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Habituation under different levels of stimulation in socially reared and isolated rats: A test of the arousal hypothesis
BEHAVIORAL BIOLOGY 2 2 , 553--558 (1978)
BRIEF REPORT Habituation under Different Levels of Stimulation in Socially Reared and Isolated Rats: A Test of the Arousal Hypothesis I DOROTHY E I N O N AND M . J. MORGAN
Department of Psychology, University of Durham, Durham DHI 3LE, England If animals reared in social isolation are more aroused by novel stimulation than animals raised in social groups, increasing the level of stimulation for the social ~, animals should produce a behavioral profile which is similar to that of isolates. In a test of this hypothesis, activity in an open field was examined in socially isolated and socially reared rats at three different levels of stimulation. The results are interpreted as supporting the hypothesis that isolates are hyperaroused.
An interesting explanation of the effects of differential rearing upon brain and behavior in the laboratory rat has recently been put forward by Walsh and Cummins (1975). They suggest that during the course of differential rearing enriched rats are subject to more arousal than isolated rats, and that through a process of adaptation the environment rich in arousal-inducing stimuli eventually results in a reduced reactivity to stimulation. Thus socially reared rats who are subjected to more arousal during the course of differential rearing are subsequently less apt to exhibit arousal reactions on exposure to novel stimulation. This proposal is in agreement with earlier suggestions that differential experience may influence "arousal" in response to subsequent experimental stimulation (Fentress, 1968a, b; Lockard, 1963; D'Amato and Jagoda, 1962; Bauman et al., 1969; Melzack, 1969). There is a certain amount of evidence which confirms that isolation reared rats are more highly aroused by novel stimulation. Isolates are both hyperactive (Morgan, 1973) and slower to habituate (Einon et al., 1975; Einon and Morgan, 1976) in the open field. They are also more ' This work was supported by a grant from the Science Research Council. We thank Professor Zangwill l'or the facilities of the Psychological Laboratory at the University of Cambridge. 553 0091-6773/78/0224-0553502.00/0 Copyright ~) 1978 by Academic Press, Inc. All rights of reproduction in any form reserved.
554
EINON AND MORGAN
susceptible to CNS stimulants (Sahakian et al., 1975) and less susceptible to certain CNS depressants (Friedman and Walker, 1969). If the differences in open field activity are to be attributed to the greater arousal potential of novel stimulation in the isolate, it should be possible to produce in socially reared animals behavioral profiles which are similar to those of isolated animals by increasing the arousal potential of the testing situation. Socially reared animals tested in a highly arousing situation should behave more like isolated rats. In the following experiment we test this hypothesis by examining the open field activity of socially reared and isolated rats at three increasing levels of auditory and visual stimulation. Each of six litters of hooded rats (Animal Suppliers Ltd.) was divided into Isolated (ISOL) and Social (SOC) rearing conditions. There were 12 males and 12 females in each condition. Details of the rearing and weaning procedures are given by Morgan et al. (1975). From weaning until the time of testing all animals were kept in standard plastic and mesh cages (Noah Kent Plastics, RB 1,45 x 28 x 22 cm), the social rats in groups of four and the isolates individually. The cages allowed visual and auditory but not tactile contact between adjacent animals in the rack. All of the animals had previously served as subjects at 45 days in an investigation of the habituation of headpoking and of object-content in an open field. They were given the present test at 60 days of age. The open field, which the animals had previously met in an objectcontact test, measured 76.2 x 76.2 cm and was constructed of bakelite with a floor of steel rods 0.6 cm in diameter and 0.6 cm apart. Three levels of auditory and visual stimulation were provided. Under the " L o w " condition the room was illuminated by a single 40-W red bulb (T.75 log Ft. Lambs) and there was no deliberately introduced noise. In the "Medium" condition the room was illuminated by 2 fluorescent strip lights on the ceiling (0.75 log Ft. Lamb) and a loudspeaker on one wall provided 70 db of " w h i t e " masking noise at the level of the open field. In the " H i g h " condition a stroboscope (EMI Type 3C) positioned 36 in. above the field was set to flash at 7 Hz, and the masking noise at the level of the open field was 92 db. Each animal was tested in three sessions, one at each of the three levels of stimulation, in an order that was balanced among animals with respect to rearing and sex. An interval of 3 clear days elapsed between two successive tests. Each test consisted of a 7-rain period, during which the number of 15-cm squares traversed were counted separately for the first and last 3 rain. The data presented graphically in Fig. 1 show that female animals were generally more active than males, and isolates were more active than social rats. The activity levels of socially reared animals decreased with time under low and moderate levels of stimulation but less so under high
ISOLATION AND AROUSAL 50,
HIGH
MED
LOW
91•-- ~S'~--
4
125
555
ffl -- o'S----
1,1,1
=¢
MJIO0
I,-
I,~ 75
\
==C O' ¢,~
I
I,
50 40
.
1-3
.
.
.
.
5 - 7 1-3 5 - 7 1-3 5 - 7
SAMPLE FIG. 1. Open field activity in male and female rats reared in social isolation or small social groups. Rats are exposed to the open field for three separate 7-min periods under three different levels of stimulation. Activity is recorded for the first (1-3) and last (5-7) 3 min of each exposure. There were 3 clear days between exposures.
levels. Isolates showed the reverse result: Their activity declined under high levels of stimulation but less so under low and moderate levels. The suggestion of a complicated interaction between rearing condition, level of stimulation, and time sample was confirmed by the analysis of variance IF (2, 88) = 22.37, P < 0.001]. The analysis also revealed significant main effects of Rearing, [/7 (1,44) = 10.28, P < 0.01], Sex IF (1, 44) = 16.70, P < 0.001], and Time Samples [F (1, 44) = 149.2, P < 0.001] but not of level of stimulation. The interaction between Rearing condition and level, however, was significant IF (2, 88) = 6.54, P < 0.01] as were those between Rearing and Time Sample [F (1, 44) = 19.38, P < 0.001] and between sex, level, and time sample IF (2, 88) = 9.43, P < 0.001]. Newman-Keuls tests showed there were no significant differences between groups in the first time sample; in the second sample, social rats showed lower activity levels than the isolates under medium and low levels of stimulation (P < 0.001), but there was no difference under the high level. The drop in activity from first to second sample was significant (P < 0.01) in social animals under medium and low levels of stimulation and in isolates under high levels of stimulation. Socially reared animals maintained their activity under high levels of stimulation but dropped significantly in the other conditions. Isolates on the other hand dropped under high levels but not under lower ones. The main prediction of the study was confirmed, in that the social rats began under high levels of stimulation to show the same pattern of activity as isolates under low and medium levels. Thus at high levels the social
556
EINON AND MORGAN
animals, like isolates under low and medium levels, showed a much reduced decline in activity from the first to the second sample. This finding is consistent with the hypothesis that isolates have increased levels of arousal in the open field. The behavior of the isolated animals under the high level of stimulation requires some explanation. There was a significant decrement in activity between the first and second sample at this high level but not under lower levels of stimulation. Although the animals moved about less in the second sample, they were by no means inactive: There was a large increase in sniffing which was directed between the bars of the floor of the open field. This sniffing was typically emitted continuously and was sometimes confined to one area of the open field. This suggests that at very high levels of arousal the isolates suffered from a hyperstimulation effect, which resulted in a temporary suppression of locomotor activity. Such a possibility arises from the claim that isolates show "stereotyped" patterns of responding in reaction to lower doses of D-amphetamine than do their social counterparts (Sahakian et al., 1975). It is possible that tl~e effects of the drug are analogous to highly arousing sensory situations, such as those that produce "freezing" or "tonic immobility" (Gallup, 1974). "Stereotyping" is often accompanied by an abrupt decrement in gross motor activity, which is replaced by such actions as sniffing and gnawing. The behavior of the isolates in the second time sample reminded us of descriptions of this behavior, and we believe that the reversed difference between isolates and social animals in this period could possibly be explained along these lines. There is some independent evidence that the relationship between sensory stimulation and exploratory activity may be an inverted U-shaped function. CNS stimulants such as D-amphetamine increase activity at low doses while reducing it at higher doses. The drug-induced changes in behavior during the ascending limb of this curve differs in many respects from the behavior of the descending limb (Simpson and Iversen, 1971). In normal rats decrements in exploration over time have been reported when stimulation is low but not when stimulation is moderately high. Thus Halliday (1967) found that activity decrements occurred in a closed maze but not in the presumably more arousing elevated maze. The suggestion that activity may be reduced if stimulation levels are too high is supported by findings that activity decrements in early trials are most marked in more emotional animals (Williams and Russell, 1972) and by the finding that maze activity is reduced by electric shock (Sheldon, 1970). Suggestions of a nonmonotonic relationship between arousal and activation are not new. Nor is the concept without its critics (see Hinde, 1970; Bolles, 1975; Fentress, 1973). While accounting adequately for the present results the suggestion that the isolated rat is simply hyperaroused does not withstand closer examination. It would be difficult to explain the differ-
ISOLATION AND AROUSAL
557
e n c e s in r e v e r s a l l e a r n i n g ( M o r g a n , 1973; R o s e n s w e i g , 1971) in this way. W h a t little e v i d e n c e is a v a i l a b l e suggests t h a t h y p e r a r o u s a l m a y well i m p r o v e r e v e r s a l l e a r n i n g ( K u l i g a n d C a l h o u n , 1972; C a l h o u n , 1974). N o r , as w e h a v e a r g u e d e l s e w h e r e ( E i n o n et al., 1976) c a n the i s o l a t e s ' a l t e r e d s u s c e p t i b i l i t y to d r u g s b e e x p l a i n e d in t e r m s of a u n i t a r y deficit.
REFERENCES Baumal, I. De Feo, J. J., and Lal, H. (1969). Decreased potency of CNS depressants after prolonged social isolation. Psychopharrnacologia 15, 153-158. Bolles, R. C. (1975). "Theory of Motivation," 2nd ed. New York: Harper and Row. Calhoun, W. H. (1974). Methamphetamine's effect on SDR: Replication and extension. Bull. Psychon. Soc. 3, 78. D'Amato, M. R., and Jagoda, H. (1962). Effect of early exposure to photopic stimulation on brightness discrimination and exploratory behavior. J. Genet. Psychol. 101,267-271. Einon, D. F., and Morgan, M. J. (1976). Habituation of object contact in socially-reared and isolated rats. (Rattus Norvegicus). Anita. Behav. 24, 415-420. Einon, D. F., Morgan, M. J., and Sahakian, B. J. (1975). The development of intersession habituation and emergence in socially-reared and isolated rats. Develop. Psychobiol. 8, 553-559. Einon, D. F., Stewart, J., Atkins0n, S., and Morgan, M. J. (1976). Effect of isolation on barbiturate anaesthesia in the rat. Psychophramacology, 50, 85-88. Fentress, J. C. (1968a). Interrupted ongoing behavior in two species of vole (Microtus agrestis and Clethrionornys britannicus). I. Response as a function of preceeding activity and the context of an apparently 'irrelevant' motor pattern. Anim. Behav. 16, 135-153. Fentress, J. C. (1968b). Interrupted ongoing behavior in two species of vole. (Microtus agrestis and Clethrionomys britannicus). II. Extended analysis of motivational variables underlying fleeing and grooming behavior. Anim. Behav. 16, 154-167. Fentress, J. C. (1973). Specific and nonspecific factors in the causation of behavior. In P. P. G. Bateson and Peter H. Kopler (Eds.), "Perspectives in Ethology" New York: Plenum Press. Friedman, A. H., and Walker, C. H. (1969). Rat brain amines, blood histamine and glucose levels in relationship to circadian changes in sleep induced by pentobarbitol sodium. J. Physiol., London 202, 133-146. Gallup, G. C. (1974). Animal hypnosis: Factual status of a fictional concept. Psychol. Bull. 81, 837-853. Halliday, M. S. (1967). Exploratory behaviour in elevated and enclosed mazes. Quart. J. Exp. Psychol. 19, 254-263. Hinde, R. A. (1970). Animal Behaviour: A Synthesis of Ethology and Comparative Psychology, 2nd ed. New York: McGraw-Hill. Kulig, B. M., and Calhoun, W. H. (1972). Enhancement of successive discrimination reversal learning by methamphetamine. Psychopharmacologia 27, 233-240. Lockard, R. B. (1963). Some effects of light upon the behavior of rodents. Psychol. Bull. 60, 509-529. Melzack, R. (1969). The role of experience in emotional arousal. Ann. N. Y. Acad. Sci. 159, 852-859. Morgan, M. J. (1973). Effects of post-weaning environment on learning in the rat. Anita. Behav. 21, 429-442. Morgan, M. J., Einon, D. F., and Nicholas, D. (1975). Effects of isolation rearing on behavioural inhibition in the rat. Quart. J. Exp. Psychol. 25, 615-634.
558
EINON AND MORGAN
Rosensweig, M. R. (1971). Effects of environment on development of brain and behavior. In E. Tombach, L. R. Aronson, and E. Shaw (Eds.), "Biopsychology of Development." New York: Academic Press. Sahakian, B. J., Robbins, T. W., Morgan, M. J., and Iversen, S. D. (1975). The effects of psychomotor stimulants on stereotypy and locomotor activity in socially deprived and control rats. Brain Res. 84, 195-205. Sheldon, M. H. (1970). Effects of electric shock on rats' activity in familiar and unfamiliar environments. Quart. J. Exp. Psychol. 22, 374-377. Simpson, B. A., and Iversen, S. D. (1971). Effects of substantia nigra lesions on the locomotor and stereotypy responses to amphetamine. Nature New Biol. 230, 30-32. Walsh, R. N., and Cummins, R. A. (1975). Mechanisms mediating the production of environmentally induced brain changes. Psychol. Bull. 82, 986-1000. Williams, D. I., and Russell, P. A. (1972). Open field behaviour in rats: Effects of handling, sex and repeated testing. Brit. J. Psychol. 63, 593-596.
BRIEF REPORT Habituation under Different Levels of Stimulation in Socially Reared and Isolated Rats: A Test of the Arousal Hypothesis I DOROTHY E I N O N AND M . J. MORGAN
Department of Psychology, University of Durham, Durham DHI 3LE, England If animals reared in social isolation are more aroused by novel stimulation than animals raised in social groups, increasing the level of stimulation for the social ~, animals should produce a behavioral profile which is similar to that of isolates. In a test of this hypothesis, activity in an open field was examined in socially isolated and socially reared rats at three different levels of stimulation. The results are interpreted as supporting the hypothesis that isolates are hyperaroused.
An interesting explanation of the effects of differential rearing upon brain and behavior in the laboratory rat has recently been put forward by Walsh and Cummins (1975). They suggest that during the course of differential rearing enriched rats are subject to more arousal than isolated rats, and that through a process of adaptation the environment rich in arousal-inducing stimuli eventually results in a reduced reactivity to stimulation. Thus socially reared rats who are subjected to more arousal during the course of differential rearing are subsequently less apt to exhibit arousal reactions on exposure to novel stimulation. This proposal is in agreement with earlier suggestions that differential experience may influence "arousal" in response to subsequent experimental stimulation (Fentress, 1968a, b; Lockard, 1963; D'Amato and Jagoda, 1962; Bauman et al., 1969; Melzack, 1969). There is a certain amount of evidence which confirms that isolation reared rats are more highly aroused by novel stimulation. Isolates are both hyperactive (Morgan, 1973) and slower to habituate (Einon et al., 1975; Einon and Morgan, 1976) in the open field. They are also more ' This work was supported by a grant from the Science Research Council. We thank Professor Zangwill l'or the facilities of the Psychological Laboratory at the University of Cambridge. 553 0091-6773/78/0224-0553502.00/0 Copyright ~) 1978 by Academic Press, Inc. All rights of reproduction in any form reserved.
554
EINON AND MORGAN
susceptible to CNS stimulants (Sahakian et al., 1975) and less susceptible to certain CNS depressants (Friedman and Walker, 1969). If the differences in open field activity are to be attributed to the greater arousal potential of novel stimulation in the isolate, it should be possible to produce in socially reared animals behavioral profiles which are similar to those of isolated animals by increasing the arousal potential of the testing situation. Socially reared animals tested in a highly arousing situation should behave more like isolated rats. In the following experiment we test this hypothesis by examining the open field activity of socially reared and isolated rats at three increasing levels of auditory and visual stimulation. Each of six litters of hooded rats (Animal Suppliers Ltd.) was divided into Isolated (ISOL) and Social (SOC) rearing conditions. There were 12 males and 12 females in each condition. Details of the rearing and weaning procedures are given by Morgan et al. (1975). From weaning until the time of testing all animals were kept in standard plastic and mesh cages (Noah Kent Plastics, RB 1,45 x 28 x 22 cm), the social rats in groups of four and the isolates individually. The cages allowed visual and auditory but not tactile contact between adjacent animals in the rack. All of the animals had previously served as subjects at 45 days in an investigation of the habituation of headpoking and of object-content in an open field. They were given the present test at 60 days of age. The open field, which the animals had previously met in an objectcontact test, measured 76.2 x 76.2 cm and was constructed of bakelite with a floor of steel rods 0.6 cm in diameter and 0.6 cm apart. Three levels of auditory and visual stimulation were provided. Under the " L o w " condition the room was illuminated by a single 40-W red bulb (T.75 log Ft. Lambs) and there was no deliberately introduced noise. In the "Medium" condition the room was illuminated by 2 fluorescent strip lights on the ceiling (0.75 log Ft. Lamb) and a loudspeaker on one wall provided 70 db of " w h i t e " masking noise at the level of the open field. In the " H i g h " condition a stroboscope (EMI Type 3C) positioned 36 in. above the field was set to flash at 7 Hz, and the masking noise at the level of the open field was 92 db. Each animal was tested in three sessions, one at each of the three levels of stimulation, in an order that was balanced among animals with respect to rearing and sex. An interval of 3 clear days elapsed between two successive tests. Each test consisted of a 7-rain period, during which the number of 15-cm squares traversed were counted separately for the first and last 3 rain. The data presented graphically in Fig. 1 show that female animals were generally more active than males, and isolates were more active than social rats. The activity levels of socially reared animals decreased with time under low and moderate levels of stimulation but less so under high
ISOLATION AND AROUSAL 50,
HIGH
MED
LOW
91•-- ~S'~--
4
125
555
ffl -- o'S----
1,1,1
=¢
MJIO0
I,-
I,~ 75
\
==C O' ¢,~
I
I,
50 40
.
1-3
.
.
.
.
5 - 7 1-3 5 - 7 1-3 5 - 7
SAMPLE FIG. 1. Open field activity in male and female rats reared in social isolation or small social groups. Rats are exposed to the open field for three separate 7-min periods under three different levels of stimulation. Activity is recorded for the first (1-3) and last (5-7) 3 min of each exposure. There were 3 clear days between exposures.
levels. Isolates showed the reverse result: Their activity declined under high levels of stimulation but less so under low and moderate levels. The suggestion of a complicated interaction between rearing condition, level of stimulation, and time sample was confirmed by the analysis of variance IF (2, 88) = 22.37, P < 0.001]. The analysis also revealed significant main effects of Rearing, [/7 (1,44) = 10.28, P < 0.01], Sex IF (1, 44) = 16.70, P < 0.001], and Time Samples [F (1, 44) = 149.2, P < 0.001] but not of level of stimulation. The interaction between Rearing condition and level, however, was significant IF (2, 88) = 6.54, P < 0.01] as were those between Rearing and Time Sample [F (1, 44) = 19.38, P < 0.001] and between sex, level, and time sample IF (2, 88) = 9.43, P < 0.001]. Newman-Keuls tests showed there were no significant differences between groups in the first time sample; in the second sample, social rats showed lower activity levels than the isolates under medium and low levels of stimulation (P < 0.001), but there was no difference under the high level. The drop in activity from first to second sample was significant (P < 0.01) in social animals under medium and low levels of stimulation and in isolates under high levels of stimulation. Socially reared animals maintained their activity under high levels of stimulation but dropped significantly in the other conditions. Isolates on the other hand dropped under high levels but not under lower ones. The main prediction of the study was confirmed, in that the social rats began under high levels of stimulation to show the same pattern of activity as isolates under low and medium levels. Thus at high levels the social
556
EINON AND MORGAN
animals, like isolates under low and medium levels, showed a much reduced decline in activity from the first to the second sample. This finding is consistent with the hypothesis that isolates have increased levels of arousal in the open field. The behavior of the isolated animals under the high level of stimulation requires some explanation. There was a significant decrement in activity between the first and second sample at this high level but not under lower levels of stimulation. Although the animals moved about less in the second sample, they were by no means inactive: There was a large increase in sniffing which was directed between the bars of the floor of the open field. This sniffing was typically emitted continuously and was sometimes confined to one area of the open field. This suggests that at very high levels of arousal the isolates suffered from a hyperstimulation effect, which resulted in a temporary suppression of locomotor activity. Such a possibility arises from the claim that isolates show "stereotyped" patterns of responding in reaction to lower doses of D-amphetamine than do their social counterparts (Sahakian et al., 1975). It is possible that tl~e effects of the drug are analogous to highly arousing sensory situations, such as those that produce "freezing" or "tonic immobility" (Gallup, 1974). "Stereotyping" is often accompanied by an abrupt decrement in gross motor activity, which is replaced by such actions as sniffing and gnawing. The behavior of the isolates in the second time sample reminded us of descriptions of this behavior, and we believe that the reversed difference between isolates and social animals in this period could possibly be explained along these lines. There is some independent evidence that the relationship between sensory stimulation and exploratory activity may be an inverted U-shaped function. CNS stimulants such as D-amphetamine increase activity at low doses while reducing it at higher doses. The drug-induced changes in behavior during the ascending limb of this curve differs in many respects from the behavior of the descending limb (Simpson and Iversen, 1971). In normal rats decrements in exploration over time have been reported when stimulation is low but not when stimulation is moderately high. Thus Halliday (1967) found that activity decrements occurred in a closed maze but not in the presumably more arousing elevated maze. The suggestion that activity may be reduced if stimulation levels are too high is supported by findings that activity decrements in early trials are most marked in more emotional animals (Williams and Russell, 1972) and by the finding that maze activity is reduced by electric shock (Sheldon, 1970). Suggestions of a nonmonotonic relationship between arousal and activation are not new. Nor is the concept without its critics (see Hinde, 1970; Bolles, 1975; Fentress, 1973). While accounting adequately for the present results the suggestion that the isolated rat is simply hyperaroused does not withstand closer examination. It would be difficult to explain the differ-
ISOLATION AND AROUSAL
557
e n c e s in r e v e r s a l l e a r n i n g ( M o r g a n , 1973; R o s e n s w e i g , 1971) in this way. W h a t little e v i d e n c e is a v a i l a b l e suggests t h a t h y p e r a r o u s a l m a y well i m p r o v e r e v e r s a l l e a r n i n g ( K u l i g a n d C a l h o u n , 1972; C a l h o u n , 1974). N o r , as w e h a v e a r g u e d e l s e w h e r e ( E i n o n et al., 1976) c a n the i s o l a t e s ' a l t e r e d s u s c e p t i b i l i t y to d r u g s b e e x p l a i n e d in t e r m s of a u n i t a r y deficit.
REFERENCES Baumal, I. De Feo, J. J., and Lal, H. (1969). Decreased potency of CNS depressants after prolonged social isolation. Psychopharrnacologia 15, 153-158. Bolles, R. C. (1975). "Theory of Motivation," 2nd ed. New York: Harper and Row. Calhoun, W. H. (1974). Methamphetamine's effect on SDR: Replication and extension. Bull. Psychon. Soc. 3, 78. D'Amato, M. R., and Jagoda, H. (1962). Effect of early exposure to photopic stimulation on brightness discrimination and exploratory behavior. J. Genet. Psychol. 101,267-271. Einon, D. F., and Morgan, M. J. (1976). Habituation of object contact in socially-reared and isolated rats. (Rattus Norvegicus). Anita. Behav. 24, 415-420. Einon, D. F., Morgan, M. J., and Sahakian, B. J. (1975). The development of intersession habituation and emergence in socially-reared and isolated rats. Develop. Psychobiol. 8, 553-559. Einon, D. F., Stewart, J., Atkins0n, S., and Morgan, M. J. (1976). Effect of isolation on barbiturate anaesthesia in the rat. Psychophramacology, 50, 85-88. Fentress, J. C. (1968a). Interrupted ongoing behavior in two species of vole (Microtus agrestis and Clethrionornys britannicus). I. Response as a function of preceeding activity and the context of an apparently 'irrelevant' motor pattern. Anim. Behav. 16, 135-153. Fentress, J. C. (1968b). Interrupted ongoing behavior in two species of vole. (Microtus agrestis and Clethrionomys britannicus). II. Extended analysis of motivational variables underlying fleeing and grooming behavior. Anim. Behav. 16, 154-167. Fentress, J. C. (1973). Specific and nonspecific factors in the causation of behavior. In P. P. G. Bateson and Peter H. Kopler (Eds.), "Perspectives in Ethology" New York: Plenum Press. Friedman, A. H., and Walker, C. H. (1969). Rat brain amines, blood histamine and glucose levels in relationship to circadian changes in sleep induced by pentobarbitol sodium. J. Physiol., London 202, 133-146. Gallup, G. C. (1974). Animal hypnosis: Factual status of a fictional concept. Psychol. Bull. 81, 837-853. Halliday, M. S. (1967). Exploratory behaviour in elevated and enclosed mazes. Quart. J. Exp. Psychol. 19, 254-263. Hinde, R. A. (1970). Animal Behaviour: A Synthesis of Ethology and Comparative Psychology, 2nd ed. New York: McGraw-Hill. Kulig, B. M., and Calhoun, W. H. (1972). Enhancement of successive discrimination reversal learning by methamphetamine. Psychopharmacologia 27, 233-240. Lockard, R. B. (1963). Some effects of light upon the behavior of rodents. Psychol. Bull. 60, 509-529. Melzack, R. (1969). The role of experience in emotional arousal. Ann. N. Y. Acad. Sci. 159, 852-859. Morgan, M. J. (1973). Effects of post-weaning environment on learning in the rat. Anita. Behav. 21, 429-442. Morgan, M. J., Einon, D. F., and Nicholas, D. (1975). Effects of isolation rearing on behavioural inhibition in the rat. Quart. J. Exp. Psychol. 25, 615-634.
558
EINON AND MORGAN
Rosensweig, M. R. (1971). Effects of environment on development of brain and behavior. In E. Tombach, L. R. Aronson, and E. Shaw (Eds.), "Biopsychology of Development." New York: Academic Press. Sahakian, B. J., Robbins, T. W., Morgan, M. J., and Iversen, S. D. (1975). The effects of psychomotor stimulants on stereotypy and locomotor activity in socially deprived and control rats. Brain Res. 84, 195-205. Sheldon, M. H. (1970). Effects of electric shock on rats' activity in familiar and unfamiliar environments. Quart. J. Exp. Psychol. 22, 374-377. Simpson, B. A., and Iversen, S. D. (1971). Effects of substantia nigra lesions on the locomotor and stereotypy responses to amphetamine. Nature New Biol. 230, 30-32. Walsh, R. N., and Cummins, R. A. (1975). Mechanisms mediating the production of environmentally induced brain changes. Psychol. Bull. 82, 986-1000. Williams, D. I., and Russell, P. A. (1972). Open field behaviour in rats: Effects of handling, sex and repeated testing. Brit. J. Psychol. 63, 593-596.