Social play in juvenile rats: a decade of methodological and experimental research.

The social play behavior of juvenile rats was originally described nearly a century ago, but research methods have only recently included the controlled laboratory investigation of psychobiological variables. This review covers the experimental literature of social play or play fighting behavior in juvenile laboratory rats reported during the last decade. Innovative measures for quantifying social play are described; hormonal, pharmacological, and neurological variables are examined; and interpretative concepts of social play are discussed. The current emphasis on measures and procedures as well as the limited scope of current research effort suggests a formative stage of research development.

Social play soliciting by male and female juvenile rats: effects of neonatal androgenization and sex of cagemates.

Male and female juvenile rats were individually exposed to nonplayful juvenile social stimuli in a novel test of play-soliciting behavior to examine hormonal and experiential determinants of sex differences. In Experiment 1, neonatally androgenized females engaged in play soliciting at a level equal to that of male controls and greater than that of nonandrogenized female controls. In Experiment 2, males and females were reared in unisexual and bisexual groups in order to compare long-term sex-related social experience effects on juvenile play soliciting. Males exposed only to other young males engaged in greater play soliciting than males exposed to both sexes; females, in contrast, were unaffected by sex of cagemates. Within rearing conditions, however, males engaged in greater play soliciting than females. The combined results suggest that perinatal gonadal androgen exposure effects on social play are prepotent and contribute essentially to sex differences in the initiation of social play behavior.

Testosterone dependent effects of methylphenidate on social investigatory behavior of the rat.

Previous work suggested a sex difference in social investigatory behavior of a novel conspecific during acute exposure to methylphenidate. In contrast to caffeine, which has been observed to increase social investigatory behavior only in males, methylphenidate decreased social investigatory behavior only in females. Testosterone-treated females were comparable to males and were unaffected by methylphenidate. Castrated males were comparable to females in their sensitivity to methylphenidate. Like caffeine, methylphenidate increased locomotor activity in both males and females, suggesting that drug effects on social investigation cannot be attributed to a nonspecific stimulant effect. The combined results reveal a sex-related interaction of circulating testosterone with acute methylphendiate exposure. Interpretations are discussed including the behavioral contrast following exposure to methylphenidate or to caffeine.

Caffeine and copulatory experience: interactive effects on social investigatory behavior.

Three experiments test the interaction of prior copulatory experience with acute caffeine exposure on social investigatory behavior of the male Norway rat. At a dosage of 20 mg/kg or greater, caffeine counteracts a decrease in social investigation attributed to copulatory experience. At a 10 mg/kg dosage, caffeine increases social investigatory behavior prior to sexual exposure but has no comparable effect after sexual exposure. The results are interpreted as confirming a long-term effect of copulatory exposure on social investigatory behavior and as describing a dose-related interaction of caffeine exposure with prior copulatory experience. Social investigation is viewed as a preliminary component of sexual behavior and the decrease in social investigation following copulatory experience as a gain in efficiency of social discrimination. Acute caffeine exposure apparently interferes with access or retrieval of reference information in long-term memory.

Social-olfactory experience and initiation of copulation in the virgin male rat.

Two experiments examined the role of olfactory sensation for initiation of normal copulatory behavior of mature male rats. Experiment 1 compared copulatory performance of peripherally anosmic social isolates with that of intact isolate controls. The results revealed significantly lower mounting, intromission, and ejaculation frequencies of the anosmic group and suggested that nonolfactory cues attain significance via an associative-learning process. Experiment 2 compared three social isolate groups of mature males with varying sexual experience prior to anosmia. Four 1-hr tests were conducted at 5-day intervals. The results indicated comparable copulatory performance of the experienced groups and absence of copulation by the majority of the nonexperienced group. With a 12-day continuous exposure to intact females, all noncopulators eventually impregnated. The results are discussed with reference to the requirement of social experience for initiation of normal sexual performance in the male rat.

Scopolamine blocks play fighting behavior in juvenile rats.

Play fighting, social investigation, and locomotor activity of prepubescent male laboratory rats were observed 20 min following administration of scopolamine hydrobromide. Play fighting was inhibited by an intraperitoneal dosage of 0.3 mg/kg and was effectively blocked at all dosages greater than 0.5 mg/kg; activity and social investigatory behavior were increased by scopolamine. Play fighting inhibition following a threshold dosage of 0.3 mg/kg scopolamine was effective at 30 min; after 120 min, drug- and saline-treated groups failed to differ reliably. Behavioral tolerance to scopolamine was observed after five days of daily treatment with 0.5 mg/kg scopolamine; play fighting, following a 0.5 mg/kg dosage of scopolamine, did not differ from that of saline-treated controls. The results are discussed in terms of central and peripheral effects of scopolamine and the competing response hypothesis.

Anosmia and play fighting behavior in prepubescent male and female rats.

Prepubescent male and female rats were paired after intranasal treatment with isotonic zinc sulfate or saline solutions to determine the influence of peripheral anosmia upon play fighting behavior. In Experiment 1, male isolate residents pinned intruders significantly more often than intruders pinned residents but anosmia treatment had no influence on pinning behavior. In Experiment 2, males and females differed significantly in all major categories of play fighting but anosmia treatment had no influence on play fighting of either males or females. In Experiment 3, male groups matched for play fighting behavior prior to intranasal zinc or saline treatment were paired with like-treated males. All males in all pairings engaged in play behavior but anosmic males played less than controls. Evidently, intranasal zinc treatment depresses play behavior only when both members of a pair are anosmic. Play behavior is more markedly affected by resident-intruder status and by gender than by peripheral anosmia.

Testosterone dependent effects of caffeine on social investigation by adult male rats.

The testosterone determinants of caffeine induced increases in locomotor activity and social investigation by adult rats was investigated. In all groups where testosterone levels were high (intact or sham castrate adult males or castrate males receiving testosterone replacement) caffeine increased the social investigation of a novel juvenile rat. In condition where androgen levels were low (adult females, castrate males and castrate males receiving oil injections) social investigation was not affected by caffeine. In contrast, locomotor activity was increased by caffeine in all treatment groups. Thus, testosterone has behaviorally specific effects on the caffeine responsiveness of the rat.

Social play in juvenile rats during scopolamine withdrawal.

Scopolamine induced blockade of play fighting in juvenile rats and the rapid induction of behavioral tolerance to an initially effective dosage suggested a rebound in social play following chronic scopolamine exposure. Juvenile rats received daily intraperitoneal scopolamine or saline injections for one week. Play soliciting and play fighting behavior were then measured at 24 and 168 hr after drug withdrawal. Scopolamine treated juveniles engaged in markedly greater play soliciting and play fighting behavior than did controls. Drug-induced increase in muscarinic receptors and supersensitivity to endogenous acetylcholine following scopolamine withdrawal is suggested as the basis for observed differences in social play.

Sex differences in investigatory and grooming behaviors of laboratory rats (Rattus norvegicus) following exposure to novelty.

Prior research suggested that during exposure to novel stimuli, rodent investigation and self-grooming behaviors may be sexually dimorphic and interact with ambient illumination. To test this notion we compared the behavior of adult male and female groups of Long-Evans hooded rats in normal room lighting (860 lx) and in very dim, red light (0.2 lx) following exposure to a novel juvenile conspecific. Illuminance level had little or no effect, but investigatory and subsequent self-grooming behaviors of males were substantially greater than those of females, and females engaged in greater ambulatory activity than did males. In a second experiment adult males and females were exposed to a novel inanimate object. No reliable sex differences were observed. We conclude that social novelty, as provided by exposure to a juvenile conspecific, stimulates greater investigation and postinvestigatory self-grooming than exposure to a novel inanimate object and that exposure to novel conspecifics presents a useful method for the investigation of sex differences, gonadal hormone effects, and interactions of hormones with neurotransmitter systems governing motor control systems.

Interactive effects of caffeine, 2-chloroadenosine and haloperidol on activity, social investigation and play fighting of juvenile rats.

The effects of caffeine, 2-chloroadenosine and haloperidol and their interaction on activity, social investigation, and two measures of play fighting (crossover and pinning), were investigated in juvenile male rats. Caffeine (20 mg/kg) increased activity, decreased crossover and pinning, but had no effect on social investigation. Both 2-chloroadenosine (0-10 mg/kg) and haloperidol (0-10 mg/kg) depressed activity, social investigation, crossover and pinning. When given together in varying dosages, caffeine and 2-chloroadenosine had behavioral effects suggestive of a competitive interaction between the two drugs. In contrast, the effects of haloperidol were not appreciably altered by simultaneous caffeine treatment. These results suggest that the influence of caffeine and 2-chloroadenosine on activity, social investigation and play fighting involve interaction with adenosine receptors.

Play soliciting in juvenile male rats: effects of caffeine, amphetamine and methylphenidate.

Three standard CNS stimulants were tested for effect on juvenile play soliciting in prepubertal male rats (n = 120). Three dosages of each stimulant were compared with a saline control. Soliciting behavior was isolated and magnified by a novel method incorporating pretest social deprivation and social response to a standard nonplayful social stimulus pretreated with scopolamine HBr. Caffeine significantly decreased frequency of play soliciting only at the high dose of 40 mg/kg. Methylphenidate and d-amphetamine significantly decreased play soliciting at all dosages tested. The method is proposed as a generally useful experimental paradigm in analyses of drug effects on play soliciting. Advantages include individual measures of soliciting behavior that correlate reliably with measures of rough-and-tumble play fighting.

Social memory deficits in adult male rats exposed to cadmium in infancy.

In two experiments infant rats were injected subcutaneously with 0, 1, or 2 mg Cd/kg on Day 5 or 6 after birth. In adulthood (150 days of age) subjects in both experiments who received the 2 mg/kg dose failed to learn the identity of a strange rat in a social recognition test. Cadmium-treated rats investigated familiar and strange rats equally, whereas control subjects investigated familiar rats much less than unfamiliar individuals. Results with rats in the 1 mg/kg group were less consistent; in Experiment 1 they failed to learn the identity of a stranger, in Experiment 2 they behaved like controls. The level of investigation of a strange rat did not differ among the experimental groups, indicating cadmium did not cause a performance deficit. The 2 mg/kg dose of cadmium had no effect on body weight in Experiment 1 and a small (6.98%), but significant, depressant effect on body weight in Experiment 2. Cadmium exposure in infancy appears to affect social memory processes long after the treatment period.

Low level lead exposure during lactation increases rough and tumble play fighting of juvenile rats.

Lactating rats were given distilled water or distilled water containing 0.067% lead chloride (500 ppm lead) as their sole source of drinking fluid from Days 1-21 of lactation. Activity, social investigation and rough and tumble play fighting behaviors of the offspring were observed on Day 26 and activity and play solicitation behaviors on Day 36. Although lead treatment reduced the mothers' fluid intake, there were no effects on pup growth and activity or on maternal behaviors. When paired with a group-housed stimulus animal on Day 26, lead-treated subjects had increases in the two measures of play fighting (crossover and pinning), and in social investigation, relative to controls. When tested with a scopolamine-treated, non-playful stimulus on Day 36, increased crossover frequencies were observed in lead-treated subjects when compared with controls. Two-min activity levels on Days 26 and 35 were unaffected by lead exposure. These results indicate that social interactive behaviors of juvenile rats are effective tools in the assessment of exposure to toxic substances early in development.

Cadmium exposure in infancy: effects on activity and social behaviors of juvenile rats.

In two experiments male and female infant rats were given single injections of cadmium chloride (0, 1, 2, 3 or 4 mg Cd/kg) on Day 5 or 6. Animals receiving the 3 and 4 mg/kg doses had high mortality rates at weaning; survivors were extremely underweight and were not used in postweaning tests. Male subjects receiving 2 mg/kg in infancy were significantly more active after weaning than littermates who had received 0 or 1 mg/kg doses, and on Day 29 they also engaged in significantly more rough and tumble play with a nontreated partner than did rats in the other groups. This effect of early cadmium exposure was also evident when males were tested with similarly treated subjects on Day 44: rats in the 2 mg/kg group had higher pinning frequencies than rats in the 0 or 1 mg/kg groups. In contrast, females in the 1 and 2 mg/kg groups did not have increased activity or rough and tumble play fighting. These data are consistent with the few correlational studies in human children which suggest changes in social behaviors associated with elevated tissue cadmium levels.

Knowledge of results and counting of sequential light flashes by retarded and intellectually normal children.

12 adolescent retarded boys and 12 younger third-grade boys of equivalent mental age observed sequential flashes of light and made judgements of numerosity. Durations of successive flashes were 300, 500, 700, and 900 msec. in trains of 1 to 15 flashes. Over six daily sessions, subgroups receiving information about accuracy after each trial made fewer errors, and subgroups receiving none made more errors. The linear trend interaction of knowledge of results with IQ was significant, with performance of the nonretarded boys decreasing to the level of the retarded boys in the no-feedback condition. With feedback, the rate of decrease in error over sessions was similiar for both levels of IQ. The results indicate a substantial effect of knowledge of results in improving accuracy of counting by retarded and nonretarded children, this effect being relatively greater for the latter group.