Dynamic Reorganization of Digit Representations in Somatosensory Cortex of Nonhuman Primates after Spinal Cord Injury

Abstract

Somatosensory cortices of adult primates reactivate over time after sensory loss. The time course and the neural mechanisms underlying the cortical reactivation are not well understood. Here we report that longitudinal high-resolution functional magnetic resonance imaging (fMRI) studies on anesthetized squirrel monkeys revealed dynamic reorganizations of digit activations in area 3b, within 2 months after severely disrupting afferent inputs by dorsal column section. We found that digit regions in which inputs were severely disrupted exhibited fMRI tactile responses. Reorganization was characterized by an early moving away phase and a late returning phase, as indicated by spatial shifts of individual digit activation centers in relation to the pre-lesion activation sites. Subsequent optical imaging studies confirmed fMRI activations, and dense microelectrode penetrations identified weak neuronal activity at the reactivated sites. Activation zones detected by fMRI and optical imaging were significantly larger in input-deprived than normal input single-digit regions and were larger than regions defined by neuronal spiking activity. This study captures the dynamic reorganization of digit representations after dorsal column lesions and reveals differences between functional imaging and microelectrode recording maps. Our observations suggest that subthreshold activity plays an important role in the reactivation of deafferented cortex and could promote behavioral recovery.