Head stabilization behavior and underlying circuit mechanisms in larval zebrafish

Animals stabilize their heads to ensure stable sensory input and effective motor coordination. Head stabilization in response to vestibular stimuli is mediated by the vestibulo-collic reflex (VCR). While the VCR has been characterized in tetrapods, it remains unknown whether fish, which lack an anatomical neck, employ head-stabilization behavior. Here, we demonstrate that larval zebrafish exhibit head-stabilization behavior: during pitch tilts, they adjust their head orientation relative to the body by rostral body flexion. The rostral body flexes ventrally during head-up posture, whereas it flexes dorsally during head-down posture. These flexions partially compensate for head pitch changes, contributing to head stabilization. We identify the neural circuits and muscles responsible for these flexions. Both dorsal and ventral flexions are mediated by the same vestibular nucleus, but neural signals were transmitted through distinct pathways, either involving or bypassing a class of reticulospinal neurons. The dorsal and ventral flexions are produced by specialized dorsal and ventral muscles in the rostral body, respectively. The neural circuits underlying these body flexions share similarities with those underlying the mammalian VCR. Together, our results suggest that a head-stabilization system may have existed in ancestral fish and may have provided an evolutionary foundation upon which the tetrapod VCR emerged.