Dynamic and Context-Dependent Modulation of Somatosensory Input in the Primate Primary Motor Cortex

Abstract

During voluntary movement, somatosensory input is attenuated, a phenomenon known as 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. However, whether proprioceptive signals to M1 are attenuated during movement and, if so, for what functional purpose remains unclear. We recorded somatosensory-evoked potentials (SEPs) in M1 of two male 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, consistent with previous findings for cutaneous input. However, a subset of M1 neurons preserved SEPs during static hold, particularly those evoked by afferents from antagonistic muscles and stretched skin. Because maintaining a stable posture required precise joint-angle control, these findings suggest that specific muscle and cutaneous afferents escape attenuation to provide information critical for posture control. Overall, our findings demonstrate that while proprioceptive muscle and cutaneous inputs to M1 are broadly suppressed during motor output, specific afferent signals are selectively maintained in a context-dependent manner to support posture control.