Social recognition and telencephalic binding sites of oxytocin in a solitary and a social Otomyine species

Abstract

This study examined the sociality of two phylogenetically closely related otomyine, murid rodent species that display differences in social behaviour in the wild. A fundamental characteristic of sociality in mammals is the ability to recognise conspecifics and discriminate between familiar and unfamiliar animals. In rodents, olfactory cues serve as the main source of such recognition and has been linked to dopaminergic reward centres in the brain, structures and regions responsible for short and long term memory, as well as neural processes involved in reducing stress. The neuropeptide, oxytocin, is produced by hypothalamic cells and can act as a neurotransmitter. Recent work has linked these neural, telencephalic structures (the nucleus accumbens, amygdala and hippocampus) to social recognition and oxytocin. Oxytocinergic receptor density is greater in such regions in social, monogamous or gregarious rodents, whereas it is much less in solitary species. Experimental studies have found mechanistic links between oxytocin function and social recognition and discrimination in laboratory mice and rats. However, no known study has tested social recognition and discrimination in wild-caught, non-typical model species in conjunction with a description of their oxytocinergic neuroanatomy. This justified my study to investigate whether the social-living, gregarious, colonial ice rat, Otomys sloggetti robertsi, show similar oxytocin receptor binding to other social species, and whether it has the ability to recognise conspecifics and discriminate between familiar and unfamiliar animals. Similarly, I investigated and compared these traits in a solitary, phylogenetically closely related species, the vlei rat, Otomys auratus.

Neither sexes of both species showed social recognition abilities based on olfactory cues. This was surprising, as social-living ice rats were predicted to display recognition abilities. Interestingly, female vlei rats showed the ability to discriminate between a familiar and novel conspecific. The results suggest that vlei and ice rats exhibit social recognition flexibility, while social discrimination demonstrated by solitary female vlei rats may provide adaptive advantages in the wild. The impaired social recognition and discrimination observed by ice rats may be explained by their temporal flexibility in social behaviour in the wild. Colonial living and social tolerance by ice rats may indicate phenotypical plasticity, or ‘social flexibility’, to harsh ecological constraints.

In contrast, the neuroanatomy of vlei and ice rats reflects their wild behaviour. Neural oxytocin receptor binding sites, identified using ligand-binding receptor autoradiography, were more intense in the nucleus accumbens, islands of Calleja, claustrum, indusium griseum, prefrontal cortex, insular cortices, extended amygdala, bed nuclei of the stria terminalis and hypothalamic nuclei of the ice rats, compared to that of the vlei rats. The overall patterns of neural oxytocin receptor (OTR) binding in ice rats are similar to that found in social voles, while that of vlei rats and solitary voles are comparable, particularly the binding intensities observed in the lateral septum. The brains of the vlei rat had OTR binding in the medial habenula and dentate gyrus, which was absent in the ice rat brains. Similarly, OTR binding was only detected in the subfields of hippocampus, intermediodorsal and rhomboid thalamic nuclei in the brain of the ice rats. As predicted from their social behaviour in the wild, the telencephalic OTR binding of the two species reflected their socially disparate behaviour, similar to other studies. Based on the lack of extreme differences in behavioural data, and various similarities in oxytocinergic receptor binding sites in the telencephalic structures, I suggest that a continuum of oxytocinergic effects on social, group-living behaviour of these related species may exist in this otomyine group. The differences in neuropeptidergic circuitry in these two species contributes further to our understanding of evolutionary neuroendocrinology of sociality.