Abstract

The zebrafish lateral line is a sensory system used to detect changes in water flow. It is comprized of clusters of superficial hair cells called neuromasts. Modulation occurs via excitatory and inhibitory efferent neurons located in the brain. Using mosaic transgenic labeling we provide an anatomical overview of the lateral line projections made by individual inhibitory efferent neurons in 5-day old zebrafish larvae. For each hemisphere we estimate there to be six inhibitory efferent neurons located in two different nuclei. Three distinct cell types were classified based on their projections; to the anterior lateral line around the head, to the posterior lateral line along the body, or to both. Our analyses corroborate previous studies employing back-fills, but our transgenic labeling allowed a more thorough characterization of their morphology. We found that individual inhibitory efferent cells connect to multiple neuromasts and that a single neuromast is connected by multiple inhibitory efferent cells. The efferent axons project to the sensory ganglia and follow the sensory axon tract along the lateral line. Time-lapse imaging revealed that inhibitory efferent axons do not migrate with the primordium as the primary sensory afferent does, but follow with an 8–14 h lag. These data bring new insights into the formation of a sensory circuit and support the hypothesis that different classes of inhibitory efferent cells have different functions. Our findings provide a foundation for future studies focussed toward unraveling how and when sensory perception is modulated by different efferent cells.

Highlights

  • Sensory systems provide information regarding the environment that is translated into behaviors aimed at increasing an organism’s chance of survival

  • All inhibitory efferent cells labeled by back-fills were labeled by the transgenic line (24 cells in 13 larvae; Figures 2F,F’,F”), indicating that the transgenic line labels all efferent cells innervating the lateral line

  • The zebrafish lateral line represents a small sensory circuit where the individual components can be analyzed in detail to understand how sensory information is processed and modulated

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Summary

Introduction

Sensory systems provide information regarding the environment that is translated into behaviors aimed at increasing an organism’s chance of survival. Inhibitory Efferent Innervation of Neuromasts overload (i.e., habituation; Groves and Thompson, 1970; Ramaswami, 2014), or supply feedforward inhibition, desensitizing sensory systems to self-induced activation (Lunsford et al, 2019; Pichler and Lagnado, 2020). The lateral line system consists of numerous sensory organs, neuromasts, which are typically arranged in superficial lines covering the head and body. Neuromasts consist of hair cells that have cilia protruding from the skin, enabling the detection of water flow and play a crucial role in behaviors such as rheotaxis, predator avoidance, and schooling (Coombs et al, 2014; Olszewski et al, 2012). As water flows past the body, the protruding cilia bend, causing the release of glutamate (Pichler and Lagnado, 2019), which is detected by the sensory afferent projections. The information is relayed to the brain (Vanwalleghem et al, 2020), so a proper behavioral response can follow

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