Abstract
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.
Highlights
The primacy of movement in all animal behavior is reflected by diverse neural circuits and sensory organs dedicated to control of motor actions (Arber and Costa, 2018; Brownstone and Bui, 2010; Brownstone and Wilson, 2008; Goulding, 2009; Grillner and El Manira, 2020; Kiehn, 2016; Orlovsky et al, 1999)
We reveal a novel spinal proprioceptor organ in the adult zebrafish and demonstrate that it functions as a sensorimotor servomechanism to optimize movement for efficient locomotion
At the region of each intervertebral disc (Figure 1B, blue), we identified a ventrolateral enlargement of spinal cord tissue located under a pouch formed by protruding bones of consecutive vertebrae, connected by the flexible intervertebral disc (Figures 1B and 1C)
Summary
The primacy of movement in all animal behavior is reflected by diverse neural circuits and sensory organs dedicated to control of motor actions (Arber and Costa, 2018; Brownstone and Bui, 2010; Brownstone and Wilson, 2008; Goulding, 2009; Grillner and El Manira, 2020; Kiehn, 2016; Orlovsky et al, 1999). A central sensory mechanism for detecting such a signal has been described previously only in lampreys, which are the only vertebrate that lack a bony skeleton but have stretch-sensitive neurons along the lateral margins of their highly flexible spinal cord (Di Prisco et al, 1990; Grillner et al, 1984; McClellan and Sigvardt, 1988). It remains unclear how, in the presence of a stabilizing vertebral column, a mechanism of central proprioception could function or how this feedback could influence motor circuits controlling behavior. In all bony vertebrates, distortions of neural tissue are primarily focused at the lateral edges of intervertebral spinal cord regions, where bones, ligaments, and CNS soft tissue interact
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