CONTACT WITH ESTRUS FEMALE AS A REWARD FOR IKSTRUMENTAL RESPONSE IN A GROWING MALE RAT FROX'I THE 3RD UP TO THE 14TK WEEK OF LIFE
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1 ACTA NEUROBIOL. EXP. 1976, 36: CONTACT WITH ESTRUS FEMALE AS A REWARD FOR IKSTRUMENTAL RESPONSE IN A GROWING MALE RAT FROX'I THE 3RD UP TO THE 14TK WEEK OF LIFE Jozef BECK and Joanna CHMIELEWSKA Institute of Obstetrics and Gynecology, School of Medicine Warsaw, Poland Abstract. The bar-press response reinforced by the contact with estrus female was investigated in growing male rats. The bar-press latency as well as the subjects' behavior changed distinctly in the course of the study with the increase of experience and maturation of the subjects. Some behaviora.1 items such as, nasogenital contact, climbing on the head, and running around showed gradual in- Prea~e during succeeding weeks of life, psrallelly to the decrease of the sitting under female, and crawling under female. A gradual shortening of the bar-press latencies was observed from the 4th to the 11th week of life succeeded by a prolongation from the lth to the 14th week. On the basis of the changes in bar-press latencies as well as of the analysis of the subjects' behavior it is suggested that the young male rat between the 4th and 7th week of life comes under an increasing influence of sexnal motivation. During the period of life between birth and the first copulation the male mammal changes radically his attitude toward the females of his species. At the onset of this period every mature female is regardet by a male puppy like a mother, and the full repertoire of the care-soliciting behavior (11) is directed towards her. Towards the end. when puberty comes and the first copulations appear, the female becomes a mate. The question arises how the motivation under-
2 536 J. BECK AND J. CHMIELEWSKA lying the contacts between males and females changes between these two stages. An experiment on rats was performed in order to investigate this problem. The evaluation of motivation was based on a careful analysis of animal behavior, whereas the response latency was used as an indicator of the level of this motivation. Rats have been chosen as study subjects for three reasons: because of the short time dividing their birth from maturity, because of their well-known postnatal behavior (4, 6, 10) and because they had been already used in the investigation of instrumental CR reinforced by the contact with conspecifics (2, 5, 7, 8, 12). METHOD Fifteen male albino rats aged 15 days at the onset of the experiment, were used as subjects. During the first 4 wk of the experiment they were caged with their mothers, later they were separated and kept 5 per cage. The 12 h reversed daylnight cycle was maintained, food and water was available ad lib. The sessions started 4-6 h after the begining of the dark period. The apparatus for investigation of instrumental response (Fig. 1) consisted of two compartments, dimensions 20 X 30 X 30 cm and 40 X 30 X 30 cm, connected by an opaque door 25 X 25 cm. In the front wall of the smaller compartment a 2 X 8 cm turning pedal or a bar of the same size was attached 4 cm above the floor. The transparent front walls and a mirror placed above the apparatus allowed the observation of the animals During the training, each session was preceded by separating the subjects from their mothers for 2 h. Subsequently before the first trial each subject was placed together with estrus female used as reinforcer in the larger compartment for 60 s. Furthermore he was placed in the smaller compartment equipped with a turning pedal (3). When the campur hen f Reinforcer carnpaminent Panspurent wa// Fig. 1. Apparatus for investigation of instrumental responses (upper view)
3 SEXUAL INSTRUMENTAL RESPONSE 53 7 subject had begun to turn the pedal, the door separating him from the reinforcer was opened enabling the contact between the animals. During the contact the door separating the compartments was open. Immediately after each contact the subject was forced back into the smaller compartment, and the reinforcer into the larger one. From the 3rd week of the experiment, when the instrumental response was already well established, the turning pedal was replaced by the bar. The sessions were 5-20 min long. Rats were tested every day during the training and once a week when the training was completed. Each session consisted of 2-3 trials during the first week and of 7 trials during the later ones. The experiment lasted about 12 wk and was finished when the ejaculation had been observed in a subject. The instrumental response latency was measured with a stopper as the time between placing the subject in its compartment and subsequent pressing of the bar. The behavior of the subjects during conta.ct (lasting up to 120 s) was carefully observed and the respective behavioral items were scored in 5 s intervals. The Smirnov-Kolmogorov test and the Sperman Q test were used for statistical analysis of data. RESULTS Changes in response latencies During the first week every subject learned to press the turning pedal for opening the door separating it from the reinforcer. This instrumental response, once established, has been subsequently sustained during the whole course of the study. The response latencies of the subjects recorded from the second week of the experiment, showed distinct changes in the course of the study. These changes consisted in the gradual shortening of latencies from the 2nd to the 9th week of the experiment and in their subsequent prolongation from the 9th to the 12th week. Figure 2 shows the cumulative distributions of latencies estimated for 4 blocks of sessions performed respectively in 2nd and 3rd, 4th-6th, 7th-9th and 10th-12th weeks of the experiment. A statistical analysis with Smirnov-Kolmogorov test indicated a statistically significant difference (with a = 0.1) between the 1st and the 2nd block of sessions (n, = 337, n, = 307, D = 12.55O/o, D,,, = 2g0/a) observed in class s, between the 2nd and the 3rd block of sessions (n, = 307, n, = 254, D = 13.53O/n, D,,, = 14O/o) observed in class 6-12 s, and between the 3rd and the 4th block of sessions (n, = 254, n, = 191, D = 15.32O/n, D,,, = 18O/o) observed in class 6-12 s.
4 J. BECK AXD J. CHMIELEWSXA Fig. 2. Cumulative distributions of the duration of instrumental response latencies far sessions performed in 2nd and 3rd week n=337 (thin continuous line), in 4th-6th n=307 ibroken line), in 7th-9th n=254 (dash point line) in 10th-12th n=191 (thick continuous line). Abscissae, the latencies duration in seconds. Ordinate, cumulative record of the number of occurrence of particular latencies in percent. Changes in behavior The changes in bar-press latencies were accompanied by the changes in the subjects' behavior during the contacts. A careful observation of the animals' behavior beginning from the second week of the study allowed to distinguish the following behavioral items: 1. The contact of the bodies The animals contact their bodies usually side to side. 2. Exploration of the body Sniffing and nuzzling other than anogenital parts of the female. 3. Crawling under Quick passing under the female body. 4. Sitting under Sitting under the ventral part of the female. 5. Running around Running around and jumping over the female.
5 SEXUAL INSTRUMENTAL RESPONSE Nasogenital contact Sniffing and nuzzling of the anogenital region of the female. 7. Climbing on the head Subject puts its forelegs on on the female's head. 8. Climbing on the body Subject puts its forelegs on other than head regions of the female's body. 9. Mounting The reinforcer is mounted by subject. 10. Intromission The reinforcer is mounted by the subject and the penis is inserted into vagina. 11. Ejaculation The reinforcer is mounted by the subject and the intromission termined by ejaculation takes place. 12. Exploratory behavior The subject was interested in other than reinforcer elements of the experimental environment. The reinforcer displayed typical behavioral patterns of the estrus female rat, such as: ear wiggling, presentation, sometimes hopping and running. Among the behavioral events directed toward the subjects, sniffing, rubbing and grooming were often observed. Particular behavioral items were displayed by the subjects with various frequency during the successive weeks of the experiment. Table I shows the per cents of time occupied by respective behavioral items observed during contacts between the subjects and the reinforcers from the 2nd up to the 12th week of the study. The per cents had been calculated for a group of subjects treated as an entity, as that made the main changes in the behavior of maturating male rats more conspicuous. In order to find out if the continuous increase or decrease of some items observed during the successive weeks was significant, the correlation with the order of the weeks of the experiment was estimated using Spearman 9 test. Particular animal reactions in the course of the study showed the following differences: (i) continuous decrease, (ii) continuous increase, and (iii) no linear correlation. To the first group there belonged two behavioral items: crawling under and sitting under. Crawling under, observed in 12.3O/o during the second week of the study, gradually decreased to 2.1 /n in last week. This item skiowed very strong negative correlation with the order of the weeks (Q = -0.90, n = 11. P < 0.001). Sitting under, observed in 5.3OIo during the second week, decreased to 0.4OIo during the last week. 5 - Acta Neurobiologiae Experimentalis
6 540 J. BECK AND J. CHMIELEWSKA Percentage of occupied by the respective behavioral items observed during the contacts between the subjects and the reinforcers In weeks 5, 9, and 10 several subjects were excluded from experiment for technical reasons. ** The per cents were counted only for a group of subjects which actually display copulatory behavior. The ubjects which had copulated in the 11th week were excluded from experiment in the 12th week. It was also negatively correlated with the order of weeks (e = -0.65, P < 0.02, n = 11). To the second group there belonged: nasogenital contact, running around, and climbing on the head. Contrary to the behavioral items which showed a continuous decrease beginning from the 2nd down to last week of the study, they increased only to the 9th or 10th week and subsequently decreased. The decrease coincided with the appearence of the first copulations. The nasogenital contacts increased more distbctly, from in the 2nd up to 9.3"/0 in the 9th week of the study (Q = 0.85, P < 0.001, n = 11). The running around increased from 0.8OIo in the 2nd up to 4.7O/o in the 9th week (q = 0.86, P < 0.01, n = 8), and the climbing on the head from 1.3O/o in the 2nd up to 7.3OIo in the 10th week (Q = 0.79, P < 0.001, n = 9). The number of mountings and intromissions increased too, but only during the last 4 weeks of the study, as before that time they have not been observed. Other behavioral items showed no constant changes in the course of the experiment.
7 SEXUAL INSTRUMENTAL RESPONSE 541 DISCUSSION Our results indicate that instrumental response reinforced by the contact with estrus female established in a male rat in the 3rd week of life continued subsequently up to the moment when the first copulations appeared. That indicates a motivation present in male rats of that time, which such contacts can satisfy. The designation of that motivation was based on an analysis of the character and frequency of appearence of particular behavioral events during successive weeks of this study. The analysis revealed that from among 12 distinguished items of the subject's behavior, two have shown a gradual decrease and three -a gradual increase in the course of the experiment. The decreasing items, namely the sitting under and crawling under, are typical items of care-soliciting behavior. Among the increasing ones, only the nasogenital contact can be recognised as an item of sexual behavior because it is typically observed during courtship among rats (13), and seems to be a form of appetitive behavior, whereas the mounting and intromission belong to consummatory act. The increase of nasogenital contacts seems to reflect the rise of sexual motivation, whereas the increase of running around and climbing on the head could be the result of a general arousal of behavior (9). The increase of a general arousal of behavior as well as the shortening of response latencies observed during the first 8 wk of the experiment can be regarded as results of an increased level of sexual motivation not satiated in this period of life. A prolongation of response latencies, rapid decrease of running around and climbing on the head as u7ell as a gradual decrease of nasogenital contacts observed after the appearence of consummatory sexual reactions support strongly this concept. Some light on the problem of sexual motivation in the maturating male rat can be thrown by Beach's theory of masculine sex drive (1). According to that theory, male sexual behavior is composed of two mechanisms; the sexual arousal mechanism and the copulatory mechanism. The copulation takes place when the sexual arousal attains the threshold of copulatory mechanism. The threshold of copulatory mechanism depends, on the other hand, on sufficiently high concentration of male sexual hormones. The sexual motivation which appears in maturating male rats responds probably to the sexual arousal. This increasing sexual arousal coincides, when the puberty comes, with the increase of concentration of male sex hormones, and this coincidence leads to switching on of the copulatory mechanism. According to the other items of behavior observed in this study, it remains unclear, why the general arousal of behavior affects only the
8 542 J. BECK AND J. CHMIELEWSKA climbing on the head, whereas the climbing on the body is not affected. Probably this behavioral item may be related to some exploratory functions and together with the exploration of the body and exploratory behavior may be based on exploratory motivation. The last behavioral item, namely the contact of the bodies, may be related to some other motivation connected with bringing the bodies to a close contact. The existance of such a motivation in an animal as highly contactive as the rat is quite possible. In conclusion, our suggest is that the young male rat between the 4th and the 7th week of life comes under the increasing pressure of the sexual motivation parallelly to the decrease of the care-soliciting motivation. Besides the care-soliciting motivation and sexual motivation, there are other motivations active in a growing-up male rat, such as, for example, the exploratory one. Hence the instrumental response reinforced by the contact with estrus female is underlied in the growing male rat by several motivations and the degree in which each of them underlies the instrumental response, depends on the age of the subject. These data were used in the thesis submitted by J. Chmielewska for the degree of Master of Biology at the Department of Animal Physiology, Institute of Zoology, University of Warsaw. REFERENCES 1. BEACH, F. A Characteristics of masculine "sex drive". In M. R. Jones (ed.), Nebrasca symposium of motivation. Univ. Nebrasca Press, Lincoln, P BECK, J Instrumental conditioned reflexes with sexual reinforcement in rats. Acta Neurobiol. Exp. 31: BECK, J Contact with male or female conspecifics as a reward for instrumental response in estrus and anestrus female rats. Acta Neurobiol. Exp. 34: BOLLES, R. C., and WOODS, P. S The ontogeny of behavior in the albino rat. Anim. Behav. 12: DENNISTON, R. H Quantification and comparision of sex drives under various conditions in terms of learned response. J. Comp. Physiol. Psychol. 47: FEIGLEY, D. A., PARSONS, P. J., HAMILTON, L. W., and SPEAR, N. E Development of habituation to novel environments in the rat. J. Comp. Physiol. Psychol. 79: JOWAISAS, D., TAYLOR, J., DEWSBURY, D. A., and MALAGODI, E. F Copulatory behavior of male rats under an imposed operant requirement. Psychon. Sci. 25: KAGAN, J Differential reward value of incomplete and complete sexual behavior. J. Comp. Physiol. Psychol. 48:
9 SEXUAL INSTRUMENTAL RESPONSE KONORSKI, J Integrative activity of the brain. An interdisciplinary approach. Univ. Chicago Press, Chicago, 531 p. 10. LARSSON, K Experience and maturation in the development of sexual behavior in male puberty rat. Behaviour 14: SCOTT, J. P Animal behavior. Univ. Chicago Press, Chicago, p SHEFFIELD, F. D., WULFF, J. J., and BACKER, R Reward value of copulation without sex drive reduction. J. Comp. Physiol. Psychol. 44: 3-9, 13. YOUNG, W. C The hormones and mating behavior. In W. C. Young (ed.), Sex and internal secretion. Williams and Wilkins Co., Baltimore, p Accepted 12 May 197G J6zef BECK, Institute of Obstetrics and Gynecology, School of Medicine, Karowa 2, Warsaw, Poland. Joanna CHMIELEWSKA Institute of Nuclear Research, Dorodna 16, Warsaw, Poland.
10 ERRATA Page 535, line 10 of Abstract, last six words should read: 11th to the 14th week. Page 537, line 7 from bottom, last words should read: (with a = 0.01)
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