Effects of Small Ischemic Lesions in the Primary Motor Cortex on Neurophysiological Organization in Ventral Premotor Cortex

Abstract

After a cortical lesion, cortical areas distant from the site of injury are known to undergo physiological and anatomical changes. However, the mechanisms through which reorganization of distant cortical areas is initiated are poorly understood. In a previous publication, we showed that the ventral premotor cortex (PMv) undergoes physiological reorganization after a lesion destroying the majority of the primary motor cortex (M1) distal forelimb representation (DFL). After large lesions destroying >50% of the M1 DFL, the PMv DFL invariably increased in size, and the amount of the increase was positively correlated with the size of lesion. To determine whether lesions destroying <50% of the M1 DFL followed a similar trajectory, we documented PMv reorganization using intracortical microstimulation techniques after small, ischemic lesions targeting subregions within the M1 DFL. In contrast to earlier results, lesions resulted in a reduction of the PMv DFL regardless of their location. Further, because recent anatomical findings suggest a segregation of PMv connectivity with M1, we examined two lesion characteristics that may drive alterations in PMv physiological reorganization: location of the lesion with respect to PMv connectivity and relative size of the lesion. The results suggest that after a lesion in the M1 DFL, the induction of representational plasticity in PMv, as evaluated using intracortical microstimulation, is related more to the size of the lesion than to the disruption of its intracortical connections.

Effects of Motor Training on the Recovery of Manual Dexterity After Primary Motor Cortex Lesion in Macaque Monkeys

“…This analysis was only conducted in the monkey with the largest lesion and, as discussed earlier, the ICMS results did not indicate a lack of corticomotoneuronal cells to the digit muscles. Nevertheless, the lack of the ICMS-defined digit region in M1 suggests that functional compensation mainly occurs in brain regions other than M1, at least when most of the digit region is damaged, as suggested by several other studies (Biernaskie and Corbett 2001;Biernaskie et al 2005;Dancause et al 2005Dancause et al , 2006Frost et al 2003;Johansen-Berg et al 2002;Liu and Rouiller 1999;Schaechter et al 2002;Serrien et al 2004;Vandermeeren et al 2003). Although further studies are needed to clarify the mechanism underlying the recovery of digit movement after M1 lesion, the experimental model established here will be useful for studying the mechanisms of recovery of manual dexterity following brain damage.…”

Reorganization of Motor Cortex after Controlled Cortical Impact in Rats and Implications for Functional Recovery

“…A number of studies supportive of this theory have demonstrated that the motor cortex of adult mammals changes its activation patterns in response to cortical injuries. Rat and non-human primate studies using intracortical microstimulation (ICMS) to derive detailed maps of the functional representations in the motor cortex have suggested that the neural substrates mediating recovery reside within the peri-infarct cortex (CastroAlamancos and Borrel, 1995;Glees and Cole, 1949;Nudo et al, 1996b), spared motor areas in the injured hemisphere such as the premotor cortex (Dancause et al, 2006b;Frost et al, 2003), and the supplementary motor area (Eisner-Janowicz et al, 2008), as well as the cortex of the uninjured hemisphere (Reinecke et al, 2003;Rema and Ebner, 2003). Neural reorganization within these spared motor regions of the injured and uninjured hemisphere is thought to be necessary for postinjury recovery of motor function (Castro-Alamancos et al, 1992;Conner et al, 2005;Kleim et al, 2003;Liu and Rouiller, 1999;Rouiller et al, 1998).…”

“…The hand representation in the ventral premotor area (PMv) expands after an ischemic lesion in the M1 hand area (Dancause et al, 2006b;Frost et al, 2003). In addition, corticocortical axons from the spared PMv hand area sprout and form novel connections with parietal somatosensory hand areas (Dancause et al, 2005).…”

Follow-up of cortical activity and structure after lesion with laser speckle imaging and magnetic resonance imaging in nonhuman primates

“…3 The nonhuman primate model of the macaque monkey was extensively used in our laboratory to assess the extent and mechanisms of spontaneous recovery from spinal cord or motor cortex lesion and to test strategies aimed at enhancing recovery. [4][5][6][7][8][9][10][11][12] The nonhuman primate model is suitable to study the consequences of a lesion of the motor cortex, produced by various interventions (surgical lesion, block of a cerebral artery, chemical lesion), [11][12][13][14][15][16][17] and to establish possible mechanisms of recovery. 4,14 The interpretation of the behavioral data is strongly dependent on the properties of the lesion, such as its extent (volume) and its precise location.…”