Pair bonding sex-specifically improves object recognition memory in monogamous prairie vole

Recent reports suggest that intimate social relationships can modulate cognitive functions by altering neuronal circuits. However, the influence of social bonding on cognition remains poorly understood. Here, we examined the effects of pair bonding on cognitive function in prairie voles (Microtus ochrogaster), a socially monogamous rodent. In the novel object recognition test, pair bonded males and females spent significantly more time investigating a novel object than a familiar one, whereas voles cohoused with a same-sex cagemate showed no such preference. However, only pair bonded females exhibited a preference index significantly above the chance level, whereas pair bonded males showed only a trend toward an increase above the chance level. In the novel location recognition test, no experimental groups preferentially explored the relocated object. The preference index showed a trend toward exceeding the chance level only in pair bonded females. Quantification of object presentation-induced c-Fos expression across 14 brain regions revealed no differences in the absolute number of c-Fos-positive cells between cagemate and pair bonded voles in either sex. However, pair bonding increased interregional correlations in the number of c-Fos-positive cell counts in males, but it decreased these correlations in females. Notably, pair bonding induced a shared correlation pattern across frontal regions including the infralimbic cortex, prelimbic cortex, anterior cingulate cortex and insular cortex in both sexes. This pattern appeared more tightly clustered in pair bonded females, suggesting greater functional coherence. Our results indicate that pair bonding enhances object recognition memory and modulates neural circuits underlying object recognition in a sex-dependent manner.