Proprioception revisited: where do we stand?

Abstract

Originally referred to as 'muscle sense', the notion that skeletal muscle held a peripheral sensory function was first described early in the 19^th century. Foundational experiments by Sherrington in the early 20^th century definitively demonstrated that proprioceptors contained within skeletal muscle, tendons, and joints are innervated by sensory neurons and play an important role in the control of movement. In this review, we will highlight several recent advances in the ongoing effort to further define the molecular diversity underlying the proprioceptive sensorimotor system. Together, the work summarized here represents our current understanding of sensorimotor circuit formation during development and the mechanisms that regulate the integration of proprioceptive feedback into the spinal circuits that control locomotion in both normal and diseased states.

Figure 1.. Sensorimotor circuits involved in locomotion

(a) Changes in muscle length are detected by group Ia sensory afferents (green) coiled around the non-contractile region of muscle spindles. γMNs (red) innervate intrafusal muscle fibers to regulate the sensitivity of stretch-sensitive muscle spindles. In the monosynaptic stretch reflex circuit, lengthening of skeletal muscle induces a deformation stimulus that activates group Ia sensory afferents, which form direct synaptic contacts on synergistic motor neurons to promote muscle contraction. Ptf1a-lineage GABApre interneurons (light blue) presynaptically inhibit monosynaptic proprioceptive feedback. (b) pSN afferents form more complex, polysynaptic connections with motor neurons. The box on the far right illustrates the innervation pattern of pSN afferents in skeletal muscle, including muscle spindle group Ia/II afferents and GTO Ib afferents. Different classes of sensory neurons exhibit different central termination patterns with cutaneous afferents ending in more dorsally (purple box) and proprioceptive afferents ending in the intermediate spinal cord (green box). Like monosynaptic circuits, polysynaptic proprioceptive and cutaneous sensory inputs are subject to presynaptic inhibition from different classes of GABApre neurons. More specifically, dorsal Ptf1a-lineage GABApre neurons (blue) target cutaneous afferents while Pax2⁺/Rorβ⁺ GABApre neurons (light/dark blue) target proprioceptive afferents that synapse on premotor interneurons.