Reactivation of deafferented cortex plays a key role in mediating recovery of lost functions, though the precise mechanism isn’t fully understood. This study simultaneously characterized the dynamic spatiotemporal features of tactile responses in areas 3b and 1 before and 6-8 weeks after partial dorsal column lesion (DCL), and examined how the reactivation relates to the recovery of simple hand use in squirrel monkeys. A combination of high spatiotemporal resolution functional intrinsic optical imaging, microelectrode mapping, behavioral assessment, and tracer histology methods were used. Compared to the normal cortex, we found that the responses of deafferented areas 3b and 1 to 3 seconds of continuous 8Hz tactile stimulation of a single digit were significantly weaker and more transient. This finding indicates loss of responses to sustained tactile stimuli. The activation area enlarged for areas 3b and 1 in both directions along digit representation (medial-lateral) and across areas (anterior-posterior). All subjects showed behavioral deficits in food reaching-grasping-retrieving task within the first five weeks after DCL, but recovered at the time when optical images were acquired. Summarily, we showed that these populations of cortical neurons responded to peripheral tactile inputs, albeit in significantly altered manners in each area, several weeks after deafferentation. We propose that compromised ascending driven inputs, impaired lateral inhibition, and local integration of input signals may account for the altered spatiotemporal dynamics of the reactivated areas 3b and 1 cortices. Further investigation with large sample sizes is needed to fully characterize the effects of deafferentation on area 1 activation size.
Significance Statement: This study simultaneously characterized the spatiotemporal dynamics of cortical responses to peripheral tactile stimuli in deafferented area 3b and area 1 following partial dorsal column lesion in temporal and spatial resolutions that have not been achieved before. Deafferented areas 3b and 1 lost their ability to respond to sustained tactile inputs and recruited surrounding cortex for processing these inputs, but in different manners spatially and temporally. This study provides novel insights into how the modules of individual digit representations in area 3b and area 1 adapt to or compensate for loss of sensory inputs and work together to process peripheral tactile inputs to contribute to behavioral recovery of impaired hand uses in non-human primates following spinal cord injury.
Authors report no conflict of interest.
This study is supported by a Dana Foundation grant (to L.M.C.), and by a National Institutes of Health Grant R01 NS069909 to L.M.C.