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Effects of social isolation in adulthood on odor preferences and urine-marking in male rats
BEHAVIORAL AND NEURAL BIOLOGY 4 4 , 1 3 9 - 1 4 3
(1985)
BRIEF REPORT Effects of Social Isolation in Adulthood on Odor Preferences and Urine-Marking in Male Rats RICHARD E. BROWN 1 Department of Psychology, Dalhousie University, Halifax, Nova Scotia B3H 4J1, Canada Male rats isolated for 60 days in adulthood spent less time investigating odors of females and urine-marked less over these odors than did males kept in groups of three. Isolated males did not differ from grouped males in their responses to
odors of unfamiliar males or their own odors. After social experience the isolated males showed an increase in urine-marking but no change in odor preferences. Individual housing therefore appears to alter olfactory communication in the same way that it does other social behaviors and these changes may be mediated by the same mechanisms. © 1985 AcademicPress, Inc.
Male rats investigate objects scented with the odors of conspecifics and urine-mark more over these odors than over unscented objects or those with their own urine odor (Brown, 1975). Sexually experienced males investigate female odors more than sexually naive males, but both urine-mark over odors with equal intensity (Brown, 1977). Both odor investigation and urine-marking are inhibited by castration and reinstated by hormone replacement therapy (Brown, 1977, 1978). These results have led to the hypothesis that urine-marking by male rats is sexually motivated (Brown, 1977). Anosmia reduces the ability of rats to recognize conspecifics and leads to a reduction in aggressive and sexual behavior (Larsson, 1971; Flannelly & Blanchard, 1982). Social experiences during development interact with olfactory stimulation with the result that socially isolated anosmic males show almost no sexual behavior (Thor & Flannelly, 1977). Social isolation during adulthood also reduces the sexual performance of male rats (Chambers, Sengstake, Walther, & Bullis, 1982; deCatanzaro & Gorzalka, This research was supported by NSERC of Canada Grant A-7441. Grateful acknowledgment is given to Robin Kind and Sonya Major for their assistance in conducting the experiments and preparing the manuscript. 139 0163-1047/85 $3.00 Copyright © 1985 by Academic Press, Inc. All rights of reproduction in any form reserved.
140
RICHARD E. BROWN
1979), and the purpose of the present experiment is to examine whether social isolation in adulthood has a similar effect on odor investigation and urine-marking behaviors. Twelve male L o n g - E v a n s hooded rats were purchased from Charles River Canada (St. Constant, Quebec) at 90 days of age. Six of these males were housed singly in 18 x 24 x 18-cm metal cages with wiremesh fronts and floors and the other six were housed in groups of three in larger cages of the same design (41.5 × 24 x 18 cm high). All rats were kept under these conditions on ad lib. Purina lab chow and water and a 12:12 L:D cycle for 60 days before testing began. Odor preference and urine-marking tests were conducted in 23 x 43 x 16-cm plastic arenas which were placed on a Lucite table top covered with unprinted newspaper. Each rat was tested in a clean cage which contained a wire-mesh block at each end. These blocks measured 5 x 10 x 2.5 cm and were wrapped with a 20 x 20-cm piece of paper towel. Odors were presented by placing two drops (approximately 0.05 ml) of urine on the center of the paper-covered block. Urine was collected using a metabolism cage as described by Brown (1977) and the test procedure was the same as that used by Brown (1975). Each rat was tested for 5 min each day on 5 consecutive days. Day 1 was a habituation day and on the next 4 days the rats were presented with pairs of blocks. On three tests, one block was odorized with urine from a female rat (F), an unknown male rat (M), or the animal's own urine (O), and the second block was nonodorized or neutral (N). Urine from female donors was taken from all stages of the estrous cycle as previous research in this laboratory has shown that males spend as much time investigating urine from nonestrous females as they do that from estrous females (Brown 1977). F o r grouped males, own urine was the odor of at least two of the animals in the group. A fourth test used two nonodorized blocks. On each test, the time spent investigating each stimulus block was recorded in seconds using two cumulative time stopwatches operated by the experimenter. When the 5-min test was completed, the paper towel was r e m o v e d from each block, the urine marks were outlined in pencil, and the area covered by urine was calculated to the nearest 0.25 cm 2 using a plastic c o v e r plate as in previous studies (Brown, 1975, 1977, 1978). Correlated samples t tests were used to analyze the odor preferences of the isolated and grouped males on each of the four tests (Table 1). Female odors were investigated more than the nonodorized blocks by both grouped (t(5) = 6.34, p < .01) and isolated males (t(5) = 4.04, p < .01), as were male odors (grouped, t(5) = 2.43, p < .05; isolated, t = 8.51, p < .01). Neither grouped nor isolated males investigated their own odor more than the neutral odor (grouped, t(5) = 2.18; isolated, t(5) = 1.20) nor was one neutral block investigated more than the other
141
SOCIAL ISOLATION AND OLFACTION IN RATS TABLE 1 Mean Time in Seconds (-+ SE) Spent Investigating Each Stimulus Odor by Grouped and Isolated Males Odor pair Group
N
N
O
N
M
N
F
N
Grouped males
13.0 (9.6)
8.8 (2.8)
22.4 (9.2)
13.6 (3.9)
69.4* (24.8)
17.9 (4.8)
93.3** (i 1.4)
13.4 (3.7)
Isolated males
22.t (6.0)
17.3 (6.4)
20.3 (4.0)
15.0 (2.5)
13.2 (3.8)
57.3** (12.9)
12.0 (2.0)
11.8 (3.4)
15.7 (4.8)
11.2 (2.8)
10.9 (4.4)
12.8 (3.7)
51.5"* (10.5)
7.4 (1.9)
(preexperience) Isolated males
(postexperience)
65.0** (8.6) 44.2* (11.3)
Note. Abbreviations for odors: N = neutral odor; O = own odor; M = male odor; F = female odor. Correlated samples t test with df = 5. * p < .05. ** p < .01.
(grouped, t(5) = 1.23; isolated, t(5) = 1.08). When the preference scores (difference scores between the odorized and nonodorized blocks) for grouped and isolated males were compared on each test, it was found that grouped males had a greater preference for female odors than did isolated males (independent groups t-test, t(10) = 2.29, p < .05) but rats in the two groups did not differ in the time spent investigating odors of males (t(10) = 0.18) or their own odors (t(10) = 0.40). The area covered by urine-marks on each block was converted into c o m m o n logarithms (log (cm 2 + l)) for statistical analysis (Table 2). Group-housed males marked more over the odors of females than over TABLE 2 Mean Log Area (_+ SE) Covered by Urine Marks on Each Stimulus Block by Grouped and Isolated Males Odor pair Group
Grouped males Isolated males
(preexperience) Isolated males
(postexperience)
N
N
O
N
M
N
F
0.36
0.15
0.80*
0.14
0.77
0.50
(0.16)
(0.16)
(0.24)
(0.10)
(0.24)
(0.22)
(0.27)
(0.20)
0.31 (0.12)
0,42 (0,23)
0,28 (0,19)
0.14 (0.13)
0.51 (0.25)
0.19 (0.17)
0.47 (0.26)
0.16 (0.12)
0.31 (0.19)
0.82 (0.27)
0.38 (0.24)
0.58 (0.10)
0.73 (0.24)
0.42 (0.19)
0.73 (0.19)
0.52 (0.29)
Note. Abbreviations for odors are the same as those used in Table 1. * p < .05, Correlated samples t test, df = 5. ** p < ,01.
1.22"*
N
0.32
142
RICHARD E. BROWN
nonodorized blocks (t(5) = 4.95, p < .01) and marked more over their own odor than over the neutral block (t(5) = 3.57, p < .01), but did not mark more over the odors of other males (t(5) = 1.43), nor did they mark more over one nonodorized block than over the other (t(5) = 0.89). In none of the four tests did the isolated males mark more over one block than over the other (largest t(5) --- 1.84). A 2 x 4 split-plot factorial A N O V A showed that over all four tests the grouped males marked more than the isolated males (F(1, 40) = 2.36, p < .05). The grouped males marked more o v e r female odors than did the isolated males (t(10) = 2.24, p < .05) but did not show a greater preference for marking over other odors. The results of this experiment indicate that adult male rats which have been isolated for 60 days show a reduced preference for investigating female odors and a general decrease in urine-marking when compared to group-housed males. The deficit in marking in isolated males is most p r o n o u n c e d with respect to female odors and suggests that sociosexual experience is important in determining odor preferences and urine-marking patterns of male rats. To verify this, the six isolated males were given 15-min paired encounters with another male in a neutral cage and 15min exposure to an intact female each day for 4 days and then the series of four odor preference and urine-marking tests was repeated using the procedure described above. The pattern of odor preferences by the socially experienced isolates did not differ from that shown on the first test (F(1, 10) = 1.96; see Table 1). Female odors were preferred to nonodorized blocks (t(5) = 4.82, p < .01), as were male odors (t(5) = 3.03, p < .05), but there was no preference for their own odor (t(5) = .80), nor for either of the nonodorized blocks (t(5) = .99). There was an increase in urine-marking by the socially experienced isolates, but the total amount of marking was not significantly greater than that shown in the first test (F(1, 10) = 2.02) and no odorized block was marked more than the neutral block with which it was paired (largest t(5) = 2.39; see Table 2). One possible reason that this social experience did not increase odor preference and urine-marking scores is that it was too brief and males did not copulate during their exposure to female rats. Over the four female encounters males averaged 1.5 mounts (range 0 to 5) and during the male encounters there was an average of 2.5 agonistic encounters (range 0 to 7). It is possible that longer term social encounters including copulation might increase preferences for female odors. The results of this experiment indicate that social isolation in adulthood reduces the amount of time spent investigating and urine-marking over female odors by male rats, but does not influence their responses to male odors. The physical environment in which the males were housed may have influenced their behavior. While the grouped males were in larger
SOCIAL ISOLATION AND OLFACTION IN RATS
143
cages than w e r e the isolates, t h e y had slightly less floor space per rat (332 c m 2 v e r s u s 432 c m 2 in the individual cages). L o n g - t e r m isolation increases l o c o m o t i o n in an o p e n field (Gentsch, Lichtsteiner, & F e e r , 1981) and general activity levels m a y have affected o d o r investigation and u r i n e - m a r k i n g r e s p o n s e s , e v e n in males placed in differential h o u s i n g in a d u l t h o o d . Since the differences b e t w e e n the isolated and the grouph o u s e d males w e r e c o n c e r n e d primarily with female odors, h o w e v e r , it s e e m s m o r e likely that sociosexual experiences influenced these o d o r related behaviors. The importance o f olfactory communication in mediating sexual behavior in rats and the close relationship between sexual experience and o d o r related b e h a v i o r s lends support to T h o r ' s (1980) h y p o t h e s i s that an o l f a c t o r y f e e d b a c k s y s t e m m a y mediate the effects o f social isolation on c o p u l a t i o n in male rats. The effects o f social experience on r e s p o n s e s to conspecific o d o r s m a y , h o w e v e r , d e p e n d on associative learning ( T h o r & Flannelly, 1977) and on the m a l e ' s motivational state. Social isolation m a y also result in a n u m b e r o f physiological c h a n g e s and alteration o f h o r m o n e levels caused by individual housing m a y influence both sexual b e h a v i o r and o d o r p r e f e r e n c e s (Brain and B e n t o n , 1979).
REFERENCES Brain, P., & Benton, D. (1979). The interpretation of physiological correlates of differential housing in laboratory rats. Life Sciences, 24, 99-116. Brown, R. E. (1975). Object-directed urine-marking by male rats (Rattus norvegicus). Behavioral Biology, 15, 251-254. Brown, R. E. (1977). Odor preference and urine-marking scales in male and female rats: Effects of gonadectomy and sexual experience on responses to conspecific odors. Journal of Comparative and Physiological Psychology, 91, 1190-1206. Brown, R. E. (1978). Hormonal control of odor preferences and urine-marking in male and female rats. Physiology and Behavior, 20, 21-24. Chambers, K. C., Sengstake, C. B., Walther, A. M., & Bullis, J. E. (1982). Disruption of sexual behavior in socially isolated male rats. Behavioral and Neural Biology, 34, 215-220. deCatanzaro, D., & Gorzalka, B. B. (1979). Postpubertal social isolation and male sexual behavior in rodents: Facilitation or inhibition is species dependent, Animal Learning and Behavior, 7, 555-561. Flannelly, K. J., & Blanchard, R. J. (1982). Decreased aggressive and social responsiveness of chronically anosmic male rats. Bulletin of the Psychonomic Society, 19, 173-176. Gentsch, C., Lichtsteiner, M., & Feer, H. (1981). Locomotor activity, defecation score and corticosterone levels during an open field exposure: A comparison among individually and group-housed rats, and genetically selected rat lines. Physiology and Behavior, 27, 183-186. Larsson, K. (1971). Impaired mating performances in male rats after anosmia induced peripherally or centrally. Brain, Behavior and Evolution, 4, 463-471. Thor, D. H. (1980). Isolation and copulatory behavior of the male laboratory rat. Physiology and Behavior, 25, 63-67, Thor, D. H., & Flannelly, K. J. (1977). Social-olfactory experience and initiation of copulation in the virgin male rat. Physiology and Behavior, 19, 411-417.
(1985)
BRIEF REPORT Effects of Social Isolation in Adulthood on Odor Preferences and Urine-Marking in Male Rats RICHARD E. BROWN 1 Department of Psychology, Dalhousie University, Halifax, Nova Scotia B3H 4J1, Canada Male rats isolated for 60 days in adulthood spent less time investigating odors of females and urine-marked less over these odors than did males kept in groups of three. Isolated males did not differ from grouped males in their responses to
odors of unfamiliar males or their own odors. After social experience the isolated males showed an increase in urine-marking but no change in odor preferences. Individual housing therefore appears to alter olfactory communication in the same way that it does other social behaviors and these changes may be mediated by the same mechanisms. © 1985 AcademicPress, Inc.
Male rats investigate objects scented with the odors of conspecifics and urine-mark more over these odors than over unscented objects or those with their own urine odor (Brown, 1975). Sexually experienced males investigate female odors more than sexually naive males, but both urine-mark over odors with equal intensity (Brown, 1977). Both odor investigation and urine-marking are inhibited by castration and reinstated by hormone replacement therapy (Brown, 1977, 1978). These results have led to the hypothesis that urine-marking by male rats is sexually motivated (Brown, 1977). Anosmia reduces the ability of rats to recognize conspecifics and leads to a reduction in aggressive and sexual behavior (Larsson, 1971; Flannelly & Blanchard, 1982). Social experiences during development interact with olfactory stimulation with the result that socially isolated anosmic males show almost no sexual behavior (Thor & Flannelly, 1977). Social isolation during adulthood also reduces the sexual performance of male rats (Chambers, Sengstake, Walther, & Bullis, 1982; deCatanzaro & Gorzalka, This research was supported by NSERC of Canada Grant A-7441. Grateful acknowledgment is given to Robin Kind and Sonya Major for their assistance in conducting the experiments and preparing the manuscript. 139 0163-1047/85 $3.00 Copyright © 1985 by Academic Press, Inc. All rights of reproduction in any form reserved.
140
RICHARD E. BROWN
1979), and the purpose of the present experiment is to examine whether social isolation in adulthood has a similar effect on odor investigation and urine-marking behaviors. Twelve male L o n g - E v a n s hooded rats were purchased from Charles River Canada (St. Constant, Quebec) at 90 days of age. Six of these males were housed singly in 18 x 24 x 18-cm metal cages with wiremesh fronts and floors and the other six were housed in groups of three in larger cages of the same design (41.5 × 24 x 18 cm high). All rats were kept under these conditions on ad lib. Purina lab chow and water and a 12:12 L:D cycle for 60 days before testing began. Odor preference and urine-marking tests were conducted in 23 x 43 x 16-cm plastic arenas which were placed on a Lucite table top covered with unprinted newspaper. Each rat was tested in a clean cage which contained a wire-mesh block at each end. These blocks measured 5 x 10 x 2.5 cm and were wrapped with a 20 x 20-cm piece of paper towel. Odors were presented by placing two drops (approximately 0.05 ml) of urine on the center of the paper-covered block. Urine was collected using a metabolism cage as described by Brown (1977) and the test procedure was the same as that used by Brown (1975). Each rat was tested for 5 min each day on 5 consecutive days. Day 1 was a habituation day and on the next 4 days the rats were presented with pairs of blocks. On three tests, one block was odorized with urine from a female rat (F), an unknown male rat (M), or the animal's own urine (O), and the second block was nonodorized or neutral (N). Urine from female donors was taken from all stages of the estrous cycle as previous research in this laboratory has shown that males spend as much time investigating urine from nonestrous females as they do that from estrous females (Brown 1977). F o r grouped males, own urine was the odor of at least two of the animals in the group. A fourth test used two nonodorized blocks. On each test, the time spent investigating each stimulus block was recorded in seconds using two cumulative time stopwatches operated by the experimenter. When the 5-min test was completed, the paper towel was r e m o v e d from each block, the urine marks were outlined in pencil, and the area covered by urine was calculated to the nearest 0.25 cm 2 using a plastic c o v e r plate as in previous studies (Brown, 1975, 1977, 1978). Correlated samples t tests were used to analyze the odor preferences of the isolated and grouped males on each of the four tests (Table 1). Female odors were investigated more than the nonodorized blocks by both grouped (t(5) = 6.34, p < .01) and isolated males (t(5) = 4.04, p < .01), as were male odors (grouped, t(5) = 2.43, p < .05; isolated, t = 8.51, p < .01). Neither grouped nor isolated males investigated their own odor more than the neutral odor (grouped, t(5) = 2.18; isolated, t(5) = 1.20) nor was one neutral block investigated more than the other
141
SOCIAL ISOLATION AND OLFACTION IN RATS TABLE 1 Mean Time in Seconds (-+ SE) Spent Investigating Each Stimulus Odor by Grouped and Isolated Males Odor pair Group
N
N
O
N
M
N
F
N
Grouped males
13.0 (9.6)
8.8 (2.8)
22.4 (9.2)
13.6 (3.9)
69.4* (24.8)
17.9 (4.8)
93.3** (i 1.4)
13.4 (3.7)
Isolated males
22.t (6.0)
17.3 (6.4)
20.3 (4.0)
15.0 (2.5)
13.2 (3.8)
57.3** (12.9)
12.0 (2.0)
11.8 (3.4)
15.7 (4.8)
11.2 (2.8)
10.9 (4.4)
12.8 (3.7)
51.5"* (10.5)
7.4 (1.9)
(preexperience) Isolated males
(postexperience)
65.0** (8.6) 44.2* (11.3)
Note. Abbreviations for odors: N = neutral odor; O = own odor; M = male odor; F = female odor. Correlated samples t test with df = 5. * p < .05. ** p < .01.
(grouped, t(5) = 1.23; isolated, t(5) = 1.08). When the preference scores (difference scores between the odorized and nonodorized blocks) for grouped and isolated males were compared on each test, it was found that grouped males had a greater preference for female odors than did isolated males (independent groups t-test, t(10) = 2.29, p < .05) but rats in the two groups did not differ in the time spent investigating odors of males (t(10) = 0.18) or their own odors (t(10) = 0.40). The area covered by urine-marks on each block was converted into c o m m o n logarithms (log (cm 2 + l)) for statistical analysis (Table 2). Group-housed males marked more over the odors of females than over TABLE 2 Mean Log Area (_+ SE) Covered by Urine Marks on Each Stimulus Block by Grouped and Isolated Males Odor pair Group
Grouped males Isolated males
(preexperience) Isolated males
(postexperience)
N
N
O
N
M
N
F
0.36
0.15
0.80*
0.14
0.77
0.50
(0.16)
(0.16)
(0.24)
(0.10)
(0.24)
(0.22)
(0.27)
(0.20)
0.31 (0.12)
0,42 (0,23)
0,28 (0,19)
0.14 (0.13)
0.51 (0.25)
0.19 (0.17)
0.47 (0.26)
0.16 (0.12)
0.31 (0.19)
0.82 (0.27)
0.38 (0.24)
0.58 (0.10)
0.73 (0.24)
0.42 (0.19)
0.73 (0.19)
0.52 (0.29)
Note. Abbreviations for odors are the same as those used in Table 1. * p < .05, Correlated samples t test, df = 5. ** p < ,01.
1.22"*
N
0.32
142
RICHARD E. BROWN
nonodorized blocks (t(5) = 4.95, p < .01) and marked more over their own odor than over the neutral block (t(5) = 3.57, p < .01), but did not mark more over the odors of other males (t(5) = 1.43), nor did they mark more over one nonodorized block than over the other (t(5) = 0.89). In none of the four tests did the isolated males mark more over one block than over the other (largest t(5) --- 1.84). A 2 x 4 split-plot factorial A N O V A showed that over all four tests the grouped males marked more than the isolated males (F(1, 40) = 2.36, p < .05). The grouped males marked more o v e r female odors than did the isolated males (t(10) = 2.24, p < .05) but did not show a greater preference for marking over other odors. The results of this experiment indicate that adult male rats which have been isolated for 60 days show a reduced preference for investigating female odors and a general decrease in urine-marking when compared to group-housed males. The deficit in marking in isolated males is most p r o n o u n c e d with respect to female odors and suggests that sociosexual experience is important in determining odor preferences and urine-marking patterns of male rats. To verify this, the six isolated males were given 15-min paired encounters with another male in a neutral cage and 15min exposure to an intact female each day for 4 days and then the series of four odor preference and urine-marking tests was repeated using the procedure described above. The pattern of odor preferences by the socially experienced isolates did not differ from that shown on the first test (F(1, 10) = 1.96; see Table 1). Female odors were preferred to nonodorized blocks (t(5) = 4.82, p < .01), as were male odors (t(5) = 3.03, p < .05), but there was no preference for their own odor (t(5) = .80), nor for either of the nonodorized blocks (t(5) = .99). There was an increase in urine-marking by the socially experienced isolates, but the total amount of marking was not significantly greater than that shown in the first test (F(1, 10) = 2.02) and no odorized block was marked more than the neutral block with which it was paired (largest t(5) = 2.39; see Table 2). One possible reason that this social experience did not increase odor preference and urine-marking scores is that it was too brief and males did not copulate during their exposure to female rats. Over the four female encounters males averaged 1.5 mounts (range 0 to 5) and during the male encounters there was an average of 2.5 agonistic encounters (range 0 to 7). It is possible that longer term social encounters including copulation might increase preferences for female odors. The results of this experiment indicate that social isolation in adulthood reduces the amount of time spent investigating and urine-marking over female odors by male rats, but does not influence their responses to male odors. The physical environment in which the males were housed may have influenced their behavior. While the grouped males were in larger
SOCIAL ISOLATION AND OLFACTION IN RATS
143
cages than w e r e the isolates, t h e y had slightly less floor space per rat (332 c m 2 v e r s u s 432 c m 2 in the individual cages). L o n g - t e r m isolation increases l o c o m o t i o n in an o p e n field (Gentsch, Lichtsteiner, & F e e r , 1981) and general activity levels m a y have affected o d o r investigation and u r i n e - m a r k i n g r e s p o n s e s , e v e n in males placed in differential h o u s i n g in a d u l t h o o d . Since the differences b e t w e e n the isolated and the grouph o u s e d males w e r e c o n c e r n e d primarily with female odors, h o w e v e r , it s e e m s m o r e likely that sociosexual experiences influenced these o d o r related behaviors. The importance o f olfactory communication in mediating sexual behavior in rats and the close relationship between sexual experience and o d o r related b e h a v i o r s lends support to T h o r ' s (1980) h y p o t h e s i s that an o l f a c t o r y f e e d b a c k s y s t e m m a y mediate the effects o f social isolation on c o p u l a t i o n in male rats. The effects o f social experience on r e s p o n s e s to conspecific o d o r s m a y , h o w e v e r , d e p e n d on associative learning ( T h o r & Flannelly, 1977) and on the m a l e ' s motivational state. Social isolation m a y also result in a n u m b e r o f physiological c h a n g e s and alteration o f h o r m o n e levels caused by individual housing m a y influence both sexual b e h a v i o r and o d o r p r e f e r e n c e s (Brain and B e n t o n , 1979).
REFERENCES Brain, P., & Benton, D. (1979). The interpretation of physiological correlates of differential housing in laboratory rats. Life Sciences, 24, 99-116. Brown, R. E. (1975). Object-directed urine-marking by male rats (Rattus norvegicus). Behavioral Biology, 15, 251-254. Brown, R. E. (1977). Odor preference and urine-marking scales in male and female rats: Effects of gonadectomy and sexual experience on responses to conspecific odors. Journal of Comparative and Physiological Psychology, 91, 1190-1206. Brown, R. E. (1978). Hormonal control of odor preferences and urine-marking in male and female rats. Physiology and Behavior, 20, 21-24. Chambers, K. C., Sengstake, C. B., Walther, A. M., & Bullis, J. E. (1982). Disruption of sexual behavior in socially isolated male rats. Behavioral and Neural Biology, 34, 215-220. deCatanzaro, D., & Gorzalka, B. B. (1979). Postpubertal social isolation and male sexual behavior in rodents: Facilitation or inhibition is species dependent, Animal Learning and Behavior, 7, 555-561. Flannelly, K. J., & Blanchard, R. J. (1982). Decreased aggressive and social responsiveness of chronically anosmic male rats. Bulletin of the Psychonomic Society, 19, 173-176. Gentsch, C., Lichtsteiner, M., & Feer, H. (1981). Locomotor activity, defecation score and corticosterone levels during an open field exposure: A comparison among individually and group-housed rats, and genetically selected rat lines. Physiology and Behavior, 27, 183-186. Larsson, K. (1971). Impaired mating performances in male rats after anosmia induced peripherally or centrally. Brain, Behavior and Evolution, 4, 463-471. Thor, D. H. (1980). Isolation and copulatory behavior of the male laboratory rat. Physiology and Behavior, 25, 63-67, Thor, D. H., & Flannelly, K. J. (1977). Social-olfactory experience and initiation of copulation in the virgin male rat. Physiology and Behavior, 19, 411-417.