Episodic swimming in the larval zebrafish is generated by a spatially distributed spinal network with modular functional organization

Abstract

Despite the diverse methods vertebrates use for locomotion, there is evidence that components of the locomotor central pattern generator (CPG) are conserved across species. When zebrafish begin swimming early in development, they perform short episodes of activity separated by periods of inactivity. Within these episodes, the trunk flexes with side-to-side alternation and the traveling body wave progresses rostrocaudally. To characterize the distribution of the swimming CPG along the rostrocaudal axis, we performed transections of the larval zebrafish spinal cord and induced fictive swimming using N-methyl-d-aspartate (NMDA). In both intact and spinalized larvae, bursting is found throughout the rostrocaudal extent of the spinal cord, and the properties of fictive swimming observed were dependent on the concentration of NMDA. We isolated series of contiguous spinal segments by performing multiple spinal transections on the same larvae. Although series from all regions of the spinal cord have the capacity to produce bursts, the capacity to produce organized episodes of fictive swimming has a rostral bias: in the rostral spinal cord, only 12 contiguous body segments are necessary, whereas 23 contiguous body segments are necessary in the caudal spinal cord. Shorter series of segments were often active but produced either continuous rhythmic bursting or sporadic, nonrhythmic bursting. Both episodic and continuous bursting alternated between the left and right sides of the body and showed rostrocaudal progression, demonstrating the functional dissociation of the circuits responsible for episodic structure and fine burst timing. These findings parallel results in mammalian locomotion, and we propose a hierarchical model of the larval zebrafish swimming CPG.

Visually driven chaining of elementary swim patterns into a goal-directed motor sequence: a virtual reality study of zebrafish prey capture

“…Based on the stereotypical dynamics of the basic motor pattern, we hypothesize that a symmetric command component (S) from a subset of descending reticulospinal (RS) neurons serves as a trigger to initiate a swim bout, whose frequency is set by the characteristic frequency of pattern generator modules in the spinal cord (Grillner et al, 1991; Wiggin et al, 2012). This signal may be symmetrically distributed about the midline of the RS system; currently, it is unclear which RS cells in the zebrafish hindbrain may be involved in carrying such a bilateral signal.…”

Selective Responses to Tonic Descending Commands by Temporal Summation in a Spinal Motor Pool

“…The observed effects on tail-beat frequency and the duration of swim episodes, however, implicate interactions with premotor populations. These effects could be via reticulospinal or spinal neurons (Kimura et al, 2013; Wiggin et al, 2012). Notably, spinal and reticulospinal neurons in larval zebrafish also demonstrate systematic differences in Rin related to recruitment order (Kinkhabwala et al, 2011; McLean et al, 2007; McLean et al, 2008), and so the pattern we describe here for motoneurons may also be relevant for differential activation of premotor populations.…”

Abnormal differentiation of dopaminergic neurons in zebrafish trpm7 mutant larvae impairs development of the motor pattern

“…Recordings were sampled at 10 kHz, digitized using a digitizing board (DigiData series 1440A, Molecular Devices, Sunnyvale, CA) and acquired using pClamp 10 software. Analysis of peripheral nerve activity was performed as described previously (Lambert et al, 2012; Wiggin et al, 2012), using custom scripts written in MATLAB (Mathworks, Natick MA). Briefly, the occurrence times of rhythmic fictive locomotor bursts were determined from a rectified and smoothed version of the voltage recording.…”