Valence of social information is encoded in different subpopulations of mushroom body Kenyon cells in the honeybee brain

Abstract

Over 600 Myr of evolutionary divergence between vertebrates and invertebrates is associated with considerable neuroanatomical variation both across and within these lineages. By contrast, valence encoding is an important behavioural trait that is evolutionarily conserved across vertebrates and invertebrates, and enables individuals to distinguish between positive (potentially beneficial) and negative (potentially harmful) situations. We tested the hypothesis that social interactions of positive and negative valence are modularly encoded in the honeybee brain (i.e. encoded in different cellular subpopulations) as in vertebrate brains. In vertebrates, neural activation patterns are distributed across distinct parts of the brain, suggesting that discrete circuits encode positive or negative stimuli. Evidence for this hypothesis would suggest a deep homology of neural organization between insects and vertebrates for valence encoding, despite vastly different brain sizes. Alternatively, overlapping localization of valenced social information in the brain would imply a ‘re-use' of circuitry in response to positive and negative social contexts, potentially to overcome the energetic constraints of a tiny brain. We used immediate early gene expression to map positively and negatively valenced social interactions in the brain of the western honeybee Apis mellifera. We found that the valence of a social signal is represented by distinct anatomical subregions of the mushroom bodies, an invertebrate sensory neuropil associated with social behaviour, multimodal sensory integration, learning and memory. Our results suggest that the modularization of valenced social information in the brain is a fundamental property of neuroanatomical organization.