Principles Governing Locomotion in Vertebrates: Lessons From Zebrafish

Abstract

Locomotor behaviors are critical for survival and enable animals to navigate their environment, find food and evade predators. The circuits in the brain and spinal cord that initiate and maintain such different modes of locomotion in vertebrates have been studied in numerous species for over a century. In recent decades, the zebrafish has emerged as one of the main model systems for the study of locomotion, owing to its experimental amenability, and work in zebrafish has revealed numerous new insights into locomotor circuit function. Here, we review the literature that has led to our current understanding of the neural circuits controlling swimming and escape in zebrafish. We highlight recent studies that have enriched our comprehension of key topics, such as the interactions between premotor excitatory interneurons (INs) and motoneurons (MNs), supraspinal and spinal circuits that coordinate escape maneuvers, and developmental changes in overall circuit composition. We also discuss roles for neuromodulators and sensory inputs in modifying the relative strengths of constituent circuit components to provide flexibility in zebrafish behavior, allowing the animal to accommodate changes in the environment. We aim to provide a coherent framework for understanding the circuitry in the brain and spinal cord of zebrafish that allows the animal to flexibly transition between different speeds, and modes, of locomotion.

Behavioral Responses of Javanese Medaka (Oryzias Javanicus) Versus Zebrafish (Danio Rerio) in Open Field Test.

“…Locomotion is integral for animal survivability to navigate foods, shelters and evade predators (Kiehn and Dougherty, 2016). Diverse modes of locomotion regulated by homologous circuit of central nervous system in vertebrates have been well documented in numerous species for centuries (Berg, et al, 2018).…”

Walking with Salamanders: From Molecules to Biorobotics

“…Thus, the lamprey studies are an invaluable inspiration for the studies in genetically tractable vertebrate models, which are increasingly used to dissect locomotor circuitries. Experiments in zebrafish using genetic tools have uncovered a modular organisation of spinal cell populations controlling speed ( Figure 1B, for review, see [25,26]), the role of reticulospinal neurons in providing excitation to spinal swimming circuits [27] and in the control of steering movements [28], and a key role for mechanosensory feedback in the control of swimming [29][30][31] (Figure 1B). In mice, several cell types have recently been genetically defined, including MLR cells controlling locomotor speed and gait transitions [32][33][34], reticulospinal cell types relaying locomotor commands [35][36][37] or steering commands to the spinal cord [38], and spinal cell types involved in locomotor rhythmogenesis and coordination (for review, see [39]) ( Figure 1D).…”

Dopaminergic Co-Regulation of Locomotor Development and Motor Neuron Synaptogenesis is Uncoupled by Hypoxia in Zebrafish

“…The vertebrate motor system offers a well-characterized model for understanding functional effects of hypoxia-associated connectivity changes. Development of motor function is a tightly regulated process, involving genetically encoded programs and specification of neuronal types and connections (Garcia-Campmany et al, 2010), but also feedback from environmental pathways, such as central pattern generators (CPGs; Berg et al, 2018;D'Elia and Dasen, 2018). The neurotransmitter dopamine has been identified as a critical mediator in several distinct aspects of motor development: dopamine is a brain-derived signaling factor affecting neurogenesis in the spine (Popolo et al, 2004;Reimer et al, 2013); descending projections from the dopaminergic diencephalospinal tract (DDT) are required for vertebrate locomotor maturation; and it is required for regulation of locomotion (Jay et al, 2015;Sharples et al, 2015).…”