A specialized spinal circuit for command amplification and directionality during escape behavior.

In vertebrates, action selection often involves higher cognition entailing an evaluative process. However, urgent tasks, such as defensive escape, require an immediate implementation of the directionality of escape trajectory, necessitating local circuits. Here we reveal a specialized spinal circuit for the execution of escape direction in adult zebrafish. A central component of this circuit is a unique class of segmentally repeating cholinergic V2a interneurons expressing the transcription factor Chx10. These interneurons amplify brainstem-initiated escape commands and rapidly deliver the excitation via a feedforward circuit to all fast motor neurons and commissural interneurons to direct the escape maneuver. The information transfer within this circuit relies on fast and reliable axo-axonic synaptic connections, bypassing soma and dendrites. Unilateral ablation of cholinergic V2a interneurons eliminated escape command propagation. Thus, in vertebrates, local spinal circuits can implement directionality of urgent motor actions vital for survival.

A spinal organ of proprioception for integrated motor action feedback.

Proprioception is essential for behavior and provides a sense of our body movements in physical space. Proprioceptor organs are thought to be only in the periphery. Whether the central nervous system can intrinsically sense its own movement remains unclear. Here we identify a segmental organ of proprioception in the adult zebrafish spinal cord, which is embedded by intraspinal mechanosensory neurons expressing Piezo2 channels. These cells are late-born, inhibitory, commissural neurons with unique molecular and physiological profiles reflecting a dual sensory and motor function. The central proprioceptive organ locally detects lateral body movements during locomotion and provides direct inhibitory feedback onto rhythm-generating interneurons responsible for the central motor program. This dynamically aligns central pattern generation with movement outcome for efficient locomotion. Our results demonstrate that a central proprioceptive organ monitors self-movement using hybrid neurons that merge sensory and motor entities into a unified network.

V2a interneuron diversity tailors spinal circuit organization to control the vigor of locomotor movements.

Locomotion is a complex motor task generated by spinal circuits driving motoneurons in a precise sequence to control the timing and vigor of movements, but the underlying circuit logic remains to be understood. Here we reveal, in adult zebrafish, how the diversity and selective distribution of two V2a interneuron types within the locomotor network transform commands into an appropriate, task-dependent circuit organization. Bursting-type V2a interneurons with unidirectional axons predominantly target distal dendrites of slow motoneurons to provide potent, non-linear excitation involving NMDA-dependent potentiation. A second type, non-bursting V2a interneurons with bidirectional axons, predominantly target somata of fast motoneurons, providing weaker, non-potentiating excitation. Together, this ensures the rapid, first-order recruitment of the slow circuit, while reserving the fast circuit for highly salient stimuli involving synchronous inputs. Our results thus identify how interneuron diversity is captured and transformed into a parsimonious task-specific circuit design controlling the vigor of locomotion.