Co-development of proprioceptive afferents and the corticospinal tract within the cervical spinal cord

Abstract

In maturity, skilled movements depend on coordination of control signals by descending pathways, such as the corticospinal tract (CST), and proprioceptive afferents (PAs). An important locus for this coordination is the spinal cord intermediate zone. Convergence of CST and PA terminations onto common regions leads to interactions that may underlie afferent gating and modulation of descending control signals during movements. We determined establishment of CST and PA terminations within common spinal cord regions and development of synaptic interactions in 4-week-old cats, which is before major spinal motor circuit refinement, and two ages after refinement (weeks 8, 11). We examined the influence of one or the other system on monosynaptic responses, on the spinal cord surface and locally in the intermediate zone, evoked by either CST or deep radial nerve (DRN) stimulation. DRN stimulation suppressed CST monosynaptic responses at 4 weeks, but this converted to facilitation by 8 weeks. This may reflect a strategy to limit CST movement control when it has aberrant immature connections, and could produce errant movements. CST stimulation showed delayed development of mixed suppression and facilitation of DRN responses. We found development of age-dependent overlap of PA and CST terminations where interactions were recorded in the intermediate zone. Our findings reveal a novel co-development of different inputs onto common spinal circuits and suggest a logic to CST-PA interactions at an age before the CST has established connectional specificity with spinal circuits.