Large-Scale Expansion of the Face Representation in Somatosensory Areas of the Lateral Sulcus after Spinal Cord Injuries in Monkeys

Abstract

Transection of dorsal columns of the spinal cord in adult monkeys results in large-scale expansion of the face inputs into the deafferented hand region in the primary somatosensory cortex (area 3b) and the ventroposterior nucleus of thalamus. Here, we determined whether the upstream cortical areas, secondary somatosensory (S2) and parietal ventral (PV) areas, also undergo reorganization after lesions of the dorsal columns. Areas S2, PV, and 3b were mapped after long-term unilateral lesions of the dorsal columns at cervical levels in adult macaque monkeys. In areas S2 and PV, we found neurons responding to touch on the face in regions in which responses to touch on the hand and other body parts are normally seen. In the reorganized parts of S2 and PV, inputs from the chin as well as other parts of the face were observed, whereas in area 3b only the chin inputs expand into the deafferented regions. The results show that deafferentations lead to a more widespread brain reorganization than previously known. The data also show that reorganization in areas S2 and PV shares a common substrate with area 3b, but there are specific features that emerge in S2 and PV.

Spinal Cord Injury Immediately Changes the State of the Brain

“…This deafferentation can lead to major long-term reorganization of cortical topographic maps, reflecting remarkable plasticity in the adult brain (Wall and Egger, 1971;Jain et al, 1997Jain et al, , 2008Bruehlmeier et al, 1998;Green et al, 1998;Curt et al, 2002;Endo et al, 2007;Ghosh et al, 2009Ghosh et al, , 2010Tandon et al, 2009). Cortical reorganization plays a critical role for functional recovery Ghosh et al, 2009;Kao et al, 2009), but excessive or aberrant reorganization can have pathological consequences, such as phantom sensations (Moore et al, 2000) and neuropathic pain (Wrigley et al, 2009).…”

Intracortical and Thalamocortical Connections of the Hand and Face Representations in Somatosensory Area 3b of Macaque Monkeys and Effects of Chronic Spinal Cord Injuries

“…The connections remain unaltered despite deafferentation of the main driving inputs from the hand to VPL and area 3b, and large-scale expansion of chin representation into the hand region of both area 3b and VPL Tandon et al, 2009;.…”

“…Somatotopy in the region of the hand and face representations in area 3b was determined before injections of neuroanatomical tracers by multiunit mapping performed under surgically sterile conditions using procedures similar to those described previously (Tandon et al, 2009).…”

“…Chronic lesions of the dorsal columns in adult primates result in large-scale brain reorganization in multiple somatosensory areas of the brain. This reorganization results in expansion of intact chin inputs into the deafferented hand region of primary somatosensory area 3b, second somatosensory area S2, parietal ventral area PV (Jain et al, , 1998aTandon et al, 2009), ventroposterior (VP) nucleus of the thalamus (Jones and Pons, 1998;Kaas et al, 1999;Jain et al, 2008), and cuneate nucleus of the brainstem . Similar reorganization in area 3b is also seen in monkeys with chronic transection of the dorsal roots from C2 to T4 (Pons et al, 1991).…”

Functional organization of motor cortex of adult macaque monkeys is altered by sensory loss in infancy

“…This reactivation produces a distorted sensory map in area 3b that no longer represents some parts of the hand and overrepresents others. This distorted map relays less than optimal sensory information to higher order sensory representations (8) and then to motor cortex, possibly altering the somatotopy of the motor representation in developing or even mature monkeys. Postlesion changes in the cortical motor map could reflect an altered use of the hand after the sensory loss, as motor cortex organization is shaped by experience (9).…”