Play is indispensable for an adequate development of coping with social challenges in the rat

In this study, young rats were deprived of early social interactions during weeks 4 and 5 of life. Different behavioral tests were conducted in adulthood to study the behavioral responses of rats lacking early social experiences. Juvenile deprivation resulted in decreased social activity and an altered sexual pattern, but did not affect locomotor activity or the performance in the elevated plus maze. Furthermore, behavioral and neuroendocrine responses of juvenile isolated rats were dramatically altered when they were confronted with territorial aggression. Juvenile deprived rats did not readily display a submissive posture in response to the resident and showed no immobility behavior after being returned to the resident's territory, while their plasma corticosterone and adrenaline concentrations were significantly increased compared to nonisolated controls. In contrast, behavioral responses in the shock prod test were not affected by previous isolation. The results suggest that early social experiences are vital for interactions with conspecifics later in life, i.e., aggression, sexual, and social interactions.     

Mounting behavior and receptive behavior in developing female rats and the effect of social isolation

Female rats were given daily tests for mounting behavior and lordosis behavior from the day of vaginal opening until Day 115. Regular mounting behavior appeared when the females had established adult behavioral estrous cycles of 4 days duration. Females reared in social isolation showed an increased frequency of climbing responses and were never observed to mount the stimulus female. However, the development of behavioral estrous cycles was normal in the isolated females.     

The genetic liability to stress and postweaning isolation have a competitive influence on behavioral organization in rats

Rats housed in social isolation postweaning (isolates) show profound behavioral and neurobiological differences when compared to socially housed rats (socials). Fischer rats (F344) relative to Lewis rats are hyperresponsive and significantly more susceptible to stressful stimuli. This investigation tested the hypothesis that the behavioral effects of postweaning isolation are more pronounced in a strain of rats with high susceptibility to stress compared to a strain with low susceptibility to stress. Seventy male Sprague-Dawley, Lewis, and F344 rats were housed individually or in groups at weaning on Day 21 and tested on Day 85 in the Behavioral Pattern Monitor. There was no interaction between strain and postweaning isolation for measures of locomotor activity and exploratory behavior (holepoking). However, the postweaning isolation-induced increase in the frequency of repetitive straight movements, a measure of behavioral organization, was more pronounced in Lewis isolates compared to Sprague-Dawley and F344 isolates. These results do not support the hypothesis that rats with a higher susceptibility to stress show more pronounced changes in behavior following postweaning isolation; instead, increased susceptibility to stress may counteract the repetitive movement patterns induced by social isolation.     

Developmental social isolation affects adult behavior,social interaction,and dopamine metabolite levels in zebrafish

The zebrafish is a social vertebrate and an excellent translational model for a variety of human disorders. Abnormal social behavior is a hallmark of several human brain disorders. Social behavioral problems can arise as a result of adverse early social environment. Little is known about the effects of early social isolation in adult zebrafish. We compared zebrafish that were isolated for either short (7 days) or long duration (180 days) to socially housed zebrafish, testing their behavior across ontogenesis (ages 10, 30, 60, 90, 120, 180 days), and shoal cohesion and whole‐brain monoamines and their metabolites in adulthood. Long social isolation increased locomotion and decreased shoal cohesion and anxiety in the open‐field in adult. Additionally, both short and long social isolation reduced dopamine metabolite levels in response to social stimuli. Thus, early social isolation has lasting effects in zebrafish, and may be employed to generate zebrafish models of human neuropsychiatric conditions.     

Ontogenetic interaction between social relationships and defensive burying behavior in the rat

The present experiments clarify sexual and social relationship factors related to the development of defensive burying behavior in rats. Rats were raised in isolation, or in a variety of pairs differing in sex, age or familiarity during the juvenile and post-juvenile period. In Experiment 1, decreased burying behavior was found in both male and female rats during the juvenile stage when they were reared in isolation, or with an adult female, or for males reared with a same-age female. In Experiment 2, female rats isolated during the juvenile stage who were reared after the juvenile stage with a same-sex, non-isolated rat, showed as much burying behavior as rats reared with a littermate; this was not found for male rats. When both male and female rats isolated during the juvenile stage were reared with each other after isolation, they maintained reduced burying behavior in adulthood. These sex differences in the effect of different social groupings are likely due to the differences in social relationships during the juvenile and after puberty, when social dominance relationships emerge in male rats. In Experiment 3, the effects of social dominance relationships on burying behavior were investigated in male rats. Subordination increased the freezing tendency as a passive defense, while social tension accompanied with rearing with an adult male produced decreased burying behavior as a proactive defense. These findings suggest that affiliative relationships involving playful contacts activate and maintain burying behavior, but familiarity is not a significant factor, while dominance relationships modulate the patterns of burying behavior.     

Effects of postweaning rearing condition on recovery of copulatory behavior from lesions of the medial preoptic area in rats

Bilateral lesions of the medical preoptic area (MPOA)–anterior hypothalamus of adult male rats markedly disrupt male copulatory behavior. In contrast, more group-reared then isolated male rats receiving bilateral MPOA lesions as juveniles copulated to ejaculation as adults. The present experiment was designed to analyze the role of rearing condition in promoting copulatory recovery from MPOA lesions in juvenile male rats. Juvenile male rats were given bilateral MPOA lesions or a sham operation and reared in isolation without handling, in isolation with daily handling, across a perforated Plexiglas divider from a male peer, or together with a male peer (social). Socially reared and handled males, but not isolated and divided males, with MPOA lesions showed evidence of copulatory recovery (combined socially reared and handled males vs combined isolated and divided males). These results support previous findings that postweaning rearing condition can affect copulatory recovery following juvenile MPOA lesions, but indicate that play experiences involving physical contact with peers are not necessary for such recovery to occur.     

Prenatal stress potentiates stress-induced behavior and reduces the propensity to play in juvenile rats.

We examined the hypothesis that prenatal stress potentiates defensive responsiveness which may interfere with the expression of appetitive behavioral activities. Sibling pairs of prenatally stressed and control juvenile rats were placed in an unfamiliar environment. The latency and frequency of social play, a sought-after activity of juvenile rats, were measured on 4 successive days beginning at 25 days of age. However, on Day 27, electric foot shock was administered in order to assess directly whether exposure to threat facilitates the occurrence of defensive behavior in prenatally stressed rats. In addition, to determine whether previous exposure to threat produces long-term suppressive effects on play, rats were retested on Day 28 in the absence of shock. Throughout the testing period, the latency to play, as indicated by one rat pouncing on the opponent, was significantly higher in prenatally stressed than control rats. The frequency of play, however, did not differ reliably between groups. These data suggest that prenatally stressed rats take longer to adapt to the test situation before initiating play than control rats. In both groups, exposure to shock on Day 27 significantly increased the latency to play. More importantly, prenatally stressed rats exhibited significantly higher durations of defensive freezing than control animals. When retested on Day 28, however, the duration of freezing declined significantly and no longer differed between groups. Data appear to support the hypothesis that prenatally stressed juvenile rats are responsive to stress which may modulate the inclination to exhibit social behavior.     

Preoperative differential housing and dorsal hippocampal lesions in rats

Rats housed in impoverished environments often show greater behavioral deficits after receiving brain lesions than to rats housed in standard or enriched environments. However, the resemblance between the effects of social isolation and those of hippocampal lesions in rats prompted the suggestion that rats socially isolated at weaning rather than grouped counterparts may show less behavioral change after sustaining dorsal hippocampal lesions when adult. In socially reared rats, hippocampal lesions produced increased ambulation and object contact in an open field, reduced passive avoidance in a runway task, and produced faster acquisition of active avoidance in a shuttle box, but there were no such differences in isolation-reared rats. Ambulation and object contact in isolates were intermediate to those of rats with lesions and intact group-housed rats, and the behavior of isolates during passive and active avoidance training was generally similar to that of grouped rats with lesions. The introduction of a distractor during approach training in an alley reduced running speeds more in rats with lesions than in controls. The several significant interactions between housing state and lesion state suggest that neural pathways associated with the hippocampal formation may mediate some behavioral effects of differential housing.     

Rewarding properties of social interactions in adolescent and adult male and female rats: impact of social versus isolate housing of subjects and partners

Social interactions have been shown to be rewarding for adolescent and adult rats; however, there has been little emphasis on comparing the strength of the rewarding value of social stimuli across ontogeny. Since age differences in social interactions may vary with sex or housing circumstances, the present study assessed social conditioned place preference (CPP) in adolescent and adult male and female Sprague-Dawley rats housed either socially or in isolation and conditioned with either group-housed or isolate-housed partners. Isolated animals of both sexes and ages demonstrated social CPP, with the strongest preference emerging in adolescent males. Social CPP was not evident in group-housed adults whereas group-housed adolescents developed a preference for the compartment previously paired with similarly housed partners; however, when socially housed adolescents were conditioned with isolated partners, social CPP did not emerge. Age differences in social CPP may reflect age-related neural alterations in brain systems implicated in regulation of social behavior.     

Social isolation in adolescence alters behaviors in the forced swim and sucrose preference tests in female but not in male rats

Social interactions in rodents are rewarding and motivating and social isolation is aversive. Accumulating evidence suggests that disruption of the social environment in adolescence has long-term effects on social interactions, on anxiety-like behavior and on stress reactivity. In previous work we showed that adolescent isolation produced increased reactivity to acute and to repeated stress in female rats, whereas lower corticosterone responses to acute stress and decreased anxiety-related behavior were noted in isolated males. These results indicate a sex specific impact on the effects of social stress in adolescence. However, little is known about whether social isolation impacts behaviors related to affect and whether it does so differently in male and female rats. The present study investigated the impact of adolescent social isolation from day 30-50 of age in male and female Sprague Dawley rats on behavior in the forced swim test at the end of adolescence and in adulthood and on behavior in the sucrose preference test in adulthood. Adult female rats that were isolated in adolescence exhibited increased climbing on the first and second day of the forced swim test and showed an increased preference for sucrose compared to adult females that were group-housed in adolescence. There were no effects in male rats. The results indicate that social isolation in adolescence produces a stable and active behavioral phenotype in adult female rats.     

Early life social isolation alters corticotropin-releasing factor responses in adult rats

Stress induced by early life social isolation leads to long-lasting alterations in stress responses and serotonergic activity. Corticotropin-releasing factor (CRF) is a neurotransmitter that mediates stress responses and alters serotonergic activity. We tested the hypothesis that the stress of early life isolation enhances responses to CRF in adulthood by determining the effect of CRF infusions into the dorsal raphe nucleus (dRN) on 5-HT release in the nucleus accumbens (NAc) of adult rats using in vivo microdialysis. Juvenile male rats were either isolated or housed in groups of three for a 3-week period beginning on postnatal day 21 after which, all rats were group-reared for an additional 2 weeks. Following the isolation/re-socialization procedure, infusion of 100 ng CRF into the dRN decreased 5-HT release in the NAc of group-reared rats. This treatment did not significantly affect 5-HT release in the NAc of isolation-reared animals. In contrast, infusion of 500 ng CRF into the dRN transiently increased 5-HT release in the NAc of both group-reared and isolated animals with isolated animals showing a more prolonged serotonergic response. Western blot and immunofluorescent staining for CRF receptors in the dRN showed that CRF₂ receptor levels were increased in the dRN of isolation-reared animals when compared with group-reared rats. Taken together, the results suggest that isolation during the early part of development causes alterations in both CRF receptor levels and CRF-mediated serotonergic activity. These effects may underlie the increased sensitivity to stress observed in isolates.     

Involvement of the pituitary-adrenal axis in socio-behavioral disturbances after short-term isolation

Short-term social isolation increased socio-explorative behavior of pairs of adult male Wistar rats. Hypophysectomy or adrenomedullectomy did not prevent this increase in social behavior. No differences between 7-day isolated (I) and non-isolated (socially housed, S) animals were observed in basal plasma corticosterone levels and these levels increased to the same level in I- and S-rats during individual exposure to the observation cage. The increase in corticosterone levels found immediately after the social interaction test was higher in I-than in S-rats. When I- and S-rats were tested together, a negative correlation was present between plasma-corticosterone levels and frequencies of social interactions. Blood pressure and heart rate were not affected by the isolation procedure. ACTH_1–24 (5 μg/100 g) did not affect the frequencies of social interactions, neither in I- nor in S-rats. Although a role for corticosterone in “basal” social behavior could not be excluded, it seems that pituitary-adrenal hormones are not important for the development and expression of socio-behavioral disturbances due to short-term isolation.     

Social behavior and social motivation in adolescent rats: role of housing conditions and partner's activity.

The present study investigated 1) the effects of individual and grouped housing on social investigation, social contact behavior, and play behavior in adolescent rats tested with low socially active (grouped) and high socially active (isolated) play partners; and 2) the effects of long-term (8 days) and short-term (24 h) isolation on social behavioral manifestations and social motivation in terms of preference or avoidance of play partners. Social isolation of adolescent rats activated play behavior and social behaviors different from play, but play was predominantly affected under the conditions of this study. Long-term isolation was more effective than short-term, and resulted in greater manifestation of play and social preference. Adolescent rats were able to modify their social behaviors in response to social activity of the play partner: in isolated animals exposed to low socially active group-housed partners, play behavior was transformed into social activities unrelated to play; exposure of group-housed adolescents to high socially active previously isolated partners resulted in an increase of play behavior. Testing that allowed avoidance of social contacts revealed a dissociation between manifestations of play behavior and social motivation: group-housed play partners of isolated animals showed elevated levels of play behavior but a tendency to avoid their isolated pairmates.     

Age dependent effects of space limitation and social tension on open-field behavior in male rats

Cage stocking density can be manipulated by changing in cage size and group size in the cage. The effects of these two factors were investigated in three developmental stages in male rats: juvenile, post-pubertal, and adult. An open-field test was conducted to measure exploratory behavior which was influenced by levels of activity, anxiety, and exploration. When the cage size was decreased, juvenile rats displayed decreased locomotion and lower propensity for exploration, whereas such changes were not evident in post-pubertal rats. When the group size was increased, adult rats exhibited higher locomotion. However, these factors did not affect risk assessment behavior of rats in these developmental stages. Thus, it appears that the effect of stocking density differs depending on the developmental stage of the animal: Juvenile rats increased anxiety following limiting space, whereas adult rats increased activity following increase in social tension.     

Suppression of adult copulatory behaviors following LiCl-induced aversive contingencies in juvenile male rats

Sexually immature juvenile male rats received an injection of .3 M (20 ml/kg) lithium chloride (LiCl) during each of 8-10 pairings (spaced at 2-3-day intervals) with an estrous female. Approximately seven weeks later, these males displayed fewer copulatory behaviors in pairings with estrous females than saline control rats. Noncontingent .3 M LiCl injections administered to juvenile males did not affect adult copulatory behaviors. Males that were either group or individually housed during the retention interval displayed comparable suppression, which suggests that copulatory suppression does not represent a generalized aversion to social interactions with another animal. Males housed during the retention interval in an environment that contained the odors of estrous females also displayed suppression comparable to that of males housed in the absence of such odors. This suggests that the associations that mediate copulatory suppression are not elicited solely by the odor cues of estrous females. These data demonstrate that LiCl-induced aversive contingencies in juvenile male rats subsequently suppress adult copulatory behaviors.     

Effects of social isolation on aging-induced orofacial movements in rats

World population is becoming older, and aging is a common risk factor for a number of pathologies. In this respect, it is important to study possible factors that could modify alterations implicated in the process of aging. The aim of the present study is to verify the effects of social isolation on the expression of orofacial movements in adult and old rats. Adult and old rats were housed isolated for 5 days or kept in their home cages in groups of six. Before and after this period, orofacial movements and open-field general activity were evaluated. Aging-induced orofacial movements were abolished by isolation. On the other hand, isolated adult rats presented an increase in orofacial movements. General activity was decreased by aging but was not modified by isolation. Our results indicate that social isolation produces different effects in adult and old rats, and these effects are specific for orofacial movements and not related to a decrease in general motor activity.     

The effects of isolation rearing on open-field behavior in male rats depends on developmental stages

The effects of the duration of isolation and age during isolation on open-field behavior in rats were examined. An inner wall divided the floor of the field into two areas, a peripheral alley and the center square, and the subjects' behavior in each area was measured. An increase in the tendency to avoid the center square was found in rats isolated during their juvenile stage, which disappeared if they were reared in pairs for a long period after isolation. On the other hand, subjects isolated during their postmaturity stage displayed an increased tendency to approach the center square whereas isolation during sexual maturity had no effect. The duration of isolation showed no consistent effect; rather, the effect depended on the age of the subjects during isolation. These findings suggest that isolation affects the open-field behavior of rats in various ways, depending on their age during isolation.     

Behavioral strategies of the African ice rat Otomys sloggetti robertsi in the cold

Thermoregulation in cold environments imposes great energy demands on small mammals. For the ice rat Otomys sloggetti robertsi, a herbivore endemic to high altitude alpine regions of southern Africa, these demands might be high since it does not hibernate and is poorly-adapted physiologically to low temperatures. We investigated whether ice rats modify their behavior patterns seasonally by recording the duration of behaviors as well as sequential transitions among behaviors for free-living adult males and females. Contrary to expectations, gender and time of day did not influence ice rat behavior in both seasons. However, there were marked seasonal differences in the duration of behaviors, with ice rats spending significantly more time foraging and basking in winter whereas they remained belowground in their burrows for longer periods of time in summer. Hoarding behavior increased significantly from summer to winter and females showed higher levels of hoarding in summer than males. Sequential analyses revealed that behaviors were strongly influenced by season. There were more two-way transitions in winter than in summer, indicating the occurrence of behavioral routines which might reduce energy expenditure. Our data suggest that ice rats modify their behavior in terms of the duration and sequences of behaviors in response to prevailing environmental conditions.     

Defensive behaviors and prosencephalic neurogenesis in pigeons (Columba livia) are affected by environmental enrichment in adulthood

Neurogenesis in the adult brain appears to be phylogenetically conserved across the animal kingdom. In pigeons and other adult non-oscine birds, immature neurons are observed in several prosencephalic areas, suggesting that neurogenesis may participate in the control of different behaviors. The mechanisms controlling neurogenesis and its relevance to defensive behaviors in non-oscine birds remain elusive. Herein, the contribution of the environment to behavior and neurogenesis of pigeons was investigated. Adult pigeons (Columba livia, n = 6/group), housed in standard (SE) or enriched environment (EE) for 42 days, were exposed to an unfamiliar environment (UE) followed by presentation to a novel object (NO). Video recordings of UE+NO tests were analyzed and scored for latency, duration and frequency of angular head movements, peeping, grooming, immobility and locomotion. Twenty-four hours later, pigeons were submitted to the tonic immobility test (TI) and number of trials for TI and TI duration were scored, followed by euthanasia 2 h later. Brains were immunohistochemically processed to reveal doublecortin (DCX), a marker for newborn neurons. Compared to those housed in SE, the pigeons housed in EE responded to a NO with more immobility. In addition, the pigeons housed in EE presented longer TI, more DCX-immunoreactive (DCX-ir) cells in the hippocampus and fewer DCX-ir cells in the lateral striatum than those housed in SE. There was no correlation between the number of DCX-ir cells and the scores of immobility in behavioral tests. Together, these data suggest that enrichment favored behavioral inhibition and neurogenesis in the adult pigeons through different, parallel mechanisms.     

Juvenile male mice: An attempt to accelerate testis function by exposure to adult female stimuli

Two experiments were conducted in order to determine whether juvenile male mice show accelerated maturation of testis function following chronic exposure to adult female mice. Experiment 1 showed that the maturation of testis function, as measured by radioimmunoassay of plasma androgens in post-weaning group-housed (6/cage) male mice, is most rapid between 22 and 42 days of age with peak androgen levels attained by 42 days of age. Experiment 2 showed that juvenile males exposed to an adult female through a wire mesh partition from 22 to 32 days of age show accelerated growth of an androgen-dependent accessory organ, the seminal vesicles, when compared to males housed either in direct contact with an adult female, in isolation or in groups of 2 or 6. The absence of dense housing conditions (i.e., juvenile males housed in isolation or pairs) promoted, whereas social conflict (i.e., juvenile males housed in direct contact with an adult female) and dense living conditions (i.e., juvenile males housed in groups of six) inhibited, the growth of the seminal vesicles. Because plasma androgens were unaffected by the differential housing conditions, it was speculated that the pulsatile pattern of androgen release in the mouse may have obscured possible group differences in circulating hormones.