Heterogeneity and dynamics of lateral line afferent innervation during development in zebrafish (Danio rerio)

Abstract

The lateral line system of larval zebrafish is emerging as a model to study a range of topics in neurobiology, from hair cell regeneration to sensory processing. However, despite numerous studies detailing the patterning and development of lateral line neuromasts, little is known about the organization of their connections to afferent neurons and targets in the hindbrain. We found that as fish grow and neuromasts proliferate over the body surface, the number of afferent neurons increases linearly. The number of afferents innervating certain neuromasts increases over time, while it decreases for other neuromasts. The ratio of afferent neurons to neuromasts differs between the anterior and posterior lateral line system, suggesting potential differences in sensitivity threshold or spatial resolution. A single afferent neuron routinely contacts a group of neuromasts, suggesting that different afferent neurons can convey information about receptive fields along the body. When afferent projections are traced into the hindbrain, where a distinct somatotopy has been previously described, we find that this general organization is absent at the Mauthner cell. We speculate that directional input from the lateral line is less important at an early age, whereas the speed of the escape response is paramount, and that directional responses arise later in development. By quantifying morphological connections in the lateral line system, this study provides a detailed foundation to understand how hydrodynamic information is processed and ultimately translated into appropriate motor behaviors.

In vivo and in vitro biophysical properties of hair cells from the lateral line and inner ear of developing and adult zebrafish

“…per Ca 2+ channel at each ribbon between lateral line (1.2) hair cells and IHCs (1.5) indicates that the efficiency of neurotransmitter release in hair cells is likely to be very similar between the mammalian cochlea and zebrafish lateral line. How the different basolateral membrane properties of developing hair cells affect synaptic signal encoding at the afferent fibre is currently unknown, mainly because we still know little about lateral line function and organization in the adult zebrafish (Nicolson & Trapani, 2011;Haehnel et al 2012;. However, we do know that the neuromasts and afferent fibres of the zebrafish lateral line undergo extensive growth and reorganization during larval stages that result in a more complex organization in the adult, which is likely to be essential to the fine-tuning of sensitivity to movement direction .…”

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

“…To find the neuromast that was connected to the recorded afferent neuron, we systematically stimulated neuromasts along the rostro-caudal axis of the body. The afferent neurons of certain neuromasts (e.g., L 2 and L 3 ) were easier to record from than others (Haehnel et al 2011).…”

Neural Control and Modulation of Swimming Speed in the Larval Zebrafish

“…From this region, signals are conveyed to glutamatergic reticulospinal (RS) cells located in the mid and hindbrain. These RS neurons are strategically located in the pathway, where visual, postural, and other sensory inputs important for selection of appropriate motor programs are thought to converge (Haehnel et al, 2012; Kohashi and Oda, 2008; Sato et al, 2007). RS neurons excite spinal CPGs (Buchanan and Grillner, 1987; Deliagina et al, 2002; Jordan, 1998) by activating NMDA receptors essential to initiate rhythmic locomotion (Hagglund et al, 2010; McDearmid and Drapeau, 2006; Roberts et al, 2008).…”