Distributed representations of chemosensory valence in a naive vertebrate brain

Abstract

Chemical cues guide essential behaviors by signaling food, danger, and social information. A major dimension of chemosensory processing is valence, which biases animals toward approach or avoidance, yet its brain-wide organization in vertebrates remains unclear. Here, we used larval zebrafish to map neuronal activity associated with behaviorally defined appetitive and aversive chemosensory cues. Free-swimming assays identified a chemically diverse stimulus panel that elicited robust approach or avoidance, and key valence-dependent motor signatures were preserved during partially immobilized two-photon Ca{superscript 2} imaging with simultaneous tail tracking. Brain-wide activity revealed partly distinct patterns of stimulus identity, valence-related activity, and movement-correlated neuronal recruitment. Stimulus identity was strongest in the olfactory bulb and pallium, whereas small, coordinated valence-related populations were distributed across multiple telencephalic and diencephalic regions. These populations were partly separable from movement-correlated neurons, especially in forebrain regions, but showed valence-specific, opposing relationships with motor output. Together, our findings show that chemosensory valence-related activity in a naive vertebrate brain is not confined to a single sensory or motor-associated region, but is organized across a distributed, regionally structured brain-wide architecture. HIGHLIGHTSNaive larval zebrafish show appetitive and aversive chemosensory behaviors that are preserved during imaging Chemosensory stimuli evoke widespread brain activity, revealing distributed stimulus identity and valence representations Valence-encoding neurons form small, coordinated populations across multiple forebrain regions Valence-related activity is partly separable from movement-correlated activity