Effective Sensory Modality Activating an Escape Triggering Neuron Switches during Early Development in Zebrafish

Developing nervous systems grow to integrate sensory signals from different modalities and to respond through various behaviors. Here, we examined the development of escape behavior in zebrafish [45-170 h postfertilization (hpf)] to study how developing sensory inputs are integrated into sensorimotor circuits. Mature fish exhibit fast escape upon both auditory/vestibular (AV) and head-tactile stimuli. Newly hatched larvae, however, do not respond to AV stimuli before 75 hpf. Because AV-induced fast escape in mature fish is triggered by a pair of hindbrain neurons known as Mauthner (M) cells, we studied functional development of the M-cell circuit accounting for late acquisition of AV-induced escape. In fast escape elicited by head-directed water jet, minimum onset latency decreased throughout development (5 ms at 45-59 hpf, 3 ms after 75 hpf). After 75 hpf, lesioning the otic vesicle (OV) to eliminate AV input resulted in loss of short-latency (< 5 ms) fast escape, whereas ablation of the sensory trigeminal ganglion (gV) to block head-tactile input did not. Before 75 hpf, however, fast escape persisted after OV lesion but disappeared after gV ablation. Laser ablation of the M-cell and Ca2+ imaging of the M-cell during escape demonstrated that M-cell firing is required to initiate short-latency fast escapes at every developmental stage and further suggest that head-tactile input activates the M-cell before 75 hpf, but that after this point AV input activates the M-cell instead. Thus, a switch in the effective sensory input to the M-cells mediates the acquisition of a novel modality for initiating fast escape.