Distributed representations of chemosensory valence in a naïve vertebrate brain

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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 Ca²⁺ 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 naïve vertebrate brain is not confined to a single sensory or motor-associated region, but is organized across a distributed, regionally structured brain-wide architecture.

HIGHLIGHTS

Naïve 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

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