Animal 1. earning& Behavior 1973. 1'01. 1. So. 3. ::::3-::::7 Influences of social isolation during development on sexual behavior of the rat*
JOHN A. DUFFY+ and SHELTON E. HENDRICKS University ofNebraska, Omaha, Nebraska 68101
Male and female rats were weaned at 14 day. of age and raised in social isolation or with three other animals. At maturity the male isolates displayed less male sexual behavior than the socially reared Ss, F ernale isolates, after ovariectomy and injection with androgen. exhibited much less male sexual behavior than control females similarly tested. After being brought into estrus by injections of estrogen and progesterone. the female sexual behavior of female social and isolate Ss did not differ. Data were interpreted as indicating that social isolation during development deprives rats of critical experiences necessary for development of appropriate responses to social stimuli eliciting male copulatory behavior in both sexes.
A frequently reported result of early social isolation is sexual and maternal behavior in isolated female pigs,and a disruption or inhibition of sexual behavior. This Stern and Hoffman (I970) studied maternal behavior in finding has been reported in numerous species. Harlow isolated guinea pigs. Neither study reported any and Harlow (1966) and Mitchell, Raymond, Ruppenthal, difference between isolated animals and controls. These and Harlow (l966) have all reported that social isolation findings are at variance with Harlow's findings in female severely disturbs or disrupts mating behavior in male and monkeys. There are, to our knowledge, no published female rhesus monkeys. Turner. Davenport. and Rogers studies concerning the effects of social isolation on the (l966) reported similar effects in chimpanzees. A sexual behavior of female rats. decrement in male sexual behavior has also been noted The present experiments were designed to replicate in guinea pigs (Gerall, 1963) and dogs (Fox & Stelzner, previous studies dealing with the influences of social 1966: Beach, 1968). However. Meier (1965) found no isolation on the sexual behavior of male rats. Further. such effect in rhesus monkeys, and Harper (l968) failed the influence of isolation on the female sexual behavior to find that social isolation affected the male or female of female rats was studied. Since male sexual behavior social behavior of guinea pigs. In rats the data are also can be readily induced in ovariectomized female rats by contradictory. Some investigators have reported a injections of androgen (Balt, 1940; Koster, 1943: Beach complete lack of sexual behavior in isolated male rats & Rasquin, 1942), it should prove interesting to see the (Gerall, Ward. & Gerall. 1967). while others (Folman & effects of isolation on this induced male behavior. It was Drori. 1965: Gruendel & Arnold. 1969) have found a expected that isolated females would show a deficit in significant decrease. but not a lack. of male sexual the display of the heterotypic male behavior. behavior. On the other hand, Beach (Beach. 1942b: Beach. 1958: Kagan & Beach. 1953) has consistently METHOD failed to find a decrement in male sexual behavior. While most of the data seem to support the view that isolation Subjects during development affects male sexual behavior. some Seventy-eight Wistar albino rats, both male and female. born equivocation does exist. In rats in particular. there seems in the laboratory during a 14-day period, were used as S:;, At the to be a need for clarification of the parameters involved start of the study, there were 31 isolate males. 15 isolate in the effects of social isolation during development on females. 16 control males. and 16 control females. All were male sexual behavior. maintained on ad lib food and water throughout the experiment. There are few studies available concerning the effects Rearing Conditions of social isolation on female sexual or maternal behavior in other than primate species. Signaret (1970) studied Ss were weaned at 14 days of age and randomly assigned by litter either to a control condition or to a social isolate rearing *This study is based upon a thesis submitted by the first condition. After weaning. the pups were housed in dark enclosed author to the Graduate College. Universitv of Nebraska at boxes. approximately 18:\ 15 x 15 ern, in a heated quiet room Omaha in partial fulfillment of the requirements for the \1:\ and bottle fed milk by hand every 4 h. the 1. using a damp gauze degree in psychology. The research was supported in part by pad at each feeding to help each pup excrete. Each isolated 5 r.s. Public Health Service Grant I ROl :\510017-01. was housed alone. while each social S was with three other Ss of Testosterone propionate was supplied by J. J. Chart of Ciba the same sex and age. Pharmaceutical Company and the estradiol benzoate by Preston Between 18 and 10 days of age. the isolated 55 were Perlman. Schering Corporation. The authors are indebted to transferred to standard individual cages in the colonv room, Helen Peterson for her technical assistance. 14 x 18 x 18 ern high. Social rearing -grours were mJ1ntain"d. -;- Present address: Department of Ps~ chology, Tulane and they were transferred at this age to cages measuring L'nivcrsity. :\ew Orleans. Louisiana 70118. 14:\ 36 x 18 em high" For approximately 7 da) s, Ss were ied a 224 DUFFY AND HENDRICKS mixture of standard laboratory food and milk. After that time, male behavior tests, after randomly voiding Ss' data to the animals maintained themselves on dry food and water. A obtain equal numbers of Ss per cell, revealed that there reverse light cycle, 12 h light and 12 h darkness, was maintained was no significant difference between the weights of the throughout the rest of the study. Only direct interaction with other animals was controlled; isolated 5~ could presumably hear, isolate and control Ss (F = 2.01, r > .05), nor was the smelL and. when cages were moved for cleaning, occasionally see interaction of Rearing Condition by Weekly Weighings other animals. When the animals were between 91 and 104 days significant (F =.04, p > .05). All Ss gained weight as the of age. the control group was transferred to individual cages and testing for male sexual behavior continued (F =4.36, the isolated group. to hold the amount of handling constant, was transferred to freshly cleaned individual cages. Also at this time, P < .005), and males weighed more than females all female Ss were ovariectomized under ether anesthesia. (F = 162.62, P< .005).
Male Sexual Behavior Tests Male Sexual Behavior
Testing for male behavior in both male and female Ss was begun when the animals were 96 to 109 days of age. Tests were The variance of the Ss' male sexual behavior data conducted in a dimly lighted room, using semicircular proved to be too heterogeneous to permit one analysis observation cages 65 ern in diam and 24'12 ern high. of variance over all the Ss' data. Data from three Ss were Ovariectomized female rats were used as lures for the male randomly voided from the male isolate group to obtain sexual behavior. All lures were made estrous by intramuscular injection of an equal number of Ss per cell (14), and these data were 25 Ilg of estradiol benzoate (EB) 48 h before testing and 500 Ilg analyzed by a Groups by Trials analysis of variance;data of progesterone 6 h before testing. Ss were tested in seven from the female Ss, which had an equal number of Ss sessions, 5 days apart. each session lasting 15 min after a 1Ornin per cell (15), were analyzed in a similar design. A adaptation period. Testing was conducted with groups of six measure of male sexual behavior was obtained by adding animals. one 5 and one lure per cage, at randomized times in the afternoon between 5 and 9 h after the- beginning of the dark the total number of responses on each of the three period. The animals were always tested in the same order in the res p0 nse scales (incomp1ete responses, complete same arena. Male sexual behavior was evaluated by recording the responses, and ejaculations) for each S for each test. number of incomplete responses (mounting the estrous lure from Analysis of these data for the male Ss showed that the the rear. palpating with the forepaws, and pelvic thrusting without a marked dismount), complete responses (mounting as social Ss exhibited significantly more male sexual described above, with a marked dismount), and ejaculations. behavior (F = 10.62, P < ,005) than the male isolate Ss. Responses were recorded on a 2G-channel Esterline-Angus event The increase in exhibited male sexual behavior over tests recorder. After the first test for male behavior, all female Ss was also found to be significant (F = 6.40, P < .005). began receiving injections of 250 Ilg of testosterone propionate lTP) intramuscularly every other day throughout the testing Each of these three component scales was also analyzed period. During the male behavior tests, the Ss were weighed separately in two-way analyses of variance. The mean weekly. number of each response for isolated and social males over the seven behavior tests is presented in Fig. 1. On Female Sexual Behavior Tests all three measures, the social males were found to have One week after the male behavior tests were completed, the exhibited more sexual behavior than the isolates. The females were tested for female sexual behavior. Each 5 received tests effect was significant for all measures (for all 25 IJ.g of EB intramuscularly 48 h before testing was to begin and analyses, p < .0I), and significant Groups by Tests 500 Il of progesterone 4 h before. Testing was conducted in the interactions were noted for the incomplete and same cages used for male sexual behavior tests, Proven sexually ejaculatory responses (F=2.19, p<.05 and F=4.l9, active males were used to elicit the sexual behavior. The female behavior, including degree of lordosis, holding of lordosis, and p < .005, respectively). darting and soliciting behaviors, was rated according to a system Analysis of the total number of male copulatory presented by Gerall, Dunlap. and Hendricks (1973). Each 5 was responses exhibited by female S5 under the influence of mounted 10 times for each of four tests I week apart, and each exogenous androgen revealed that socially reared females mount was scored on all three scales by an experienced scorer using a single blind technique. The E doing the scoring did not exhibited significantly more sexual behavior than the know to which groups the Ss he was scoring belonged. isolate group (F = 4.33, P < .05). All Ss showed significant improvement over tests (F = 3.24, p < .01), RESULTS but there was no significant Groups by Trials interaction. A separate analysis of the incomplete Of the 78 Ss initially included in the study, 61 responses yielded the same results as the analysis of the survived to 90 days of age. Of the 17 that died, 14 were total score. There were too few complete responses to be male isolates, while only 3 were in the social groups. meaningfully analyzed. The mean number of complete None of the female isolates died. All but one of the and incomplete responses per group is presented in deaths occurred during the immediate postweaning Fig. 2. period (I4·25 days of age). The survival rate for isolated Since the nature of the male behavior data made the males was found to be significantly poorer (p < .0I) use of analysis of variance somewhat questionable. than any of the other groups, using a test for differences nonparametric procedures were also applied. Summing between proportions (Bruning& Kintz, 1968). all responses ove[ the seven tests and using the Analysis of the weekly weights of the Ss during the Mann-Whitney U test to evaluate the differences I\FLUE]\CES OF SOCIAL ISOLA110\ OS SEXUAL BEHAVIOR 225 between the social and isolate males and the social and isolate females revealed the same between-groups ~4 differences seen in the analyses of variance (p ~ .0I). (f) -SOCIAL Z ~ ..... - ... ISOLATE Female Sexual Behavior (f)3 z~ <[ WW Analysis of the female Ss' female behavior total scores ;:Ef- did not detect a difference between the two groups of ~ 2 n, females (F =1.93. p> .05). All Ss showed a significant ;:E o improvement over tests (F = 3.49, P < .05), but the u Groups by Tests interaction was not significant. None of z the component scales of the total score, lordosis, holding. or darting, showed a significant difference between the social and isolate animals. Again, (f) application of a Mann-Whitney U test to the female w behavior scores yielded the same result as analysis of lJ) ~2 va riance: no difference between groups. 8s w zc:r:: DISCUSSION
Harper. l. Lffccts of isolation from birth on the social behaviour Signoret. J. P, Sexual behaviour patterns in female domestic pigs of guinea pigs in adulthood, Animal Behaviour. 1968, 16, IS1I5 scrota i,) reared in isolation from males. Animal 58-64, Behaviour. 197<':. 18. 165-168. Kagan, L & Beach, L A, Effects of early experience on mating Stern. 1. J'. & Hoffman. B. \1. Effects of social isolation until behavior in male rats, Journal of Comparative & Physiological adulthood on maternal behavior in guinea pigs, Psychonomic Psychology, 1953,46,204-208, Science. 1970. 21. ~5-16. Koster. R, Hormonal factors in male behavior of the female rat, Turner. C. H.. Davenport. R. K.. & Rogers. C. \1. The effect of Endocrinology, 1943,33,334-348, early deprivation on the social behavior of adolescent Meier, G, W, Other data on the effects of social isolation during chimpanzees, American Journal of Psychiatry. 1969. 125. rearing upon adult reproductive behaviour in the rhesus 1531-1536, monkey iMacaca mulattai. Animal Behaviour. 1965. l J, 228-231. Mitchell, G. D.. Raymond. I::. J.. Ruppenthal. G. c., & Harlow. (Received for publication January 19, 1973: H. F. Long-term effects of total 51 upon behavior of rhesus resubmitted April 27. 1973; monkeys. Psychological Reports. 1966. 18. 567-580. accepted May 16. 1973.)