Neuronal Birth Order Identifies a Dimorphic Sensorineural Map

Abstract

Spatially distributed sensory information is topographically mapped in the brain by point-to-point correspondence of connections between peripheral receptors and central target neurons. In fishes, for example, the axonal projections from the mechanosensory lateral line organize a somatotopic neural map. The lateral line provides hydrodynamic information for intricate behaviors such as navigation and prey detection. It also mediates fast startle reactions triggered by the Mauthner cell. However, it is not known how the lateralis neural map is built to subserve these contrasting behaviors. Here we reveal that birth order diversifies lateralis afferent neurons in the zebrafish. We demonstrate that early-and late-born lateralis afferents diverge along the main axes of the hindbrain to synapse with hundreds of second-order targets. However, early-born afferents projecting from primary neuromasts also assemble a separate map by converging on the lateral dendrite of the Mauthner cell, whereas projections from secondary neuromasts never make physical contact with the Mauthner cell. We also show that neuronal diversity and map topology occur normally in animals permanently deprived of mechanosensory activity. We conclude that neuronal birth order correlates with the assembly of neural submaps, whose combination is likely to govern appropriate behavioral reactions to the sensory context.

Frequency response properties of primary afferent neurons in the posterior lateral line system of larval zebrafish

“…Larval zebrafish are emerging as a model vertebrate system to tackle questions on aspects of the lateral line system with unprecedented detail. While strong advances have been made in elucidating the development and organization of lateral line afferent neurons and their connected neuromasts (Alexandre and Ghysen 1999;Gompel et al 2001;Liao 2010;Nagiel et al 2008;Pujol-Marti et al 2012;Raible and Kruse 2000;Sarrazin et al 2010;Sato et al 2010), physiological studies have lagged behind Trapani and Nicolson 2011). The ability to conduct electrophysiological recordings from identified neurons in vivo in an optically transparent, model genetic system opens the door to substantially advance our functional understanding this unique sensory modality.…”

The Development and Growth of Tissues Derived from Cranial Neural Crest and Primitive Mesoderm Is Dependent on the Ligation Status of Retinoic Acid Receptor γ: Evidence That Retinoic Acid Receptor γ Functions to Maintain Stem/Progenitor Cells in the Absence of Retinoic Acid

“…5C, D). The HGn39D transgenic line was used to examine neural tissues of the lateral line system within the anterior regions of the head [23]. This analysis demonstrated a loss of anterior lateral line ganglia in the RARgagonist-treated embryos at 3 dpf compared with controls at the same time point (Fig.…”

“…Therefore, Gal4FF expression is likely to recapitulate that of the endogenous genes [22]. The transgenic zebrafish reporter line HGn39D was used to visualize the lateral line [23]. The transgenic zebrafish reporter line Tcf:mini-p was used to visualize canonical Wnt signaling [24], which was kindly provided by Dr. Ishitani (Kyushu University).…”

Sensing External and Self-Motion with Hair Cells: A Comparison of the Lateral Line and Vestibular Systems from a Developmental and Evolutionary Perspective

“…Major differences, however, exist between the two systems in how spatial information in the sensory stimulus is encoded centrally. For instance, lateral line afferent fibers project in two segregated streams either to the Mauthner cell system where these projections can initiate quick motor behavior, or to an ascending pathway where an ordered topographical representation of the sensory surface is formed in the CNS that mirrors the body surface [Alexandre and Ghysen 1999; Pujol-Martí and López-Schier 2014; Pujol-Martí et al 2012]. By contrast, vestibular afferent terminations from the various inner ear endorgans overlap extensively, reflecting convergence and synaptic interactions that relate directly to secondary neuron populations that mediate motor outputs [Straka and Dieringer 2004].…”