Some principles of organization of spinal neurons underlying locomotion in zebrafish and their implications

Abstract

Recent studies of the spinal motor system of zebrafish, along with work in other species, are leading to some principles that appear to underlie the organization and recruitment of motor networks in cord: (1) broad neuronal classes defined by a set of transcription factors, key morphological features, and transmitter phenotypes arise in an orderly way from different dorso-ventral zones in spinal cord; (2) motor behaviors and both motoneurons and interneurons differentiate in order from gross, often faster, movements and the neurons driving them to progressively slower movements and their underlying neurons; (3) recruitment order of motoneurons and interneurons is based upon time of differentiation; (4) different locomotor speeds involve some shifts in the set of active interneurons. Here we review these principles and some of their implications for other parts of the brain, other vertebrates, and limbed locomotion.

Figure 1

Summary of principles of organization of spinal neurons. (A) Spinal neurons of particular transmitter phenotypes and morphologies are specified in a dorso-ventral fashion by the combination of transcription factors activated by gradients of diffusible morphogens. V0 interneurons are a mixture of excitatory and inhibitory cells, all with commissural axons; V1 cells are inhibitory with a primary ascending ipsilateral axon; V2 interneurons are a mixture of excitatory and inhibitory cells with a primary descending axon; V3 cells are excitatory and have either a commissural or ipsilateral descending axon. (B) A summary schematic of the developmental order of spinal circuitry and the associated movement in larval zebrafish. Neurons responsible for progressively slower movements in larvae are added as zebrafish develop. (C) Schematic summarizing the recruitment order of interneurons and motoneurons, which occurs from the bottom of spinal cord up. (D) Schematic summarizing the switch in premotor interneuron activity responsible for driving the progressive dorso-ventral activation of motoneurons as larvae swim faster and faster.