Forelimb training drives transient map reorganization in ipsilateral motor cortex

Abstract

Skilled motor training results in reorganization of contralateral motor cortex movement representations. The ipsilateral motor cortex is believed to play a role in skilled motor control, but little is known about how training influences reorganization of ipsilateral motor representations of the trained limb. To determine whether training results in reorganization of ipsilateral motor cortex maps, rats were trained to perform the isometric pull task, an automated motor task that requires skilled forelimb use. After either 3 or 6 months of training, intracortical microstimulation (ICMS) mapping was performed to document motor representations of the trained forelimb in the hemisphere ipsilateral to that limb. Motor training for 3 months resulted in a robust expansion of right forelimb representation in the right motor cortex, demonstrating that skilled motor training drives map plasticity ipsilateral to the trained limb. After 6 months of training, the right forelimb representation in the right motor cortex was significantly smaller than the representation observed in rats trained for 3 months and similar to untrained controls, consistent with a normalization of motor cortex maps. Forelimb map area was not correlated with performance on the trained task, suggesting that task performance is maintained despite normalization of cortical maps. This study provides new insights into how the ipsilateral cortex changes in response to skilled learning and may inform rehabilitative strategies to enhance cortical plasticity to support recovery after brain injury.

The ipsilateral corticospinal responses to cross-education are dependent upon the motor-training intervention

“…Intriguingly, non-paced strength training had no effect on CSE or SICI. This finding is consistent with previous studies, whereby skilled motor training leads to the functional reorganization of movement representation maps in contralateral M1 and the ipsilateral M1 (Pruitt et al 2016), but is absent following repetitive unskilled motor training (Kleim et al 1998;Plautz et al 2000;Carroll et al 2002). Therefore, the ipsilateral corticospinal adaptations to unilateral visuomotor training and slow-paced strength training are distinct to that of non-paced strength training, despite no differences in the extent of the cross-education effect.…”

“…In the context of cross-education and bilateral transfer, several acute studies that have used TMS have shown increased CSE (Muellbacher et al 2000;Hortobágyi et al 2003;Perez and Cohen 2008;Howatson et al 2011;Frazer et al 2017), decreased SICI (Perez and Cohen 2008;Leung et al 2015), and decreased interhemispheric inhibition (IHI) (Perez and Cohen 2008;Howatson et al 2011) in the iM1. While some structural changes occur within several motor areas (Ruddy et al 2017;Pruitt et al 2016), experimental findings from chronic cross-education studies support a mixture of increased CSE (Hendy et al 2015;Kidgell et al 2011;Kidgell et al 2015) and a decrease in cortical inhibition (SICI, IHI and silent period duration) (Hortobágyi et al 2011;Hendy et al 2012;Kidgell et al 2015;Coombs et al 2016;Mason et al 2017) in the neural structures innervating the untrained limb.…”

“…It is well accepted that motor learning is associated with functional changes (i.e., plasticity) within several regions of the cerebral cortex, including pre-motor areas and M1 (Fu et al 1995;Butefisch et al 2000;Hardwick et al 2013;Doyon and Benali 2005). There is a growing body of literature that suggests plasticity within the M1 is the most likely cortical adaptation following cross-education, simply because of the important role that the M1 plays in the early phases of motor learning (Muellbacher et al 2002;Pruitt et al 2016). In the context of cross-education and bilateral transfer, several acute studies that have used TMS have shown increased CSE (Muellbacher et al 2000;Hortobágyi et al 2003;Perez and Cohen 2008;Howatson et al 2011;Frazer et al 2017), decreased SICI (Perez and Cohen 2008;Leung et al 2015), and decreased interhemispheric inhibition (IHI) (Perez and Cohen 2008;Howatson et al 2011) in the iM1.…”

Traumatic Brain Injury Occludes Training-Dependent Cortical Reorganization in the Contralesional Hemisphere

“…1C). 25 Rats were anesthetized with a cocktail of ketamine hydrochloride (50 mg/kg), xylazine (20 mg/kg), and acepromazine (5 mg/kg) injected intramuscularly, and given supplemental doses as needed.…”

“…The maximum stimulation intensity was chosen based on previous studies that indicate ipsilateral motor responses are evoked at higher currents than contralateral responses. 25,32,33 The presence of ipsilateral forelimb movement was first determined, and the current was then lowered to find the lowest threshold at which ipsilateral movement was reliably evoked. After determining the threshold current for ipsilateral responses, the current was again lowered until a threshold was found for contralateral movement.…”