Activation of a multisensory, multifunctional nucleus in the zebrafish midbrain during diverse locomotor behaviors

Action potentials from the brain control the activity of spinal neural networks to produce, by as yet unknown mechanisms, a variety of motor behaviors. Particularly lacking are details on how identified descending neurons integrate diverse sensory inputs to generate specific locomotor patterns. We have examined the operations of the principal neurons in an intriguing midbrain nucleus, the nucleus of the medial longitudinal fasciculus (nMLF), in the larval zebrafish. The nMLF is the most rostral grouping of neurons that projects from the brain well into the spinal cord of teleost fishes, yet there is little direct physiological data available regarding its function. We report here that a distinct set of large, individually-identifiable neurons in nMLF (the MeL and MeM neurons) are activated by diverse sensory stimuli and contribute to distinct locomotor behaviors. Using in vivo confocal calcium imaging we observed that both photic and mechanical stimuli elicit calcium responses indicative of the firing of action potentials. Calcium responses were observed simultaneously with distinct swimming, turning and struggling movements of the larval trunk. While selectively contralateral responses were at times observed in response to a head-tap stimulus, these nMLF cells showed roughly similar numbers of bilateral responses. Calcium responses were observed at a range of latencies, suggesting involvement with both slow swimming patterns and the burst swimming component of the escape behavior. The MeL cells in particular were strongly activated during light-evoked slow swimming. The activation of MeL cells during the slow and burst forward swim gaits is consistent with their driving and/or coordinating the activity of slow and fast central pattern generators in spinal cord. As such, the MeL cells may help to shape a variety of larval behaviors including the optomotor response, escape swimming and prey capture.