Chemosensory modulation of eye-body coordination in larval zebrafish

Coordinated eye-body movements are essential for many animal behaviors, yet the influence of chemosensory inputs on these movements remains underexplored. Here, we enhance the Fish-On-Chips optofluidic platform to reveal that larval zebrafish use coupled saccade-tail flips for chemosensory avoidance, but not pursuit. Spontaneous saccades, which alternate in direction, are closely synchronized with tail flips via anticipatory adjustments in tail flip event rate, directionality, and kinematics. In response to ethologically representative chemosensory cues, this coordination is differentially modulated based on valence. Aversive chemical cues increase saccade frequency and the proportion of saccade-coupled tail flips, while also enhancing the turning intent as the coupling strengthens. Conversely, appetitive chemicals promote more sustained gliding movements without impacting saccades or their tail flip coupling. Brain-wide neuronal activity imaging reveals that the pallium, a cortical homolog in teleosts, strongly represents the sensorimotor transformation of aversive cue-associated coupled saccade-tail flips. Our findings underscore the critical role of chemosensory cues in regulating eye-body coordination in an early vertebrate species, highlighting a deep evolutionary integration of sensory inputs to optimize locomotion.