Dynamic and context-dependent modulation of proprioceptive input in primate primary motor cortex

During voluntary movement, somatosensory input is attenuated—sensory gating—which may prevent the CNS from being overwhelmed by predictable afferent feedback not essential for motor control. In the cerebral cortex, sensory gating has been demonstrated in primary (S1) and higher-order sensory areas. The primary motor cortex (M1) is the major cortical output relay to the spinal cord and muscles, and proprioceptive feedback is crucial for shaping motor output, much as in S1. However, whether proprioceptive signals to M1 are attenuated during movement, and if so, why, remains unclear. We recorded somatosensory-evoked potentials (SEPs) in M1 of two monkeys performing a wrist task while electrically stimulating muscle and cutaneous afferents innervating forearm extensors and adjacent skin. Both local field potentials and single-neuron recordings revealed significant suppression of muscle-evoked SEPs during Active movement and Static hold phases, providing direct evidence that proprioceptive input to M1 is generally gated during motor execution, as previously reported for cutaneous input. Yet, amidst this suppression, SEPs in a subset of M1 neurons were preserved during Static hold, especially those evoked by antagonist muscle afferents. Because monkeys had to maintain precise joint angles for stable posture, these results suggest that proprioceptive signals from antagonist muscles—likely reflecting spindle activity in lengthening muscles—escape attenuation to provide information essential for joint angle control. Overall, our findings demonstrate that while proprioceptive input to M1 is broadly suppressed during motor output, specific afferent signals from antagonist muscles are selectively maintained in a context-dependent manner to support posture control.