigned to the demonstrators. As only five demonstrators were available for eight observer rats, three of them (A, B and C, see Table 1) ‘instructed’ two experimental animals.
101
Table 1 From left to right, demonstrators (with their 8 s lever, left or right) assigned to observer rats, and control rats paired to the observer animals Demonstrators
8-s Lever
Observers
Controls
A
R
B
R
C
L
D E
L L
O1 O2 O3 O4 O5 O6 O7 O8
C1 C2 C3 C4 C5 C6 C7 C8
2.4. Testing The experiment started the day after the last training session and lasted for 14 daily sessions. The rats worked 7 days a week. The first three sessions lasted for 50 and the next eleven for 60 trials. Each session was divided in two parts. In the first one, called ‘observational part’, a demonstrator performed the task (30 trials) while an observer was in the observational chamber. The ‘test part’ followed: the demonstrator was removed and the observer was placed in the testing chamber to perform the same task. No correction mode was used. For control rats, the test chamber was empty during the observational phase, but the computer monitored the sounds, ejected and quickly retracted the levers and distributed reinforcers on 95% of the trials, to mimic the apparatus operations of a demonstrator session.
3. Results The session duration, the trial durations, the responses latencies, the total number of responses and the number of correct responses on the left and right levers were recorded during each session. The mean trial duration did not differ between groups and responses were recorded on 99% of the trials. Response latency was defined as the time elapsed between the lever protrusion and the
102
F. Simons, H. Lejeune / Beha6ioural Processes 41 (1997) 97–105
first leverpress. This latency quickly became shorter than 0.1 s, i.e. shorter than the rat’s reaction time. These data could be explained by a mechanical artifact. Animals started to press the lever as it was still moving, before a response could actually be recorded. As this became possible, the lever was already depressed, which explains the extremely short average latencies. We can observe, on the left side of Fig. 2, that the mean response latencies on levers A and B were not significantly different (F(1, 8) =0.03, P = 0.95). However, the right side of Fig. 2 shows that he mean latency on the short lever was twice as long as the mean latency on the long lever (F(1, 8)=7.29, PB 0.03). The mean performance of observer and control rats, as measured by the mean percentage of correct responses in the discrimination task, is displayed in Fig. 3. Visual inspection shows that, after a few sessions, learning curves diverged before converging again. Therefore, data were grouped into three blocks: sessions 1 – 6, 7 – 10 and, finally, 11–14. Within – between ANOVAs were computed separately for each block of data. The first block (sessions 1 – 6) yielded neither a session nor a group effect (F(5, 70) = 2.05, P = 0.082, and F(1, 14)=0.25, P =0.63, respectively). For the second data block (sessions 7 – 10), the ANOVA revealed significant effects of the session, the group, and a session ×group interaction (F(3, 42)= 8.36, PB 0.0002, F(1, 14) = 8.65, P B 0.02, and F(3, 42)=3.16, P B0.05, respectively). The last block (sessions 11 – 14) yielded only a significant session effect (F(3, 42) = 4.23, P B 0.02).
Fig. 2. Mean response latencies pooled over control and observer rats, in the four last sessions from the 14-session observational testing. * Significant difference at PB 0.03.
Fig. 3. Mean performance of observer and control rats as measured by the proportion of correct responses over successive sessions.
Another way to describe the results was to record, for each rat, the number of sessions needed to reach a performance criterion, such as 70% correct responses. This criterion cannot be reached haphazardly, as the probability of obtaining by chance 70% of correct responses on 60 trials is equal to 0.0008. Data from the observer and control rats were compared with the t-test. Differences were significant: observers reached the criterion earlier than controls (t(14)=0.571, PB 0.02). This differential evolution is illustrated in Fig. 4.
Fig. 4. Number of rats which reached 70% of correct responses, cumulated over successive sessions.
F. Simons, H. Lejeune / Beha6ioural Processes 41 (1997) 97–105
4. Discussion The aim of the present experiment was to investigate whether naive rats could learn by observation a duration discrimination task modeled by demonstrator conspecifics. Effects of demonstrators on the acquisition of a time discrimination by observer rats were found: first, their mean percent of correct responses was significantly higher than that of controls at training sessions 7 – 10; second, the learning rate was faster for observer rats, as they reached the 70% correct responses criterion significantly earlier than controls. Results shown on Fig. 3 are similar to those obtained with pigeons by Biederman and Vanayan (1988). In that experiment, four groups of observer pigeons were compared in the acquisition of a discrimination between an erect and an inverted triangle. These groups differed along two parameters: the observation of a proficient versus a non-proficient demonstrator, and the observation of the apparatus operation versus a demonstrator conspecific. In the first experiment, the four groups remained highly similar over the first 5 of 8 training sessions. Between – group differences became significant only thereafter (as can be seen in Fig. 1, p. 37), as was the case in our study. In particular, the main effect of proficiency was significant (watching a skilled versus an unskilled model), as was the main effect of yoking (watching the apparatus operations versus a conspecific model). Trying to explain how observer rats benefited from the demonstrator’s performance, we might first reject hypotheses that do not seem to fit the data. Firstly, stimulus enhancement might be questioned because observer and control rats were magazine-trained and shaped in the test cubicle prior to the demonstration and test sessions. Thus, both groups of rats already learned an R – Rf relationship involved in performing the task and might be considered as displaying similar interest towards the levers, the food cup and the experimental context. Further, as duration is an ubiquitous stimulus or event dimension and not a physical item such as a lever or a food cup, applying the stimulus enhancement concept to
103
time would require broadening it. However, as it seems likely that indices such as odor marks left by the demonstrators played a role and might be taken into account, stimulus enhancement cannot be completely discarded in the explanation of the above results. Second, social facilitation, i.e. an increase of behavior present in the repertoire of the animal, due to the mere presence of a conspecific can be eliminated, not only because observers were tested alone after each observation session, but also because the complex behavior pattern to be performed had to be learned and did not belong to the natural repertoire of the species. Third, as emulation was described so far only in chimpanzees, it would be farfetched speculation to resort to this hypothesis, particularly as in the emulation experiment reported above, and which used the ‘duplicate cage’ procedure, the model (the experimenter) and the observer (the chimpanzee) remained within sight of each other during the tests. The question remains of whether true imitative social learning might be involved. Before trying to answer this question, we might first describe how demonstrators behaved and consider what should be learned to master the duration discrimination task. All the demonstrators followed the same behavioral sequence. As soon as a sound stimulus was presented, they moved to the short lever side and stood in front of the aperture through which the short lever should be presented. If the short lever did not appear, they waited for a few more seconds before moving to the other side of the cubicle and facing the long lever location. This strategy was optimal: as the sounds ended, the rats stood in front of the correct lever. This response strategy might also explain the difference between short and long response latencies, displayed in Fig. 2: the rats had only a short time to be well oriented towards the short lever (1 s), whereas they faced the long lever before the end of the long duration stimulus. Merely copying the model’s displacements within the test chamber cannot lead to correct performance, because the key to proficient behavior is the mastery of the relationship between the duration of the sound stimulus and the displace-
104
F. Simons, H. Lejeune / Beha6ioural Processes 41 (1997) 97–105
ment pattern of the demonstrator rat. Similarly, measuring the duration of the demonstrator’s immobility in front of the right and left levers or memorizing a long sequence of behavior over successive trials is to no avail, as short and long stimuli were presented at random within and between sessions. Therefore, the contribution of ‘blind’ imitation in the mastery of the task could only be modest, with regard to the importance of the discovery of the relationship between particular behavior patterns and durations. There are two remaining hypotheses. The first suggests that imitative social learning took place, i.e. that observer rats learned more rapidly the relationship between a duration (short or long) and a particular behavior pattern displayed by the demonstrator in the test box. They, thus, might have more rapidly learned an S (sound duration) – R (displacement patterning) relationship that could be grafted on the leverpress – reinforcer link they mastered from the start of the experiment, before being caught up by control rats towards the end of the 14-session test. In other words, the first term of the already mastered leverpress – reinforcer (R–Rf) link was changed into a more elaborated behavioral pattern, conditional upon the duration of the previous sound stimulus. As controls only mastered the R – Rf link and were not exposed to a proficient demonstrator, they had to discover the complementary S – R relationship by trial and error, without the help of behavioral clues. The second hypothesis considers that proficiency of the observer rats might also be explained by the learning of an S – S relationship. For instance, they might have learned that, after a short tone (S1), movements (S2) of the left lever produced reward, and after a long tone, movements of the right lever had the same outcome. This would have rendered the sight of the left lever more appealing after a short tone (as would the sight of the right lever after a long tone), and, consequently, have induced approach to that lever and emission of the already mastered leverpress. Rats might thus have learned which lever movement (due to the demonstrator action) produced reward after one or the other sound duration. This conditional discrimination would have been
an instance of S–S learning, within the frame of instrumental conditioning. Even if this hypothesis does not at all put emphasis on imitating the demonstrator, it may play a determining role in the early discovery of the S–S link and of the key importance of time. Testing this hypothesis would involve control rats observing the mere apparatus operations, with, additional to the simultaneous protrusion of both levers, movement of the ‘correct’ lever associated to the just preceding duration stimulus, a condition similar to the one used in Heyes et al. (1994), where control rats could observe the correct joystick movements (to the left or to the right). The reasons why both groups of rats did not differ over the six first training sessions may be two-fold. Firstly, a stimulus enhancement process might have been as potent for observers than for controls. Such a hypothesis is supported by the fact that the importance of time (and thus its estimation) can only emerge progressively from the interaction between the animal and the temporal contingencies of the task. Another and complementary hypothesis should, however, not be disregarded: acquired equivalence learning. Indeed, control rats had not to pay attention to the short or long duration of the sound stimuli, as they had the same outcome: simultaneous protrusion of both levers. Thus, controls had to extinguish this learned equivalence while discovering the importance of the temporal dimension of the sound stimuli. Complementary experimentation to test this hypothesis should involve control rats hearing the tones, without seeing subsequent lever protrusion and retraction. This last hypothesis does, however, not exclude S–R or S–S learning in experimental rats, as explained above. It nevertheless suggests that differences between experimental and control animals might have been less evident. In conclusion, there is no doubt that both the observers and the controls eventually displayed behavior patterns highly similar to those of demonstrators, as casual observation showed, because the discrimination task does not leave much room for behavioral variation. However, displaying similar behavior patterns and proficiency levels was probably mediated by learning processes
F. Simons, H. Lejeune / Beha6ioural Processes 41 (1997) 97–105
which were partially different. Observing a proficient conspecific might have contributed to a more rapid discovery of the crucial relationship between a particular duration and its related response patterns (S – R), or to the more rapid learning of the relationship between the duration stimuli and their correlated lever movements (S – S). In any case, the attention of observer rats was directed earlier to the key importance of time.
Acknowledgements We are very grateful to John Wearden for his proofreading and to the referees for helpful comments. This paper is based on a dissertation submitted by the corresponding author, in partial fulfilment of the requirements for a master’s degree in biology at the University of Lie`ge.
References Biederman, G.B., Vanayan, M., 1988. Observational learning in pigeons: The function of quality of observed performance in simultaneous discrimination. Learn. Motiv. 19, 31–43. Block, R.A. (Ed.) 1990. Cognitive models of psychological time. Lawrence Erlbaum, Hillsdale, NJ, p. 283. Church, R.M., Getty, D.J., Lerner, N.D., 1976. Duration discrimination by rats. J. Exp. Psychol. Anim. Behav. Proc. 2, 303 – 312. Clayton, D.A., 1978. Socially facilitated behavior. Q. Rev. Biol. 53, 373 – 391. Galef, B., 1988. Imitation in animals: history, definition and interpretation of data from psychological laboratory. In: Zentall, T.R., Galef, B.P. (Eds.), Social Learning: Psychological and Biological Perspectives, Lawrence Erlbaum, Hillsdale, NJ, pp. 3 – 28. Galef, B., 1990. Tradition in animals: Field observations and laboratory analyses. In: Beckoff, M., Jamieson, D. (Eds.), Interpretations and Explanations in the Study of Behaviour: Comparative Perspectives, Westview Press, Boulder, CO, pp. 74 – 95. Galef, B.G. Jr., Clark, M., 1971. Social factors in the poison avoidance and feeding behavior of wild and domesticated rats pup. J. Comp. Physiol. Psychol. 75, 341–357. Galef, B.G., Manzig, L.A., Field, R.M., 1986. Imitation learning in budgerigars: Dawson and Foss revisited. Behav. Proc. 13, 191 – 202. Gibbon, J., Allan, L., 1984. Timing and time perception. Ann. NY Acad. Sci. 423, 654. Helfrich, H. (Ed.) 1996. Time and Mind. Hogrefe and Huber, Seattle, WA, 209 pp.
105
Heyes, C.M., 1994. Social learning in animals: Categories and mechanisms. Biol. Rev. 69, 207 – 231. Heyes, C.M., Dawson, G.R., 1990. Demonstration of observational learning in rats using a bi-directional control. Q. J. Exp. Psychol. 42B, 59 – 71. Heyes, C.M., Dawson, G.R., Nokes, T., 1992. Imitation in rats: initial responding and transfer evidence. Q. J. Exp. Psychol. 45B, 229 – 240. Heyes, C.M., Jaldow, E., Nokes, T., Dawson, G.R., 1994. Imitation in rats (Rattus nor6egicus): The role of the demonstrator action. Behav. Proc. 32, 173 – 182. Itani, J., Nishimura, A., 1973. The study of infrahuman culture in Japan. In: Montana, W. (Ed.), Symp. 4th Int. Cong. Primatology, Precultural Primate Behaviour, Karger, Basel, pp. 26 – 50. Kawai, M., 1965. Newly acquired pre-cultural behaviour of the natural troop of Japanese monkeys on Koshima isle. Primates 6, 1 – 30. Kelly, J.B., Mastreton, B., 1977. Auditory sensitivity of the albinos rat. J. Comp. Physiol. Psychol. 91, 930 – 936. Lejeune, H., Macar, F., 1993. Temporal processes: Thematic issue. Psychologica Belgica 33 (2), 350. Logue, A.W., 1988. A comparison of taste aversion learning in humans and other vertebrates: Evolutionary pressures in common. In: Bolles, R.C., Beecher, M.D. (Ed.s), Evolution and Learning, Lawrence Erlbaum, Hillsdale, NJ, pp. 97 – 116. Macar, F., Grondin, S., Casini, L., 1994. Controlled attention sharing influences time estimation. Memory Cognition 22, 673 – 686. Macar, F., Pouthas, V., Friedman, W. J. (Eds.) 1992. Time, Action and Cognition: Towards Bridging the Gap, Kluwer Academic, Dordrecht, 407 pp. Meck, W.H., 1983. Selective adjustment of the speed of the internal clock and memory processes. J. Exp. Psychol. Anim. Behav. Proc. 9, 171 – 201. Mineka, S., Davidson, M., Cook, M., Keir, R., 1984. Observational conditioning of snake fear in rhesus monkeys. J. Abnorm. Psychol. 93, 355 – 372. Nagell, K., Olguin, R.S., Tomasello, M., 1993. Processes of social learning in the tool use of chimpanzees (Pan troglodytes) and human children (Homo sapiens). J. Comp. Psychol. 107, 174 – 186. Richelle, M., Lejeune, H. (Eds.) 1980. Time in Animal Behaviour. Pergamon Press, Oxford, 273 pp. Robert, M., 1990. Observational learning in fish, birds, and mammals: a classified bibliography spanning over 100 years of research. Psychol. Rec. 40, 289 – 311. Spence, K.W., 1937. Experimental studies of learning and higher mental processes in infra-human primates. Psychol. Bull. 34, 806 – 850. Thorpe, W., 1963. Learning and Instinct in Animals. 2nd ed. Methuen, London, 558 pp. Tomasello, M., Davis-Dasilva, M., Camak, L., Bard, K., 1987. Observational learning of tool use by young chimpanzees. Human Evol. 2, 175 – 183. Wood, D., 1989. Social interaction as tutoring. In: Bornstein, M., Bruner, J. (Eds.), Interaction in Human Development. Blackwell, London, pp. 59 – 80.
Observational learning of duration discrimination in rats (Rattus nor6egicus) F. Simons a,*, H. Lejeune b b
a Cogniti6e Psychology Laboratory, Uni6ersity of Lie`ge, 5 bd du Rectorat, B32, 4000 Lie`ge, Belgium Psychobiology of Temporal Processes Unit, Uni6ersity of Lie`ge, 5 bd du Rectorat, B32, 4000 Lie`ge, Belgium
Received 31 October 1996; received in revised form 25 April 1997; accepted 6 May 1997
Abstract Hungry ‘observer’ rats watched at trained conspecific ‘demonstrators’ performing a duration discrimination (1 vs. 8 s sound) before being themselves exposed to the same task. Performance of ‘observer’ rats was compared with that of naive control rats who learned the same task without observing a demonstrator. Statistical analysis showed that observing a trained demonstrator significantly contributed to the rapid discovery of the relationship between a particular duration and its related response patterns or stimuli, increasing learning speed with regard to the control animals. © 1997 Elsevier Science B.V. Keywords: Duration discrimination; Imitation; Observational learning; Rat; Social learning
1. Introduction Scientists have long been interested in observational learning, and several early cases were reported both in the wild and in laboratory settings. For instance, in 1871, Darwin (Galef, 1988) commented the difficulty of trapping or poisoning a wild animal which had seen conspecifics poisoned or trapped (see also Logue, 1988). In 1884, Romanes (Galef, 1988) considered that observational * Corresponding author. Fax: + 32 436 62859; e-mail: [email protected]
learning was responsible for the continuity of behavior schedules and the perfection of instinct. In fact, these reports did not describe what would have been regarded as true social imitative learning (Robert, 1990; Heyes, 1994). Indeed, learning can occur without the presence or the influence of a conspecific, as animals submitted alone to a same environment may develop the same new behavior. In such cases, learning does not derive from the social environment and can be labeled ‘single stimulus learning’ or ‘asocial learning’. Categories of asocial learning can be distinguished on the basis of the type of experience (S, S–S or
0376-6357/97/$17.00 © 1997 Elsevier Science B.V. All rights reserved. PII S 0 3 7 6 - 6 3 5 7 ( 9 7 ) 0 0 0 3 9 - 9
98
F. Simons, H. Lejeune / Beha6ioural Processes 41 (1997) 97–105
R – S) which causes a change in the organism, and the type of behavior that is the signature of this change. Social learning, on the other hand, supposes, first, that a demonstrator plays a role in generating matching behavior and, second, that this behavior will be produced later on in the absence of the demonstrator (Heyes, 1994). Without claiming to be exhaustive, we may firstly illustrate asocial learning and mention local enhancement, which can be defined as ‘an apparent imitation resulting from directing the animal’s attention to a particular object or to a particular part of the environment’ (Thorpe, 1963, p. 143). For instance, a rat finding food in a hole will draw the attention of a nearby conspecific to this location in the environment (Galef and Clark, 1971). The conspecific’s behavior may then develop by trial and error, but not by imitation of a demonstrator’s behavior. A less restrictive definition was proposed by Spence (1937), and further expanded by Heyes (1994), under the label stimulus enhancement: learning may occur ‘when observation of a demonstrator (or its products) exposes the observer to a single stimulus (rather than a relationship between events) at t1, and single stimulus exposure effects a change in the observer detected, in any behavior at t2’ (Heyes, 1994, p. 216). Social facilitation or contagious behavior, i.e. the increase in the intensity, frequency or initiation of behaviors present in the repertoire of the animal (Clayton, 1978) is another case of single stimulus or asocial learning. To occur, social facilitation requires the presence of conspecifics engaged in the same behavior (for instance, satiated chickens start eating again if they are placed together with eating conspecifics). However, contagious behavior is not a case of social learning, because the effects are detected only in the presence of conspecifics (at t1) and not in their absence (at t2). Second, a process similar but more sophisticated than stimulus enhancement was described in chimpanzees (Pan troglodytes). Common chimpanzees and 2-year-old children were presented with a rake-like tool and an attractive but out of reach food item. In each group, half of the subjects saw a demonstrator using the tool in one
way and the other half observed a demonstrator using the tool in another way. As they had to retrieve the food item, chimpanzees in both conditions displayed an identical use of the tool, whereas children did what the demonstrators did: they faithfully reproduced the demonstrator’s behavior. Thus, children imitated the demonstrator’s behavior whereas chimpanzees did not (Tomasello et al., 1987; Nagell et al., 1993). They only learned functional relationships within the task, such as the tool–goal relationship, but they did not precisely learn how the demonstrators behaved. This learning process has been described as emulation, a label borrowed from research on social learning in human development (e.g. Wood, 1989) Finally, animals may specifically imitate the behavior of a conspecific. These cases are labeled imitative social learning. For instance, monkeys observing a conspecific’s fear in response to the presence of a snake will exhibit the same behavior when exposed to the same stimulus (Mineka et al., 1984). In other respects, the famous potato washing by Japanese monkeys (Macaca fuscata) (Kawai, 1965; Itani and Nishimura, 1973) rather seems to be a case of stimulus enhancement instead of imitative social learning (see Galef, 1990). Second, budgerigars (Melopsittacus undulatus) which observed a conspecific using its feet to remove a flat cover from a food cup were more likely to use the same appendages than birds which observed a demonstrator using its beak. This effect was, however, fragile and transitory, as the observer birds switched to a beak response after just a few trials (Galef et al., 1986). Third, rats which had the opportunity to push a joystick for food immediately after observing, from an adjacent compartment, a conspecific demonstrator moving this lever in front of them, 50 times either to the right or to the left, pushed the joystick in a direction opposite to the observed one (Heyes and Dawson, 1990). The plausibility of imitative social learning was furthermore strengthened by a transfer test, the axis of the joystick having been rotated 90° between observation of a model and testing sessions (Heyes et al., 1992). Later experiments conducted by the same team proved that the activity of a conspecific
F. Simons, H. Lejeune / Beha6ioural Processes 41 (1997) 97–105
demonstrator was indispensable for imitative learning to occur. Rats having observed a joystick moving automatically, either in the presence or the absence of a passive conspecific, did not show observation-consistent responding (Heyes et al., 1994). As was the case for asocial learning, instances of social learning can be classified according to the underlying mechanisms (Heyes, 1994). Snake fear is a case of observational conditioning or S – S learning, which depends upon a pavlovian conditioning mechanism. Indeed, in the first part of the process, the observer was exposed to the unconditioned fear response (UCR) of a conspecific facing a snake (S1). Exposure to this association changed the UCR into an unconditioned stimulus (UCS) eliciting, in the absence of the conspecific, a matching fear response to the snake stimulus. Observational conditioning involves unconditioned behavior, and not a topographical novel response, as is the case in the two last examples listed above (cover lifting in budgerigars and joystick pushing in rats). In these cases, the observer’s behaviors were instances of observational learning of an R – S relationship, i.e. a subset of the instrumental response – reinforcer (R – RF) conditioning process. Observers learned a positive relationship between a demonstrator’s novel response and an appetitive reinforcement and, subsequently, produced the same novel topographically matching behavior. Procedures designed to analyze observational learning basically resort to one of three categories: the ‘duplicate cage’ procedure, the ‘non-exposed control procedure’ and the ‘pattern control procedure’. In experiments using the ‘duplicate cage’ procedure, a demonstrator and an observer are kept in separate but identical experimental enclosures fitted with identical response and reinforcement devices. Demonstrators and observers thus remain in sight of each other as demonstration and imitation attempts go on (as in the above described emulation case). In experiments using the ‘non-exposed control’ procedure, observer animals watch models perform from a separate and ‘nude’ enclosure, whereas controls are not exposed to demonstrators, but only to the apparatus operations. With the ‘pattern control’ procedure,
99
one manipulandum is present, as in the second procedure, but this manipulandum has particular properties: it can be used in two or several ways. Pushing a joystick in one or the other direction, as in the bi-directional control procedure of Heyes and Dawson (1990), is a good example. Whereas the second procedure does not provide a control for local or stimulus enhancement (learning rate may increase by autoshaping of the response or because the attention of the observer was attracted to a particular feature in the environment), the third does: the response device must not only be manipulated, but the nature of the behavior (lift the cover with the beak or the paw) or its directional patterning (push to the left or to the right) are determinant. The experiment described hereafter addresses for the first time the social learning of a measure of time. Living organisms do not have a time ‘sense’ and time is a dimension of every phenomenon or event. However, it might happen that only their durations can allow organisms to discriminate between two events which otherwise share common features, and it is commonly argued that time discrimination is indispensable to survival. It thus is reasonable to assume that living organisms possess mechanisms specifically devoted to measuring time (for classical animal data, see Richelle and Lejeune, 1980; Gibbon and Allan, 1984; more recent perspectives and human data are discussed, for instance, in Block, 1990; Macar et al., 1992; Lejeune and Macar, 1993; Helfrich, 1996). In particular, the role played by attention in time estimation has been highlighted in animals and humans (Meck, 1983; Macar et al., 1994). Methods have long been developed to test temporal accuracy and sensitivity of animals or humans to time. One of them, the temporal discrimination procedure, was used here (Church et al., 1976). Demonstrator rats were trained to listen to a short or a long sound, before two retractable response levers (‘A’ and ‘B’) where simultaneously introduced in the experimental enclosure. If the sound stimulus had been short (1 s) food reinforcement followed a press on lever ‘A’; if it had been long (8 s), a press on lever ‘B’ was reinforced, and vice versa. Thereafter, ‘naive’ rats
100
F. Simons, H. Lejeune / Beha6ioural Processes 41 (1997) 97–105
observed from a ‘nude’ adjacent compartment a conspecific model performing with high efficiently (94 – 100% correct presses, depending upon the session or the subject). The demonstrator was then removed and the observer rat was put in the demonstration compartment for a series of discrimination trials. With regard to the procedure categories distinguished above, the experimental design followed here can be included within the non-exposed control category. The possible influence of stimulus enhancement, autoshaping or incidental learning was reduced by shaping observer and control rats on both levers, prior to their exposure to the experimental conditions. As the observer rats already mastered the leverpress – food (R–RF) relationship (which was not the case in the series of experiments by Heyes and collaborators), the one and only relevant information was the demonstrator’s strategy with regard to the short and long sounds. Previous leverpress training, indeed, potentially increased the likelihood of true imitative social learning in the explanation of observer rats’ time discrimination behavior.
2. Materials and methods
2.1. Subjects Sixteen naive 5-month-old male Wistar albino rats were randomly assigned to the ‘observer’ or ‘control’ groups. Five other male rats (10-monthold) were the ‘demonstrators’. All animals were maintained at 85% of free-feeding weight and had free access to water in their home cage. They were kept on a 12-h light/dark cycle (lights on 06:30 h).
be protruded in the chamber or retracted in 0.75 s. Retractable levers were used to prevent responding before the end of the sound signal. Neither response devices nor food cup were located in the observation compartment. Observer or control rats were thus not reinforced while watching the model or the operation of the apparatus. A loudspeaker was placed 350 mm above the food dispenser. It delivered a 4000 Hz, 40 dB tone (Kelly and Mastreton, 1977) of 1 (short signal), or 8 s (long signal). Results were collected on an 8086 PC.
2.3. Procedure 2.3.1. Training of the ‘demonstrator’ rats The five demonstrator rats had an experimental history on a Fixed-Interval 60-s schedule. Errorless discrimination training took place over five consecutive 40-trial sessions (1–5). In these sessions, the 1 or 8 s sounds were delivered and followed by the presentation of the correct lever. The left lever was arbitrarily associated to the 8 s signal for three demonstrators, and to the short signal for the remaining two. The correct lever remained accessible until the first response was given or a maximum delay of 60 s. This errorless procedure was maintained until each sound stimulus was followed by a leverpress. On the next 25 days, both levers were simultaneously presented after each stimulus duration and rats were exposed to 60-trial sessions twice a day (sessions 6–54). A correction procedure was used: each error was followed by the same trial until a cor-
2.2. Apparatus Animals were trained and tested in a long perspex chamber (80 ×40 ×40 cm) with an aluminum grid floor, as shown in Fig. 1. This chamber was divided in two compartments of equal size by a transparent partition. In the left compartment, two identical retractable levers were located at 7 cm on either side of a food tray, and 5 cm above the floor. Each lever required a 20-g force to be depressed. These two levers could
Fig. 1. Perspex test chamber.
F. Simons, H. Lejeune / Beha6ioural Processes 41 (1997) 97–105
rect response was recorded. Sounds were randomly scheduled, with the restriction that a same duration could not be presented three times consecutively (except in the correction mode). Each trial was followed by an Inter-Trial-Interval (ITI) of 10–20 s. From session 22, a ‘spectator’ rat was placed in the observer compartment to accustom the demonstrator to the proximity of a conspecific. During the next four sessions (23 – 26), demonstrators were influenced by the spectators, as the response latencies increased. Thereafter, habituation to the presence of a conspecific developed and demonstrators performed with short response latencies and an efficiency of 94 – 100%, depending on the session and the subject.
2.3.2. Training of the ‘obser6er’ and ‘control’ rats Observers and control rats underwent a hand shaping procedure to leverpress for food pellets. Half of the animals of each group were shaped on the left and the other half on the right lever. After shaping and to avoid any lever preference, the location of the inserted lever was changed from one session to the next. In the first four training sessions (session 1– 4) the lever was protruded into the chamber before the animal went in and was not retracted. Each leverpress was reinforced and this training stopped after 30 food pellets were earned. At the end of these four sessions, each animal readily pressed both levers with a response latency less than three seconds. They were then accustomed to the lever movements. On sessions 5–8, the rats were introduced into the chamber before a lever was presented. The lever remained accessible until 30 responses were made (as previously, each response was reinforced). Thereafter, in the same session, the lever was briefly retracted before being presented again until 15 responses were made. It was then again retracted after ten and eventually five responses were produced by the rat. During this phase, the inserted lever was changed from one session to the next, as previously. Finally, both levers were presented simultaneously during two sessions of 40 trials each (11–12). At the end of training, observers were assigned to the demonstrators. As only five demonstrators were available for eight observer rats, three of them (A, B and C, see Table 1) ‘instructed’ two experimental animals.
101
Table 1 From left to right, demonstrators (with their 8 s lever, left or right) assigned to observer rats, and control rats paired to the observer animals Demonstrators
8-s Lever
Observers
Controls
A
R
B
R
C
L
D E
L L
O1 O2 O3 O4 O5 O6 O7 O8
C1 C2 C3 C4 C5 C6 C7 C8
2.4. Testing The experiment started the day after the last training session and lasted for 14 daily sessions. The rats worked 7 days a week. The first three sessions lasted for 50 and the next eleven for 60 trials. Each session was divided in two parts. In the first one, called ‘observational part’, a demonstrator performed the task (30 trials) while an observer was in the observational chamber. The ‘test part’ followed: the demonstrator was removed and the observer was placed in the testing chamber to perform the same task. No correction mode was used. For control rats, the test chamber was empty during the observational phase, but the computer monitored the sounds, ejected and quickly retracted the levers and distributed reinforcers on 95% of the trials, to mimic the apparatus operations of a demonstrator session.
3. Results The session duration, the trial durations, the responses latencies, the total number of responses and the number of correct responses on the left and right levers were recorded during each session. The mean trial duration did not differ between groups and responses were recorded on 99% of the trials. Response latency was defined as the time elapsed between the lever protrusion and the
102
F. Simons, H. Lejeune / Beha6ioural Processes 41 (1997) 97–105
first leverpress. This latency quickly became shorter than 0.1 s, i.e. shorter than the rat’s reaction time. These data could be explained by a mechanical artifact. Animals started to press the lever as it was still moving, before a response could actually be recorded. As this became possible, the lever was already depressed, which explains the extremely short average latencies. We can observe, on the left side of Fig. 2, that the mean response latencies on levers A and B were not significantly different (F(1, 8) =0.03, P = 0.95). However, the right side of Fig. 2 shows that he mean latency on the short lever was twice as long as the mean latency on the long lever (F(1, 8)=7.29, PB 0.03). The mean performance of observer and control rats, as measured by the mean percentage of correct responses in the discrimination task, is displayed in Fig. 3. Visual inspection shows that, after a few sessions, learning curves diverged before converging again. Therefore, data were grouped into three blocks: sessions 1 – 6, 7 – 10 and, finally, 11–14. Within – between ANOVAs were computed separately for each block of data. The first block (sessions 1 – 6) yielded neither a session nor a group effect (F(5, 70) = 2.05, P = 0.082, and F(1, 14)=0.25, P =0.63, respectively). For the second data block (sessions 7 – 10), the ANOVA revealed significant effects of the session, the group, and a session ×group interaction (F(3, 42)= 8.36, PB 0.0002, F(1, 14) = 8.65, P B 0.02, and F(3, 42)=3.16, P B0.05, respectively). The last block (sessions 11 – 14) yielded only a significant session effect (F(3, 42) = 4.23, P B 0.02).
Fig. 2. Mean response latencies pooled over control and observer rats, in the four last sessions from the 14-session observational testing. * Significant difference at PB 0.03.
Fig. 3. Mean performance of observer and control rats as measured by the proportion of correct responses over successive sessions.
Another way to describe the results was to record, for each rat, the number of sessions needed to reach a performance criterion, such as 70% correct responses. This criterion cannot be reached haphazardly, as the probability of obtaining by chance 70% of correct responses on 60 trials is equal to 0.0008. Data from the observer and control rats were compared with the t-test. Differences were significant: observers reached the criterion earlier than controls (t(14)=0.571, PB 0.02). This differential evolution is illustrated in Fig. 4.
Fig. 4. Number of rats which reached 70% of correct responses, cumulated over successive sessions.
F. Simons, H. Lejeune / Beha6ioural Processes 41 (1997) 97–105
4. Discussion The aim of the present experiment was to investigate whether naive rats could learn by observation a duration discrimination task modeled by demonstrator conspecifics. Effects of demonstrators on the acquisition of a time discrimination by observer rats were found: first, their mean percent of correct responses was significantly higher than that of controls at training sessions 7 – 10; second, the learning rate was faster for observer rats, as they reached the 70% correct responses criterion significantly earlier than controls. Results shown on Fig. 3 are similar to those obtained with pigeons by Biederman and Vanayan (1988). In that experiment, four groups of observer pigeons were compared in the acquisition of a discrimination between an erect and an inverted triangle. These groups differed along two parameters: the observation of a proficient versus a non-proficient demonstrator, and the observation of the apparatus operation versus a demonstrator conspecific. In the first experiment, the four groups remained highly similar over the first 5 of 8 training sessions. Between – group differences became significant only thereafter (as can be seen in Fig. 1, p. 37), as was the case in our study. In particular, the main effect of proficiency was significant (watching a skilled versus an unskilled model), as was the main effect of yoking (watching the apparatus operations versus a conspecific model). Trying to explain how observer rats benefited from the demonstrator’s performance, we might first reject hypotheses that do not seem to fit the data. Firstly, stimulus enhancement might be questioned because observer and control rats were magazine-trained and shaped in the test cubicle prior to the demonstration and test sessions. Thus, both groups of rats already learned an R – Rf relationship involved in performing the task and might be considered as displaying similar interest towards the levers, the food cup and the experimental context. Further, as duration is an ubiquitous stimulus or event dimension and not a physical item such as a lever or a food cup, applying the stimulus enhancement concept to
103
time would require broadening it. However, as it seems likely that indices such as odor marks left by the demonstrators played a role and might be taken into account, stimulus enhancement cannot be completely discarded in the explanation of the above results. Second, social facilitation, i.e. an increase of behavior present in the repertoire of the animal, due to the mere presence of a conspecific can be eliminated, not only because observers were tested alone after each observation session, but also because the complex behavior pattern to be performed had to be learned and did not belong to the natural repertoire of the species. Third, as emulation was described so far only in chimpanzees, it would be farfetched speculation to resort to this hypothesis, particularly as in the emulation experiment reported above, and which used the ‘duplicate cage’ procedure, the model (the experimenter) and the observer (the chimpanzee) remained within sight of each other during the tests. The question remains of whether true imitative social learning might be involved. Before trying to answer this question, we might first describe how demonstrators behaved and consider what should be learned to master the duration discrimination task. All the demonstrators followed the same behavioral sequence. As soon as a sound stimulus was presented, they moved to the short lever side and stood in front of the aperture through which the short lever should be presented. If the short lever did not appear, they waited for a few more seconds before moving to the other side of the cubicle and facing the long lever location. This strategy was optimal: as the sounds ended, the rats stood in front of the correct lever. This response strategy might also explain the difference between short and long response latencies, displayed in Fig. 2: the rats had only a short time to be well oriented towards the short lever (1 s), whereas they faced the long lever before the end of the long duration stimulus. Merely copying the model’s displacements within the test chamber cannot lead to correct performance, because the key to proficient behavior is the mastery of the relationship between the duration of the sound stimulus and the displace-
104
F. Simons, H. Lejeune / Beha6ioural Processes 41 (1997) 97–105
ment pattern of the demonstrator rat. Similarly, measuring the duration of the demonstrator’s immobility in front of the right and left levers or memorizing a long sequence of behavior over successive trials is to no avail, as short and long stimuli were presented at random within and between sessions. Therefore, the contribution of ‘blind’ imitation in the mastery of the task could only be modest, with regard to the importance of the discovery of the relationship between particular behavior patterns and durations. There are two remaining hypotheses. The first suggests that imitative social learning took place, i.e. that observer rats learned more rapidly the relationship between a duration (short or long) and a particular behavior pattern displayed by the demonstrator in the test box. They, thus, might have more rapidly learned an S (sound duration) – R (displacement patterning) relationship that could be grafted on the leverpress – reinforcer link they mastered from the start of the experiment, before being caught up by control rats towards the end of the 14-session test. In other words, the first term of the already mastered leverpress – reinforcer (R–Rf) link was changed into a more elaborated behavioral pattern, conditional upon the duration of the previous sound stimulus. As controls only mastered the R – Rf link and were not exposed to a proficient demonstrator, they had to discover the complementary S – R relationship by trial and error, without the help of behavioral clues. The second hypothesis considers that proficiency of the observer rats might also be explained by the learning of an S – S relationship. For instance, they might have learned that, after a short tone (S1), movements (S2) of the left lever produced reward, and after a long tone, movements of the right lever had the same outcome. This would have rendered the sight of the left lever more appealing after a short tone (as would the sight of the right lever after a long tone), and, consequently, have induced approach to that lever and emission of the already mastered leverpress. Rats might thus have learned which lever movement (due to the demonstrator action) produced reward after one or the other sound duration. This conditional discrimination would have been
an instance of S–S learning, within the frame of instrumental conditioning. Even if this hypothesis does not at all put emphasis on imitating the demonstrator, it may play a determining role in the early discovery of the S–S link and of the key importance of time. Testing this hypothesis would involve control rats observing the mere apparatus operations, with, additional to the simultaneous protrusion of both levers, movement of the ‘correct’ lever associated to the just preceding duration stimulus, a condition similar to the one used in Heyes et al. (1994), where control rats could observe the correct joystick movements (to the left or to the right). The reasons why both groups of rats did not differ over the six first training sessions may be two-fold. Firstly, a stimulus enhancement process might have been as potent for observers than for controls. Such a hypothesis is supported by the fact that the importance of time (and thus its estimation) can only emerge progressively from the interaction between the animal and the temporal contingencies of the task. Another and complementary hypothesis should, however, not be disregarded: acquired equivalence learning. Indeed, control rats had not to pay attention to the short or long duration of the sound stimuli, as they had the same outcome: simultaneous protrusion of both levers. Thus, controls had to extinguish this learned equivalence while discovering the importance of the temporal dimension of the sound stimuli. Complementary experimentation to test this hypothesis should involve control rats hearing the tones, without seeing subsequent lever protrusion and retraction. This last hypothesis does, however, not exclude S–R or S–S learning in experimental rats, as explained above. It nevertheless suggests that differences between experimental and control animals might have been less evident. In conclusion, there is no doubt that both the observers and the controls eventually displayed behavior patterns highly similar to those of demonstrators, as casual observation showed, because the discrimination task does not leave much room for behavioral variation. However, displaying similar behavior patterns and proficiency levels was probably mediated by learning processes
F. Simons, H. Lejeune / Beha6ioural Processes 41 (1997) 97–105
which were partially different. Observing a proficient conspecific might have contributed to a more rapid discovery of the crucial relationship between a particular duration and its related response patterns (S – R), or to the more rapid learning of the relationship between the duration stimuli and their correlated lever movements (S – S). In any case, the attention of observer rats was directed earlier to the key importance of time.
Acknowledgements We are very grateful to John Wearden for his proofreading and to the referees for helpful comments. This paper is based on a dissertation submitted by the corresponding author, in partial fulfilment of the requirements for a master’s degree in biology at the University of Lie`ge.
References Biederman, G.B., Vanayan, M., 1988. Observational learning in pigeons: The function of quality of observed performance in simultaneous discrimination. Learn. Motiv. 19, 31–43. Block, R.A. (Ed.) 1990. Cognitive models of psychological time. Lawrence Erlbaum, Hillsdale, NJ, p. 283. Church, R.M., Getty, D.J., Lerner, N.D., 1976. Duration discrimination by rats. J. Exp. Psychol. Anim. Behav. Proc. 2, 303 – 312. Clayton, D.A., 1978. Socially facilitated behavior. Q. Rev. Biol. 53, 373 – 391. Galef, B., 1988. Imitation in animals: history, definition and interpretation of data from psychological laboratory. In: Zentall, T.R., Galef, B.P. (Eds.), Social Learning: Psychological and Biological Perspectives, Lawrence Erlbaum, Hillsdale, NJ, pp. 3 – 28. Galef, B., 1990. Tradition in animals: Field observations and laboratory analyses. In: Beckoff, M., Jamieson, D. (Eds.), Interpretations and Explanations in the Study of Behaviour: Comparative Perspectives, Westview Press, Boulder, CO, pp. 74 – 95. Galef, B.G. Jr., Clark, M., 1971. Social factors in the poison avoidance and feeding behavior of wild and domesticated rats pup. J. Comp. Physiol. Psychol. 75, 341–357. Galef, B.G., Manzig, L.A., Field, R.M., 1986. Imitation learning in budgerigars: Dawson and Foss revisited. Behav. Proc. 13, 191 – 202. Gibbon, J., Allan, L., 1984. Timing and time perception. Ann. NY Acad. Sci. 423, 654. Helfrich, H. (Ed.) 1996. Time and Mind. Hogrefe and Huber, Seattle, WA, 209 pp.
105
Heyes, C.M., 1994. Social learning in animals: Categories and mechanisms. Biol. Rev. 69, 207 – 231. Heyes, C.M., Dawson, G.R., 1990. Demonstration of observational learning in rats using a bi-directional control. Q. J. Exp. Psychol. 42B, 59 – 71. Heyes, C.M., Dawson, G.R., Nokes, T., 1992. Imitation in rats: initial responding and transfer evidence. Q. J. Exp. Psychol. 45B, 229 – 240. Heyes, C.M., Jaldow, E., Nokes, T., Dawson, G.R., 1994. Imitation in rats (Rattus nor6egicus): The role of the demonstrator action. Behav. Proc. 32, 173 – 182. Itani, J., Nishimura, A., 1973. The study of infrahuman culture in Japan. In: Montana, W. (Ed.), Symp. 4th Int. Cong. Primatology, Precultural Primate Behaviour, Karger, Basel, pp. 26 – 50. Kawai, M., 1965. Newly acquired pre-cultural behaviour of the natural troop of Japanese monkeys on Koshima isle. Primates 6, 1 – 30. Kelly, J.B., Mastreton, B., 1977. Auditory sensitivity of the albinos rat. J. Comp. Physiol. Psychol. 91, 930 – 936. Lejeune, H., Macar, F., 1993. Temporal processes: Thematic issue. Psychologica Belgica 33 (2), 350. Logue, A.W., 1988. A comparison of taste aversion learning in humans and other vertebrates: Evolutionary pressures in common. In: Bolles, R.C., Beecher, M.D. (Ed.s), Evolution and Learning, Lawrence Erlbaum, Hillsdale, NJ, pp. 97 – 116. Macar, F., Grondin, S., Casini, L., 1994. Controlled attention sharing influences time estimation. Memory Cognition 22, 673 – 686. Macar, F., Pouthas, V., Friedman, W. J. (Eds.) 1992. Time, Action and Cognition: Towards Bridging the Gap, Kluwer Academic, Dordrecht, 407 pp. Meck, W.H., 1983. Selective adjustment of the speed of the internal clock and memory processes. J. Exp. Psychol. Anim. Behav. Proc. 9, 171 – 201. Mineka, S., Davidson, M., Cook, M., Keir, R., 1984. Observational conditioning of snake fear in rhesus monkeys. J. Abnorm. Psychol. 93, 355 – 372. Nagell, K., Olguin, R.S., Tomasello, M., 1993. Processes of social learning in the tool use of chimpanzees (Pan troglodytes) and human children (Homo sapiens). J. Comp. Psychol. 107, 174 – 186. Richelle, M., Lejeune, H. (Eds.) 1980. Time in Animal Behaviour. Pergamon Press, Oxford, 273 pp. Robert, M., 1990. Observational learning in fish, birds, and mammals: a classified bibliography spanning over 100 years of research. Psychol. Rec. 40, 289 – 311. Spence, K.W., 1937. Experimental studies of learning and higher mental processes in infra-human primates. Psychol. Bull. 34, 806 – 850. Thorpe, W., 1963. Learning and Instinct in Animals. 2nd ed. Methuen, London, 558 pp. Tomasello, M., Davis-Dasilva, M., Camak, L., Bard, K., 1987. Observational learning of tool use by young chimpanzees. Human Evol. 2, 175 – 183. Wood, D., 1989. Social interaction as tutoring. In: Bornstein, M., Bruner, J. (Eds.), Interaction in Human Development. Blackwell, London, pp. 59 – 80.