1. Helen Wills Neuroscience Institute and Department of Molecular and Cell Biology, University of California in Berkeley, Berkeley, California 94720, USA
2. Department of Physiology, Program in Neuroscience, University of California in San Francisco, San Francisco, California 94158-2324, USA
3. Department of Chemistry, Ludwig Maximilians-Universität, Munich, Germany
4. Physical Bioscience Division and Material Science Division, Lawrence Berkeley National Laboratory, Berkeley, California 94720, USA
5. These authors contributed equally to this work.
6. Present address: School of Biomedical Sciences, University of Queensland, Queensland 4072, Australia.

Correspondence to: Herwig Baier²Ehud Y. Isacoff^1,4 Correspondence and requests for materials should be addressed to E.Y.I. (Email: ehud@berkeley.edu) or H.B. (Email: herwig.baier@ucsf.edu).

Abstract

Locomotion relies on neural networks called central pattern generators (CPGs) that generate periodic motor commands for rhythmic movements¹. In vertebrates, the excitatory synaptic drive for inducing the spinal CPG can originate from either supraspinal glutamatergic inputs or from within the spinal cord^{2, 3}. Here we identify a spinal input to the CPG that drives spontaneous locomotion using a combination of intersectional gene expression and optogenetics⁴ in zebrafish larvae. The photo-stimulation of one specific cell type was sufficient to induce a symmetrical tail beating sequence that mimics spontaneous slow forward swimming. This neuron is the Kolmer–Agduhr cell⁵, which extends cilia into the central cerebrospinal-fluid-containing canal of the spinal cord and has an ipsilateral ascending axon that terminates in a series of consecutive segments⁶. Genetically silencing Kolmer–Agduhr cells reduced the frequency of spontaneous free swimming, indicating that activity of Kolmer–Agduhr cells provides necessary tone for spontaneous forward swimming. Kolmer–Agduhr cells have been known for over 75 years, but their function has been mysterious. Our results reveal that during early development in zebrafish these cells provide a positive drive to the spinal CPG for spontaneous locomotion.

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