Rapid experience-dependent tuning of spinal and transcortical stretch reflexes supports goal-directed movement

Abstract

The short-latency stretch reflex (SLR) is the fastest sensorimotor response in human limbs. The spinal SLR scales with background muscle activity and is affected by recent movement history. But adaptive plasticity of spinal reflexes has classically been studied through operant conditioning, which induces an arbitrary change in reflex size over days to weeks. In contrast, rapid, experience-dependent feedback adaptation is often attributed to transcortical mechanisms underlying the long-latency reflex (LLR). Whether task constraints can progressively shape the SLR within a single session remains unclear. Here, naive human adults (n = 16; 9 females, 7 males) performed an instructed-delay reaching task while holding a robotic manipulandum which delivered brief haptic perturbations during action preparation. We recorded high-density surface electromyography (64-channel arrays) from the pectoralis major and posterior deltoid to investigate reflex gains. Pre-perturbation muscle activity showed no systematic goal-directed change. With a long-enough preparatory delay (750 ms), SLR gains decreased progressively with experience when the planned movement was expected to stretch the homonymous muscle, rather than shorten it. This tuning occurred in both muscles, was evident within individual participants, and was accompanied by a corresponding decrease in reflexively generated force opposing perturbations toward the cued target. No such tuning was detected with a short preparatory delay (250 ms). LLR responses were goal-directed from the first trial blocks and progressed in a comparable manner across the session, at both preparatory delays. Our study shows that spinal feedback circuits can progressively adapt within a single session to support the performance of goal-directed movements.