Key Features of Structural and Functional Organization of Zebrafish Facial Motor Neurons Are Resilient to Disruption of Neuronal Migration

Abstract

SUMMARY The location of neurons early in development can be critical for their ability to differentiate and receive normal synaptic inputs. Indeed, disruptions in neuronal positioning lead to a variety of neurological disorders. Neurons have, however, shifted their positions across phylogeny, suggesting that changes in location do not always spell functional disaster. To investigate the functional consequences of abnormal positioning, we leveraged previously reported genetic perturbations to disrupt normal neuronal migration – and thus positioning – in a population of cranial motor neurons, the facial branchiomotor neurons (FBMNs). We used a combination of topographical, morphological, physiological, and behavioral analyses to determine if key functional features of FBMNs were still established in migration mutants, in spite of a dramatic rostrocaudal re-positioning of these neurons in hindbrain. We discovered that FBMNs seem remarkably resilient to a disruption in positioning, suggesting that they may not rely heavily on rostrocaudal positioning to guide their functional development. Thus, the role of positioning may vary across the developing nervous system, with some populations – like facial motor neurons – exhibiting greater resilience to abnormal positioning that permits them to shift location as a part of evolutionary change.

Hindbrain neurovascular anatomy of adult goldfish (Carassius auratus)

“…The descending branches are not present in the early larval stages of zebrafish, but are clearly visible in adult goldfish, along with a significant subventricular arterial tree that lies over the facial motor tract. Although migrating facial motoneurons are present in many vertebrates (Gilland & Baker, ), there has been no reported paralleling path of vasculature that follows the neurons (McArthur & Fetcho, ; Han et al., ). Abundant blood flow to neurons is necessary for proper functions but, presumably, supply from any nearby source would meet that need.…”

Role of branchiomotor neurons in controlling food intake of zebrafish larvae

“…The feeding deficits resulting from branchiomotor neuron ablation are likely due to effects on the movement of jaw muscles, the primary target of the trigeminal and facial branchiomotor neurons. However, food intake also involves coordination with gas exchange and swallowing, which are respectively controlled by opercular/gill muscles innervated by vagal (and some facial) branchiomotor neurons (Chandrasekhar et al, 1997; Higashijima et al, 2000; McArthur and Fetcho, 2017), and by oropharyngeal muscles (Kohei Hatta, University of Hyogo, personal communication). Our results suggest strongly that branchiomotor neurons are indispensible for controlling the motor programs involved in feeding, and establish a foundation for dissecting the neural circuits controlling food intake.…”

“…The branchiomotor neurons, a subset of cranial motor neurons (Guthrie, 2007), include the trigeminal (nV) and facial (nVII) branchiomotor neurons that innervate jaw and facial muscles (Chandrasekhar, 2004). Branchiomotor neuron organization and development have been studied extensively in zebrafish, chick and mice (Chandrasekhar et al, 1997; Higashijima et al, 2000; Lumsden and Krumlauf, 1996; McArthur and Fetcho, 2017; Studer et al, 1996). However, the formation of the neural networks driving jaw muscle movement, and the functional outputs of these circuits (jaw movement and food intake) have received less attention (McArthur and Fetcho, 2017).…”

“…Branchiomotor neuron organization and development have been studied extensively in zebrafish, chick and mice (Chandrasekhar et al, 1997; Higashijima et al, 2000; Lumsden and Krumlauf, 1996; McArthur and Fetcho, 2017; Studer et al, 1996). However, the formation of the neural networks driving jaw muscle movement, and the functional outputs of these circuits (jaw movement and food intake) have received less attention (McArthur and Fetcho, 2017). The zebrafish larva represents an excellent model to investigate the assembly and function of the motor circuits driving jaw movements.…”

“…By 5 days post-fertilization, the embryonic yolk sac has been depleted and zebrafish larvae begin exogenous feeding for nutrition. Transgenic lines expressing fluorescent reporters, cytotoxic enzymes, and calcium sensors in branchiomotor neurons and jaw muscles have been generated (Higashijima et al, 2000; Higashijima et al, 1997; Mapp et al, 2010; McArthur and Fetcho, 2017), facilitating an investigation of the organization and functional outputs of the branchiomotor circuits.…”