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.

Shore crabs reveal novel evolutionary attributes of the mushroom body

“…In short, the crab mushroom body column appears to embody all known arrangements across Pancrustacea. If each arrangement of a specific type of intrinsic neurons represents a distinct computational property, as suggested from studies of honeybees and fruit flies ( Perisse et al, 2013 ; Traniello et al, 2019 ), then the crab would appear to be singularly well-equipped. The same applies to its calycal arrangements, which in H. nudus are elaborate and discretely partitioned into territories denoted by different morphologies of intrinsic neurons and afferents.…”

Analysis of Synaptic Microcircuits in the Mushroom Bodies of the Honeybee

“…Transcriptomic approaches or analyses of immediate early gene (IEG) expression have revealed interesting candidate genes and gene activation patterns relevant to brain plasticity [116,117]. Monitoring the spatial expression patterns of IEGs using RNA in situ hybridization or immunolabeling of IEG products may be extremely helpful in the future to identify neuronal substrates in the brain involved in structural neuronal plasticity in a specific behavioral context [118][119][120]. The crucial part, however, will be genetic manipulation experiments using knockdown or knockout techniques such as RNA interference or CRISPR/Cas9 gene editing.…”

Meta-analysis of honey bee neurogenomic response links Deformed wing virus type A to precocious behavioral maturation

“…To obtain focal bees for these studies, honeycomb frames of capped brood were stored in an incubator and newly eclosed adults were collected every 24 hours. This method has been regularly used to form groups of bees in which the exact age is known 40,41 . Therefore, we suggest that behavioral maturation-related gene expression in DWV-A infected samples was specifically due to viral infection and not conflated with experimental conditions.…”