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

Abstract

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.

A Gradient in Endogenous Rhythmicity and Oscillatory Drive Matches Recruitment Order in an Axial Motor Pool

“…In zebrafish, neural networks exhibit topographic patterns of functional organization due to their order of development (Kimura et al, 2006; McLean and Fetcho, 2009; Kinkhabwala et al, 2011; Koyama et al, 2011; Miri et al, 2011; Liao and Haehnel, 2012; Pujol-Marti et al, 2012; Satou et al, 2012). In the spinal cord, the networks that are recruited during the most powerful movements are the first to develop, with slower networks layered on as zebrafish grow into free-swimming larvae.…”

Developmental and architectural principles of the lateral-line neural map

“…This result suggests that each neuron is pre-specified to occupy a particular position along the somatotopic axis. Importantly, cellular birth dating showed that neuronal morphology, behavior and projection pattern correlate with the time of neurogenesis (Liao, 2010; Pujol-Martí et al, 2010; Liao and Haehnel, 2012). During the first wave of neurogenesis, early differentiating lateralis afferents project dorsal central axons and innervate posterior neuromasts, whereas late-differentiating neurons project central axons more ventrally and innervate anterior neuromasts ( Figure 2 ).…”

“…Very recent neuroanatomical work has re-explored the projection patterns of the lateralis afferent neurons in the zebrafish larva, putting emphasis on their connectivity (Faucherre et al, 2010; Liao, 2010; Haehnel et al, 2012; Liao and Haehnel, 2012; Pujol-Martí et al, 2012). These studies have revealed two classes of lateralis afferents in the posterior lateral line (Liao and Haehnel, 2012; Pujol-Martí et al, 2012).…”

“…These studies have revealed two classes of lateralis afferents in the posterior lateral line (Liao and Haehnel, 2012; Pujol-Martí et al, 2012). The first neuronal sub-class projects central axons to contact the lateral dendrite of the Mauthner cell, a bona fide output neuron of the lateral line ( Figure 2B ; Pujol-Martí et al, 2012).…”

Optogenetic Activation of Zebrafish Somatosensory Neurons using ChEF-tdTomato

“…Animals respond to touch as early as 21 hr postfertilization (hpf), indicating that coherent somatosensory circuits have formed 5,18 . During larval development at least some trigeminal and RB neurons synapse onto the Mauthner cell to activate classic escape responses, but accumulating evidence suggests that there are multiple classes of somatosensory neurons with different patterns of connectivity that may elicit variations on the escape behavior 2,4,10,12,14,15,16,17 . Our motivation for developing this method was to characterize the behavioral function of different classes of somatosensory neurons, but this approach could in principle be used to study the function of almost any neuron or population of neurons in larval zebrafish.…”