Plasticity of Primary Somatosensory Cortex Paralleling Sensorimotor Skill Recovery From Stroke in Adult Monkeys

Abstract

Adult owl and squirrel monkeys were trained to master a small-object retrieval sensorimotor skill. Behavioral observations along with positive changes in the cortical area 3b representations of specific skin surfaces implicated specific glabrous finger inputs as important contributors to skill acquisition. The area 3b zones over which behaviorally important surfaces were represented were destroyed by microlesions, which resulted in a degradation of movements that had been developed in the earlier skill acquisition. Monkeys were then retrained at the same behavioral task. They could initially perform it reasonably well using the stereotyped movements that they had learned in prelesion training, although they acted as if key finger surfaces were insensate. However, monkeys soon initiated alternative strategies for small object retrieval that resulted in a performance drop. Over several- to many-week-long period, monkeys again used the fingers for object retrieval that had been used successfully before the lesion, and reacquired the sensorimotor skill. Detailed maps of the representations of the hands in SI somatosensory cortical fields 3b, 3a, and 1 were derived after postlesion functional recovery. Control maps were derived in the same hemispheres before lesions, and in opposite hemispheres. Among other findings, these studies revealed the following 1) there was a postlesion reemergence of the representation of the fingertips engaged in the behavior in novel locations in area 3b in two of five monkeys and a less substantial change in the representation of the hand in the intact parts of area 3b in three of five monkeys. 2) There was a striking emergence of a new representation of the cutaneous fingertips in area 3a in four of five monkeys, predominantly within zones that had formerly been excited only by proprioceptive inputs. This new cutaneous fingertip representation disproportionately represented behaviorally crucial fingertips. 3) There was an approximately two times enlargement of the representation of the fingers recorded in cortical area 1 in postlesion monkeys. The specific finger surfaces employed in small-object retrieval were differentially enlarged in representation. 4) Multiple-digit receptive fields were recorded at a majority of emergent, cutaneous area 3a sites in all monkeys and at a substantial number of area 1 sites in three of five postlesion monkeys. Such fields were uncommon in area 1 in control maps. 5) Single receptive fields and the component fields of multiple-digit fields in postlesion representations were within normal receptive field size ranges. 6) No significant changes were recorded in the SI hand representations in the opposite (untrained, intact) control hemisphere. These findings are consistent with "substitution" and "vicariation" (adaptive plasticity) models of recovery from brain damage and stroke.

Remodeling of somotasensory hand representations following cerebral lesions in humans

“…This is consistent with the neurophysiological findings of animal research reviewed in the introduction indicating that the remodeling of somatosensory neural substrates subsequent to focal cortical lesions generally preserves the original neural topography. In addition, the results from AKH indicating overlapping representational surfaces for ventral digits 4 and 5 and dorsal digits 3 and 4 are consistent with the multi-digit receptive fields that have been observed subsequent to cortical lesions in animals [20]. Finally, the similarity between the results obtained for the dorsal and ventral surfaces constitutes an important contribution to the scarce literature (from either human or animal studies) regarding the plasticity of the dorsal (hairy surface) of the hands.…”

Young patients with focal seizures may have the primary motor area for the hand in the postcentral gyrus

“…A previous human study of epilepsy surgery in extratemporal lobe epilepsy suggested that surgical resection of the postcentral gyrus resulted in more pronounced deficits of the contralateral extremities compared to that after resection of the precentral gyrus (Polkey, 2000). Weakness of the contralateral hand associated with lesioning of the postcentral gyrus was attributed to loss of proprioception by the investigators (Polkey, 2000;Xerri et al, 1998).…”

“…Previous studies revealed that a lesion (Xerri et al, 1998) or cooling (Brinkman et al, 1985) confined to the presumed postcentral gyrus resulted in hemiparesis of the contralateral upper extremity in monkeys. A previous human study of epilepsy surgery in extratemporal lobe epilepsy suggested that surgical resection of the postcentral gyrus resulted in more pronounced deficits of the contralateral extremities compared to that after resection of the precentral gyrus (Polkey, 2000).…”

In Vivo Calcium Imaging Reveals Functional Rewiring of Single Somatosensory Neurons after Stroke

“…Regarding the spatial aspects of stroke-induced rewiring, studies of brain structure indicate heightened plasticity in periinfarct cortex, with enhanced axonal sprouting, synaptogenesis, and turnover of dendritic spines (Stroemer et al, 1995;Xerri et al, 1998;Cramer and Chopp, 2000;Biernaskie and Corbett, 2001;Carmichael et al, 2001;Carmichael, 2003Carmichael, , 2006Gonzalez and Kolb, 2003;Brown et al, 2007). Interestingly, dendritic spine plasticity is greatest within Ͻ1 mm of the infarct (Brown et al, 2007), indicating the need to evaluate both the function and spatial location of individual neurons in close proximity to the periinfarct cortex.…”