Volumetric effects of motor cortex injury on recovery of ipsilesional dexterous movements

Abstract

Damage to the motor cortex of one hemisphere has classically been associated with contralateral upper limb paresis, but recent patient studies have identified deficits in both upper limbs. In non-human primates, we tested the hypothesis that the severity of ipsilesional upper limb motor impairment in the early post-injury phase depends on the volume of gray and white matter damage of the motor areas of the frontal lobe. We also postulated that substantial recovery would accompany minimal task practice and that ipsilesional limb recovery would be correlated with recovery of the contralesional limb. Gross (reaching) and fine hand motor functions were assessed for 3-12 months post-injury using two motor tests. Volumes of white and gray matter lesions were assessed using quantitative histology. Early changes in post-lesion motor performance were inversely correlated with white matter lesion volume indicating that larger lesions produced greater decreases in ipsilesional hand movement control. All monkeys showed improvements in ipsilesional hand motor skill during the post-lesion period, with reaching skill improvements being positively correlated with total lesion volume indicating larger lesions were associate with greater ipsilesional motor skill recovery. We suggest that reduced trans-callosal inhibition from the lesioned hemisphere may play a role in the observed skill improvements. Our findings show that significant ipsilesional hand motor recovery is likely to accompany injury limited to frontal motor areas. In humans, more pronounced ipsilesional motor deficits that invariably develop after stroke may, in part, be a consequence of more extensive subcortical white and gray matter damage.

Recovery of precision grasping after motor cortex lesion does not require forced use of the impaired hand in macaca mulatta

“…It is abundantly clear from the present findings, including our previous work and classical work that the non-human primate brain is capable of considerable recovery of function after lesions that damage a substantial portion of the arm/hand areas of M1, LPMC and other frontal lobe areas (Darling et al 2009; Darling et al 2011a). This has important implications for rehabilitation therapies as nearly exclusive forced-use of the impaired hand for an extended period of time, as in constraint induced movement therapy (Taub et al 1993; Wolf et al 2006), may not be required to enhance recovery of hand function after lesions limited to lateral frontal lobe motor areas that spare a portion of M1c.…”

“…After detailed microscopic analysis, the cortical and subcortical limits of each lesion site were plotted onto anatomically homologous Nissl stained tissue sections from the non-lesioned hemisphere (see Figs. 1 and 3 of Darling et al 2011) using the microscope and an attached MAC 5000 motorized stage (Ludl Electronic Products, Hawthore, NY) which was connected to Neurolucida data collection software system (MBF Bioscience, Williston, Vermont, USA). Gray matter and white matter lesion site volumes were then calculated using Neurolucida software as previously described (Pizzimenti et al, 2007; Darling et al, 2009).…”

Role of primary motor cortex in the control of manual dexterity assessed via sequential bilateral lesion in the adult macaque monkey: A case study

“…5B and 6B; percentages above 100% in Table 1 for the left hand in Ac-P1, Rec-P1 and Pl-P1 periods; see also Darling et al, 2011a;Manganotti et al, 2008;Kaeser et al, 2010). Using transcranial magnetic stimulation, the unaffected hemisphere has been reported to be disinhibited during the early period following a unilateral stroke, as suggested by the loss of the interhemispheric connection originating from the lesioned hemisphere (Shimizu et al, 2002).…”

Laterality affects spontaneous recovery of contralateral hand motor function following motor cortex injury in rhesus monkeys

“…After detailed microscopic analysis, the cortical and subcortical limits of each lesion site were plotted onto anatomically homologous Nissl-stained tissue sections from the non-lesioned hemisphere (see Figs. 1 and 3 of Darling et al 2011) using the microscope and an attached MAC 5000 motorized stage (Ludl Electronic Products, Hawthore, NY, USA) which was attached to Neurolucida data collection software (MBF Bioscience, Williston, VT, USA). Gray matter and white matter lesion site volumes were then calculated using Neurolucida software as previously described (Pizzimenti et al 2007; Darling et al 2009).…”