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Empathic learning of a passive-avoidance response in domesticated Rattus norvegicus
Anita. Behav., 1971, 19, 112-114
EMPATHIC LEARNING
OF A PASSIVE-AVOIDANCE
RESPONSE IN
DOMESTICATED RA TTUS NOR VEGICUS BY R I C H A R D LORE,* A N I U T A BLANC & P E T E R S U E D F E L D
Department of Psychology, Rutgers University, New Brunswick, New Jersey 08903 Abstract. Twelve experimental rats were exposed to demonstrator conspecifics learning to avoid physical contact with a lighted candle in an adjacent compartment. Control rats were also exposed to a lighted candle and a conspecific for comparable periods, but, in the control condition, the demonstrator animal could not contact the flame. Immediately after the exposure period a candle was placed in the observer animal's cage. The experimental rats made fewer physical contacts with the candle flame and learned to avoid the candle faster than control animals. These results indicate that domesticated rats learn a passive avoidance response faster after exposure to another animal acquiring the same response. A similar mechanism might account for the wild rat's ability to avoid traps and poisoned food. Attempts to eliminate wild rat populations by the use o f poisons or traps have not been particularly successful. Even the most comprehensive trapping and poison control programmes have produced only a temporary reduction in the target area's rat population. Several mechanisms have been proposed to account for the remarkable ability of these animals to avoid potentially harmful objects and situations. Barnett (1963) suggests that wild rats initially avoid any new object encountered in their home environment. Eventually, curiosity overcomes their fear and a small sample o f the poisoned food is eaten. If the animal recovers, the bait is avoided thereafter. Calhoun (1962) noted that some animals never enter or 'sample' traps even when the traps are present for long periods. He suggested that young rats can be influenced by the avoidance behaviour of their older associates. Similar conclusions were made earlier by Thompson (1953). Lorenz (1966) goes much further; he states t h a t ' . , the rat operates basically with the same methods as those of man, by traditional transmission of experience and its dissemination within the dose community' (p. 155). While Lorenz's assumptions appear unwarranted, it is possible that rats could learn to avoid a potentially harmful object by exposure to another animal's experiences with similar stimuli. The present experiment was designed to provide information on this question. As our pain stimulus, we chose a lighted candle because
inexperienced laboratory rats will readily approach and investigate this object (Lore 1969). In a typical session, the rat begins to approach the candle as soon as it is placed within the cage. After a brief pause, the rat slowly extends its nose into the base of the flame, then quickly withdraws and retreats to the far corner of the cage. The same sequence will be repeated several times during a brief time period. Rats learn to avoid the candle only after experiencing a number of mild burns about the head. Methods The subjects were forty-eight Long-Evans rats born and reared in the Douglass College colony. Between birth and weaning the rats were housed in large maternity cages. On day 21 the rats were placed in individual cages where they remained until the experiment began when they were 180 to 190 days old. The testing cage had metal sides, a wire mesh floor and a clear Plexiglas top. Two large compartments (19 x 33 x 33.5 cm) on either end were separated by a third, much narrower compartment (6"3 x 33 x 33.5 cm) by clear Plexiglas sides. The pain stimulus was a lighted candle (approximately 1.0 cm diameter and 11.4 cm long) mounted on a magnetic base so that it could be attached to the wire mesh floor of the cage. Each of the twelve experimental animals was placed in one large compartment of the test cage for a 20-min period. Then, a same-sex demonstrator rat and a lighted candle were placed into the second large compartment. The candle was located in the interior corner of the demonstrator's compartment so that it was as
*Present address: Department of Psychology, Virginia Commonwealth University, Richmond, Virginia 23220, U.S.A. 112
LORE ET AL.: EMPATHIC LEARNING IN RATS close as possible to the experimental rat's quarters. The demonstrator animal remained with the candle until he had successfully avoided the candle for a 20-min period. Immediately after removing the demonstrator from its compartment, a new candle was placed in the experimental animal's compartment; and the number of nose-flame contacts made before the animal successfully avoided the flame for 20 min was recorded. Twelve control rats were treated identically except that in the control group the candle was not accessible to the demonstrator because it was located in the small middle compartment. Thus, the control and experimental animals were both exposed to another rat and a lighted candle for comparable time periods, but only the experimental group had the opportunity to see the demonstrator actually contact and learn to avoid the lighted candle. There were seven males and five females each in the experimental, control, and two demonstrator groups. Results
Table I indicates that the experimental group made fewer nose-flame contacts and reached the avoidance criterion faster than either the control or the demonstrator animals for the experimental group. An analysis of variances of the nose-flame contacts revealed significant Table I. Performance in the Candle-Avoidance Test
Group
Mean (so) Time (SD) taken number to avoid of nose-flame candle for 20 contacts consecutiveman
Experimental
2.92 (1.55)
24.1 (8;9)
Control
4"83 (2-55)
31 "8 (11'2)
Demonstrators (for experimental subjects only)
5.33 (2.07)
31"5 (9.2)
differences between
the
groups
(F=4.09,
df= 2/33, P<0-03). Multiple t-tests indicated that the experimental animals made significantly fewer contacts than the other two groups which did not differ from one another. Similarly, an analysis of variance of the reciprocals of the time to reach criterion measure was significant (F = 8.72, df= 2/33, P<0.001). Again, multiple t-tests demonstrated significance only between the experimental animals and the remaining two groups.
113
Discussion
Our results indicate that Rattus norvegicus can acquire a passive avoidance response much faster if it has been exposed to a conspecific learning the same response. A similar mechanism might account for the wild rat's successful avoidance of traps or poisoned food and thus be of considerable survival value for the species. The question of precisely how the experimental animals benefited from the demonstrator's experience has not been isolated in this study. Rats may be capable of true imitative behaviour but this higher order ability does not have to be invoked to explain the present results. Perhaps the demonstrator's experiences with the candle serve to direct the attention of the observer to the pain stimulus. We did not formally record the behaviour of the observer animals during the demonstration phase of the study, but informal observations indicated that the introduction of the demonstrator sharply reduced the cage exploration activity of the observer rat and directed its attention to the demonstrator. On several occasions, the demonstrator's rapid withdrawal from the flame elicited a startle from the observer and seemed to sustain its visual orientation towards the demonstrator. It is likely that some aspect of the demonstrator's behaviour serves as a cue which induces fear in the nearby animal. The increased fear then makes for better performances at simple avoidance tasks. It is important to note that all of the experimental animals contacted the flame at least once. Hence, it is unlikely that these animals somehow 'knew' that the candle had to be avoided prior to actually contacting the flame. Rather, it appears that the demonstrator's experiences somehow alerted the experimental animals to be wary of the test environment. Although imitation learning of a passive avoidance response has not been previously demonstrated in this species, prior work indicates that inexperienced rats do behave differently when exposed to a fearful conspecifie (Davitz & Mason 1955). It would be interesting to isolate precisely how the fearful animal communicates this mood change to the observer. The hooded rats used in this study have pigmented eyes and hence their visual acuity is superior to that of albino rats (Lashley 1930). There is evidence that hooded rats learn to lever press for food faster if they have been exposed to a trained rat performing the same response
114
ANIMAL
BEHAVIOUR,
in an adjacent cage (Corson 1967), but Powell (1968) could not replicate Corson's results with albino rats. Apparently, visual cues are effective only in rats that possess good visual acuity. Perhaps olfactory or auditory cues emitted by the demonstrator while learning to avoid the candle are important. However, even after experiencing a burn, our animals seldom emitted any audible sounds so it appears unlikely that the superior performance of the experimental rats was mediated by distress squeals. More interesting is the possibility that the demonstrator animals emit an alarm pheromone that enhances the acquisition of a simple avoidance response. In this study, any change in the quality or intensity of the odour of the demonstrator animal would have been present in the experimental rat's compartment because the hardware cloth floor of the test apparatus did permit the free exchange of air. Alarm pheromones have not been clearly demonstrated in any mammalian species, but rats can be taught to discriminate between the odour of stressed and non-stressed rats (Valenta & Rigby 1968) and Carr, Martorano & Krames (1970) have recently reported findings which suggest that the odour of stressed mice releases a withdrawal response in conspecifics. If olfactory cues are sufficient, then the observer would not have to be in visual contact with the demonstrator nor would the demonstrator even have to learn the same avoidance task. For example, observer animals may avoid a dangerous object in their environment, more effectively by simply being exposed to the odour of demonstrator animals receiving electric shock.
19,
t
Acknowledgments This study was supported in part by Public Health Service Research Grant 17249, and in part by a grant from the Rutgers Research Council to R. Lore.
REFERENCES Barnett, S. A. (1963). The Rat: A Study in Behavior. Chicago: Aldine Publishers. Calhoun, J. B. (1962). The Ecology and Sociology of the Norway Rat. Public. Health Service Publication No. 1008. Carr, W. J., Martorano, R. D. & Krames, L. (1970). Responses of mice to odors associated with stress. J. comp. physiol. Psychol., 71, 223-228. Corson, J. A. (1967). Observational learning of a lever pressing response. Psyehon. Sci., 7, 197-198. Davitz, J. R. & Mason, D. J. (1955). Socially facilitated reduction of a fear response in rats. J. eomp. Physiol. Psychol., 48, 149-151. Lashley, K. S. (1930). The comparative visual acuity of pigmented and albino rats. J. genet. Psyehol., 37, 481--484. Lore, R. K. (1969). Pain Avoidance behavior of rats reared in restricted and enriched environments. Dev. Psychol., 1, 482-484. Lorenz, K..1966). On Aggression. New York: Bantam Books. Powell, R. W. (1968). Observational learning versus shaping: A replication. Psychon. Sci., 10, 263-264. Thompson, H. V. (1953). Experimental live trapping of rats, with observations of their behaviour. Br. J. anita. Behav., 1, 96-111. Valenta, J. G. & Rigby, M. K. (1968). Discrimination of the odor of stressed rats. Science, N.Y., 161, 599-601. (Received 23 February 1970; revised 14 July 1970; seeond revision 8 September 1970MS. number: A951)
EMPATHIC LEARNING
OF A PASSIVE-AVOIDANCE
RESPONSE IN
DOMESTICATED RA TTUS NOR VEGICUS BY R I C H A R D LORE,* A N I U T A BLANC & P E T E R S U E D F E L D
Department of Psychology, Rutgers University, New Brunswick, New Jersey 08903 Abstract. Twelve experimental rats were exposed to demonstrator conspecifics learning to avoid physical contact with a lighted candle in an adjacent compartment. Control rats were also exposed to a lighted candle and a conspecific for comparable periods, but, in the control condition, the demonstrator animal could not contact the flame. Immediately after the exposure period a candle was placed in the observer animal's cage. The experimental rats made fewer physical contacts with the candle flame and learned to avoid the candle faster than control animals. These results indicate that domesticated rats learn a passive avoidance response faster after exposure to another animal acquiring the same response. A similar mechanism might account for the wild rat's ability to avoid traps and poisoned food. Attempts to eliminate wild rat populations by the use o f poisons or traps have not been particularly successful. Even the most comprehensive trapping and poison control programmes have produced only a temporary reduction in the target area's rat population. Several mechanisms have been proposed to account for the remarkable ability of these animals to avoid potentially harmful objects and situations. Barnett (1963) suggests that wild rats initially avoid any new object encountered in their home environment. Eventually, curiosity overcomes their fear and a small sample o f the poisoned food is eaten. If the animal recovers, the bait is avoided thereafter. Calhoun (1962) noted that some animals never enter or 'sample' traps even when the traps are present for long periods. He suggested that young rats can be influenced by the avoidance behaviour of their older associates. Similar conclusions were made earlier by Thompson (1953). Lorenz (1966) goes much further; he states t h a t ' . , the rat operates basically with the same methods as those of man, by traditional transmission of experience and its dissemination within the dose community' (p. 155). While Lorenz's assumptions appear unwarranted, it is possible that rats could learn to avoid a potentially harmful object by exposure to another animal's experiences with similar stimuli. The present experiment was designed to provide information on this question. As our pain stimulus, we chose a lighted candle because
inexperienced laboratory rats will readily approach and investigate this object (Lore 1969). In a typical session, the rat begins to approach the candle as soon as it is placed within the cage. After a brief pause, the rat slowly extends its nose into the base of the flame, then quickly withdraws and retreats to the far corner of the cage. The same sequence will be repeated several times during a brief time period. Rats learn to avoid the candle only after experiencing a number of mild burns about the head. Methods The subjects were forty-eight Long-Evans rats born and reared in the Douglass College colony. Between birth and weaning the rats were housed in large maternity cages. On day 21 the rats were placed in individual cages where they remained until the experiment began when they were 180 to 190 days old. The testing cage had metal sides, a wire mesh floor and a clear Plexiglas top. Two large compartments (19 x 33 x 33.5 cm) on either end were separated by a third, much narrower compartment (6"3 x 33 x 33.5 cm) by clear Plexiglas sides. The pain stimulus was a lighted candle (approximately 1.0 cm diameter and 11.4 cm long) mounted on a magnetic base so that it could be attached to the wire mesh floor of the cage. Each of the twelve experimental animals was placed in one large compartment of the test cage for a 20-min period. Then, a same-sex demonstrator rat and a lighted candle were placed into the second large compartment. The candle was located in the interior corner of the demonstrator's compartment so that it was as
*Present address: Department of Psychology, Virginia Commonwealth University, Richmond, Virginia 23220, U.S.A. 112
LORE ET AL.: EMPATHIC LEARNING IN RATS close as possible to the experimental rat's quarters. The demonstrator animal remained with the candle until he had successfully avoided the candle for a 20-min period. Immediately after removing the demonstrator from its compartment, a new candle was placed in the experimental animal's compartment; and the number of nose-flame contacts made before the animal successfully avoided the flame for 20 min was recorded. Twelve control rats were treated identically except that in the control group the candle was not accessible to the demonstrator because it was located in the small middle compartment. Thus, the control and experimental animals were both exposed to another rat and a lighted candle for comparable time periods, but only the experimental group had the opportunity to see the demonstrator actually contact and learn to avoid the lighted candle. There were seven males and five females each in the experimental, control, and two demonstrator groups. Results
Table I indicates that the experimental group made fewer nose-flame contacts and reached the avoidance criterion faster than either the control or the demonstrator animals for the experimental group. An analysis of variances of the nose-flame contacts revealed significant Table I. Performance in the Candle-Avoidance Test
Group
Mean (so) Time (SD) taken number to avoid of nose-flame candle for 20 contacts consecutiveman
Experimental
2.92 (1.55)
24.1 (8;9)
Control
4"83 (2-55)
31 "8 (11'2)
Demonstrators (for experimental subjects only)
5.33 (2.07)
31"5 (9.2)
differences between
the
groups
(F=4.09,
df= 2/33, P<0-03). Multiple t-tests indicated that the experimental animals made significantly fewer contacts than the other two groups which did not differ from one another. Similarly, an analysis of variance of the reciprocals of the time to reach criterion measure was significant (F = 8.72, df= 2/33, P<0.001). Again, multiple t-tests demonstrated significance only between the experimental animals and the remaining two groups.
113
Discussion
Our results indicate that Rattus norvegicus can acquire a passive avoidance response much faster if it has been exposed to a conspecific learning the same response. A similar mechanism might account for the wild rat's successful avoidance of traps or poisoned food and thus be of considerable survival value for the species. The question of precisely how the experimental animals benefited from the demonstrator's experience has not been isolated in this study. Rats may be capable of true imitative behaviour but this higher order ability does not have to be invoked to explain the present results. Perhaps the demonstrator's experiences with the candle serve to direct the attention of the observer to the pain stimulus. We did not formally record the behaviour of the observer animals during the demonstration phase of the study, but informal observations indicated that the introduction of the demonstrator sharply reduced the cage exploration activity of the observer rat and directed its attention to the demonstrator. On several occasions, the demonstrator's rapid withdrawal from the flame elicited a startle from the observer and seemed to sustain its visual orientation towards the demonstrator. It is likely that some aspect of the demonstrator's behaviour serves as a cue which induces fear in the nearby animal. The increased fear then makes for better performances at simple avoidance tasks. It is important to note that all of the experimental animals contacted the flame at least once. Hence, it is unlikely that these animals somehow 'knew' that the candle had to be avoided prior to actually contacting the flame. Rather, it appears that the demonstrator's experiences somehow alerted the experimental animals to be wary of the test environment. Although imitation learning of a passive avoidance response has not been previously demonstrated in this species, prior work indicates that inexperienced rats do behave differently when exposed to a fearful conspecifie (Davitz & Mason 1955). It would be interesting to isolate precisely how the fearful animal communicates this mood change to the observer. The hooded rats used in this study have pigmented eyes and hence their visual acuity is superior to that of albino rats (Lashley 1930). There is evidence that hooded rats learn to lever press for food faster if they have been exposed to a trained rat performing the same response
114
ANIMAL
BEHAVIOUR,
in an adjacent cage (Corson 1967), but Powell (1968) could not replicate Corson's results with albino rats. Apparently, visual cues are effective only in rats that possess good visual acuity. Perhaps olfactory or auditory cues emitted by the demonstrator while learning to avoid the candle are important. However, even after experiencing a burn, our animals seldom emitted any audible sounds so it appears unlikely that the superior performance of the experimental rats was mediated by distress squeals. More interesting is the possibility that the demonstrator animals emit an alarm pheromone that enhances the acquisition of a simple avoidance response. In this study, any change in the quality or intensity of the odour of the demonstrator animal would have been present in the experimental rat's compartment because the hardware cloth floor of the test apparatus did permit the free exchange of air. Alarm pheromones have not been clearly demonstrated in any mammalian species, but rats can be taught to discriminate between the odour of stressed and non-stressed rats (Valenta & Rigby 1968) and Carr, Martorano & Krames (1970) have recently reported findings which suggest that the odour of stressed mice releases a withdrawal response in conspecifics. If olfactory cues are sufficient, then the observer would not have to be in visual contact with the demonstrator nor would the demonstrator even have to learn the same avoidance task. For example, observer animals may avoid a dangerous object in their environment, more effectively by simply being exposed to the odour of demonstrator animals receiving electric shock.
19,
t
Acknowledgments This study was supported in part by Public Health Service Research Grant 17249, and in part by a grant from the Rutgers Research Council to R. Lore.
REFERENCES Barnett, S. A. (1963). The Rat: A Study in Behavior. Chicago: Aldine Publishers. Calhoun, J. B. (1962). The Ecology and Sociology of the Norway Rat. Public. Health Service Publication No. 1008. Carr, W. J., Martorano, R. D. & Krames, L. (1970). Responses of mice to odors associated with stress. J. comp. physiol. Psychol., 71, 223-228. Corson, J. A. (1967). Observational learning of a lever pressing response. Psyehon. Sci., 7, 197-198. Davitz, J. R. & Mason, D. J. (1955). Socially facilitated reduction of a fear response in rats. J. eomp. Physiol. Psychol., 48, 149-151. Lashley, K. S. (1930). The comparative visual acuity of pigmented and albino rats. J. genet. Psyehol., 37, 481--484. Lore, R. K. (1969). Pain Avoidance behavior of rats reared in restricted and enriched environments. Dev. Psychol., 1, 482-484. Lorenz, K..1966). On Aggression. New York: Bantam Books. Powell, R. W. (1968). Observational learning versus shaping: A replication. Psychon. Sci., 10, 263-264. Thompson, H. V. (1953). Experimental live trapping of rats, with observations of their behaviour. Br. J. anita. Behav., 1, 96-111. Valenta, J. G. & Rigby, M. K. (1968). Discrimination of the odor of stressed rats. Science, N.Y., 161, 599-601. (Received 23 February 1970; revised 14 July 1970; seeond revision 8 September 1970MS. number: A951)