Physiology of afferent neurons in larval zebrafish provides a functional framework for lateral line somatotopy

Fishes rely on the neuromasts of their lateral line system to detect water flow during behaviors such as predator avoidance and prey localization. Although the pattern of neuromast development has been a topic of detailed research, we still do not understand the functional consequences of its organization. Previous work has demonstrated somatotopy in the posterior lateral line, whereby afferent neurons that contact more caudal neuromasts project more dorsally in the hindbrain than those that contact more rostral neuromasts (Gompel N, Dambly-Chaudiere C, Ghysen A. Development 128: 387-393, 2001). We performed patch-clamp recordings of afferent neurons that contact neuromasts in the posterior lateral line of anesthetized, transgenic larval zebrafish (Danio rerio) to show that larger cells are born earlier, have a lower input resistance, a lower spontaneous firing rate, and tend to contact multiple neuromasts located closer to the tail than smaller neurons, which are born later, have a higher input resistance, a higher spontaneous firing rate, and tend to contact single neuromasts. We suggest that early-born neurons are poised to detect large stimuli during the initial stages of development. Later-born neurons are more easily driven to fire and thus likely to be more sensitive to local, weaker flows. Afferent projections onto identified glutamatergic regions in the hindbrain lead us to hypothesize a novel mechanism for lateral line somatotopy. We show that afferent fibers associated with tail neuromasts respond to stronger stimuli and are wired to dorsal hindbrain regions associated with Mauthner-mediated escape responses and fast, avoidance swimming. The ability to process flow stimuli by circumventing higher-order brain centers would ease the task of processing where speed is of critical importance. Our work lays the groundwork to understand how the lateral line translates flow stimuli into appropriate behaviors at the single cell level.