Distinct networks of expressed genes are associated with neophobia in the hippocampus of male and female Eurasian tree sparrows (Passer montanus)

Abstract

Neophobia, avoidance of novel stimuli, is an ecologically and evolutionarily relevant behavioral trait that varies among individuals and across species. Especially among wild animals, the neuromolecular mechanisms underlying individual variation in neophobia have not been well characterized. We examined three neophobic behaviors in captive female and male Eurasian tree sparrows (Passer montanus) from a wild population introduced to the USA in 1870: responses towards novel objects, novel foods, and repeated presentations of the same initially novel object. We compared transcriptomic patterns associated with neophobia in three brain regions, the striatum, dorsal hippocampus, and rostral hippocampus, using differential expression and co-expression network analyses. We found that the striatum and hippocampus had distinct transcriptomic profiles, as did the rostral and caudal subregions of the hippocampus, supporting recent hypotheses that these subregions are functionally specialized. Despite the absence of sex differences in neophobic behaviors, neophobia-associated gene modules revealed sex-specific patterns within brain regions. For females, neophobic behaviors more strongly correlated with gene modules in the caudal hippocampus, a region involved in stress and anxiety, whereas for males, neophobic behaviors correlated with gene modules in the rostral hippocampus, a region that may play a larger role in spatial cognition. These modules exhibited significant overlap, suggesting that neophobic behaviors in both females and males are driven by shared neurobiological mechanisms, though they exhibit sex-specific patterns of brain region localization. Further, this work highlights the importance of examining both male and female animals in neurobiological research.