Subsets of extraocular motoneurons produce kinematically distinct saccades during hunting and exploration

Animals construct diverse behavioral repertoires by moving a limited number of body parts with varied kinematics and patterns of coordination. There is evidence that distinct movements can be generated by changes in activity dynamics within a common pool of motoneurons or by selectively engaging specific subsets of motoneurons in a task-dependent manner. However, in most cases, we have an incomplete understanding of the patterns of motoneuron activity that generate distinct actions and of how upstream premotor circuits select and assemble such motor programs. In this study, we used two closely related but kinematically distinct types of saccadic eye movement in larval zebrafish as a model to examine circuit control of movement diversity. In contrast to the prevailing view of a final common pathway, we found that in the oculomotor nucleus, distinct subsets of motoneurons were engaged for each saccade type. This type-specific recruitment was topographically organized and aligned with ultrastructural differences in motoneuron morphology and afferent synaptic innervation. Medially located motoneurons were active for both saccade types, and circuit tracing revealed a type-agnostic premotor pathway that appears to control their recruitment. By contrast, a laterally located subset of motoneurons was specifically active for hunting-associated saccades and received premotor input from pretectal hunting command neurons. Our data support a model in which generalist and action-specific premotor pathways engage distinct subsets of motoneurons to elicit varied movements of the same body part that subserve distinct behavioral functions.