A neural circuit basis for binasal input-enhanced chemosensory avoidance

Abstract

Optimizing navigational strategies in nature requires the detection and processing of survival-relevant cues. Our understanding of how animals utilise parallel inputs from paired sensory organs for this purpose and the underlying neural circuit mechanisms remain limited. Here we developed microfluidics-based behavioral and brainwide imaging platforms to study the neural integration of bilateral olfactory inputs and chemosensory avoidance in larval zebrafish. We show that larval zebrafish efficiently escape from cadaverine-carrying streams using undirected large turns, where both angular velocity and adaptation of turn duration exhibit bilateral olfactory input-dependence. In contrast, concomitant swim bout frequency modulation (i.e., klinokinesis) only requires unilateral input. Throughout the olfactory processing pathways, a distributed neural representation with a wide spectrum of ipsilateral-contralateral stimulus selectivity is maintained. Nonlinear sensory information gain with bilateral signal convergence is especially prominent in neurons weakly encoding unilateral cadaverine stimulus, and associated with stronger activation of sensorimotor neurons in the downstream brain regions. Collectively, these results provide insights into how the vertebrate model sums parallel input signals to guide navigational behavior.