Early social adversity modulates the relation between attention biases and socioemotional behaviour in juvenile macaques

Affect-biased attention may play a fundamental role in early socioemotional development, but factors influencing its emergence and associations with typical versus pathological outcomes remain unclear. Here, we adopted a nonhuman primate model of early social adversity (ESA) to: (1) establish whether juvenile, pre-adolescent macaques demonstrate attention biases to both threatening and reward-related dynamic facial gestures; (2) examine the effects of early social experience on such biases; and (3) investigate how this relation may be linked to socioemotional behaviour. Two groups of juvenile macaques (ESA exposed and non-ESA exposed) were presented with pairs of dynamic facial gestures comprising two conditions: neutral-threat and neutral-lipsmacking. Attention biases to threat and lipsmacking were calculated as the proportion of gaze to the affective versus neutral gesture. Measures of anxiety and social engagement were also acquired from videos of the subjects in their everyday social environment. Results revealed that while both groups demonstrated an attention bias towards threatening facial gestures, a greater bias linked to anxiety was demonstrated by the ESA group only. Only the non-ESA group demonstrated a significant attention bias towards lipsmacking, and the degree of this positive bias was related to duration and frequency of social engagement in this group. These findings offer important insights into the effects of early social experience on affect-biased attention and related socioemotional behaviour in nonhuman primates, and demonstrate the utility of this model for future investigations into the neural and learning mechanisms underlying this relationship across development.

Social isolation impairs the prefrontal-nucleus accumbens circuit subserving social recognition in mice

The medial prefrontal cortex (mPFC) plays important roles in social behaviors, but it is not clear how early social experiences affect the mPFC and its subcortical circuit. We report that mice singly housed for 8 weeks immediately after weaning (SH mice) show a deficit in social recognition, even after 4 weeks of re-socialization. In SH mice, prefrontal infralimbic (IL) neurons projecting to the shell region of nucleus accumbens (NAcSh) showed decreased excitability compared to normally group housed (GH) mice. Furthermore, NAcSh-projecting IL neurons were activated when the mice encountered a familiar conspecific, which was not shown in SH mice. Chemogenetic inhibition of NAcSh-projecting IL neurons in normal mice selectively impaired social recognition without affecting social interaction, whereas activation of these neurons reversed social recognition deficit in SH mice. Therefore, mPFC IL-NAcSh projection is a novel brain circuit affected by early social experience; its activation is required for the social recognition.

Associations of early social experience with offspring DNA methylation and later life stress phenotype

ABSTRACTIn a wild population of spotted hyenas, we tested the hypothesis that maternal care during the first year of life and social connectedness during two periods of early development lead to differences in DNA methylation and fecal glucocorticoid metabolites (fGCMs) later in life. We found that although maternal care and social connectedness during the communal den dependent period were not associated with fGCMs, greater social connectedness after hyenas leave their communal den is associated with lower adult fGCMs. Additionally, more maternal care and social connectedness after leaving the communal den corresponded with higher global (%CCGG) DNA methylation. Finally, we identified multiple DNA methylation biomarkers near genes involved in inflammation that may link maternal care and stress phenotype. Our findings suggest that both maternal care during the first year of life and social connections after leaving the den influence DNA methylation and contribute to a developmentally plastic stress response.