Effects of isolation-rearing on the development of social behaviors in male Mongolian gerbils (Meriones unguiculatus)

Abstract

Social isolation has been shown to modify behavioral patterns and neuroendocrine function in many species. In this study, we examined the influence of post-weaning social isolation on the behavioral development and fecal testosterone and corticosterone levels of male Mongolian gerbils. In Experiment 1, isolation-reared (IR) males spent more time engaged in social-sniffing. IR males also showed more aggressive and anxiety-related behaviors than group-reared males (GR; three animals per cage). In Experiment 2, a screen-divided-reared condition (SDR) was examined in addition to GR (two males per cage) and IR males. In the SDR group, two subjects were separated by a wire mesh screen allowing for sensory communication and limited physical contact but not direct social interactions. SDR males showed similar patterns in sniffing and anxiety-related behaviors to IR males; however, an increase in aggression was not observed. No differences in fecal testosterone and corticosterone levels were found among males in different rearing conditions. These results suggest that post-weaning social isolation affects behavioral development without affecting testosterone and corticosterone levels. The behavioral changes observed may therefore be regulated by different mechanisms; increases in social-sniffing and anxiety-related behaviors may be caused by the deprivation of direct social interactions, whereas the enhancement of aggressive behaviors may be caused by the lack of sensory stimulation and limited physical contact with other individuals.

Introduction

Social deprivation in the early stages of life modifies adult behavioral patterns, neuroanatomy, and neurochemistry in many mammals. Animals reared in conditions of social deprivation show similar behavioral symptoms as humans suffering from psychiatric disorders. Research examining the effects of social deprivation using non-human primates and rodents are therefore a useful model for understanding the basic mechanisms underlying human psychopathologies (for reviews, see [12], [20], [46]). The effects of social deprivation vary according to the age at onset of isolation (e.g., neonatal, post-weaning, and adulthood), the length of isolation, and the type of isolation (e.g., from mother or peers) [12]. Post-weaning social isolation (i.e., isolation-rearing) is one of the most thoroughly investigated forms of social deprivation. In male rats, for example, isolation-rearing enhances locomotor activity in a novel environment [5], aggressiveness [48], anxiety levels [49], and endocrinological responses to stressful events [45]. Behavioral changes induced by isolation-rearing vary according to the species and specific strain [44]. For example, isolation-rearing induces greater changes in rats than in mice [6], [39]. These results suggest that the effects of social deprivation are influenced by the social structure of the species. i.e., gregarious species living in social units are more affected than less social ones. This notion is supported by results obtained using additional types of social deprivation. These studies have shown that highly social prairie voles are more susceptible to the effects of social isolation during the postnatal period or adulthood [31], [37] compared to their less social relatives (montane and meadow voles).

The Mongolian gerbil (Meriones unguiculatus) is a small desert rodent that originates from Mongolia and northern China [1]. In nature, this species forms colonies consisting of multiple males and females. Dominant males defend their territories by attacking intruder males or by scent-marking. Scent-marking is performed by rubbing the mid-ventral sebaceous glands on small objects in the environment [51]. Unlike mice and rats, reproduction within Mongolian gerbil colonies is limited to a particular pair [38], and both males and females are involved in raising the pups [4], [7]. These characteristics indicate that this gerbil is a highly social species. It is therefore conceivable that social isolation may have an impact on behavior in this species.

In fact, several studies have demonstrated that social isolation enhanced social investigation, aggression, and anxiety-related behavior in male gerbils [35], [36], [43], although available information is very limited as compared to mice and rats. For example, it is still unclear how gerbils behaviorally and endocrinologically mature during the period between the weaning and adulthood. Given that the gerbil is becoming increasingly popular as a model for anxiety and psychopharmacological research [3], [9], [32], further fundamental studies are needed to better understand the behavioral characteristics of this species. Moreover, most previous studies on the effects of isolation-rearing in mice, rats, and gerbils have examined behavioral changes that manifest in adulthood [13], [48]. That is, they have focused only on the result of isolation-rearing, not on the process. Very few studies have examined the effects of isolation-rearing from the point of view of behavioral development [21]. Therefore, as well as clarifying the ontogeny of social behavior (i.e., scent-marking and social interactions between individuals) and endocrine development (i.e., fecal testosterone and corticosterone levels) in male Mongolian gerbils, we investigated the influence of isolation-rearing on the behavioral development and endocrinological status during the post-weaning stage in Experiment 1 of this study.

In addition, Experiment 2 was conducted to investigate the environmental factors responsible for behavioral changes induced by isolation-rearing. Isolation-rearing deprives the subjects of sensory communication (e.g., olfactory, visually, auditory, and tactile stimulation) and direct social experience between individuals (e.g., play-fighting, allogrooming). Few studies have examined the effects of these factors separately [17]. To address this issue, we introduced a rearing condition wherein subjects were housed together in a cage but were separated from each other by a wire mesh screen. This setup allowed the animals to communicate using sensory cues but prevented them from interacting directly. By observing the behavioral and physiological changes of animals reared in this condition, along with isolated or group-reared animals, the effects of direct social interaction deprivation between individuals were investigated.