Two distinct proprioceptive representations of voluntary movements in primate spinal neurons

Abstract

When willingly setting our body in motion, we simultaneously know where and how our limbs are moving. While this indicates that proprioceptive information is readily represented in the neurons of the central nervous system, it is still unclear how. We recorded the activity of spinal neurons with direct projections from muscle spindle afferents in four monkeys, while they performed simple wrist movements. Against the assumption that these spinal neurons act as a simple relay of afferent input, we found the majority (56%) of neurons had firing patterns incongruent with a simple representation of spindle activity, and the minority had congruent patterns. Two groups of neurons showed distinct intrinsic characteristics (spike width, base firing rate and firing irregularity), and distinct control of their input-output gain. These results are the first demonstration that proprioceptive representation is achieved by the coordinated activity of distinct groups of neurons during volitional movement.

Proprioception and the predictive sensing of active self-motion

“…Indeed, recent work by Seki and colleagues provides clear support for this proposal. During active movements, the essential information provided about the position and movement of limbs by the proprioceptive system [ 22 , 23 ] is actually facilitated rather than suppressed at the level of the spinal cord [ 24•• , 25 , 26 ]. Further, movement-specific facilitation has been reported at subsequent stages of proprioceptive processing from the dorsal column–medial lemniscus pathway to the somatosensory thalamus [ 24•• , 27 ].…”