Structural integrity of callosal midbody influences intermanual transfer in a motor reaction-time task

Abstract

Training one hand on a motor task results in performance improvements in the other hand, also when stimuli are randomly presented (nonspecific transfer). Corpus callosum (CC) is the main structure involved in interhemispheric information transfer; CC pathology occurs in patients with multiple sclerosis (PwMS) and is related to altered performance of tasks requiring interhemispheric transfer of sensorimotor information. To investigate the role of CC in nonspecific transfer during a pure motor reaction-time task, we combined motor behavior with diffusion tensor imaging analysis in PwMS. Twenty-two PwMS and 10 controls, all right-handed, were asked to respond to random stimuli with appropriate finger opposition movements with the right (learning) and then the left (transfer) hand. PwMS were able to improve motor performance reducing response times with practice with a trend similar to controls and preserved the ability to transfer the acquired motor information from the learning to the transfer hand. A higher variability in the transfer process, indicated by a significantly larger standard deviation of mean nonspecific transfer, was found in the PwMS group with respect to the control group, suggesting the presence of subtle impairments in interhemispheric communication in some patients. Then, we correlated the amount of nonspecific transfer with mean fractional anisotropy (FA) values, indicative of microstructural damage, obtained in five CC subregions identified on PwMS's FA maps. A significant correlation was found only in the subregion including posterior midbody (Pearson's r = 0.74, P = 0.003), which thus seems to be essential for the interhemispheric transfer of information related to pure sensorimotor tasks.

Figure 1

Experimental design including mRT Task and diffusion tensor imaging. The temporal order of random blocks of finger opposition movements performed with the right and then left hand is shown. For the right hand, nonspecific learning was calculated as the difference in RT between the random blocks R2 and R4 (dotted lines). The amount of nonspecific transfer from the right to the left hand was calculated as the difference in RT between the random blocks R2 and L2 (dashed lines). The subdivision of CC into five subregions (CC1–CC5) is displayed on the pictured brains. RT (response time) and FA (fractional anisotropy) indicate respectively the measures of motor performance and callosal damage in the five callosal subregions connecting the two hemispheres. Right hand is the “Learning Hand” and left hand is the “Transfer Hand”, controlled respectively by the learning and the transfer hemispheres.

Figure 2

PwMS and control subjects performing the RT task with the right and left hand: mean response time. The abscissa shows blocks and performing hand in temporal order; variance is expressed as SE. Nonspecific learning is shown in dotted lines, nonspecific transfer‐hand performance is shown in dashed lines; *P < 0.05, **P < 0.001.

Figure 3

Linear correlation between the amount of nonspecific transfer (Delta_Transfer) and fractional anisotropy in (A) CC1, (B) CC2, (C) CC3, (D) CC4, (E) CC5, and (F) whole CC. Solid line represents the linear fitting. Pearson's correlation coefficient r and P value are reported; as shown, Delta_Transfer correlated with FA only in CC3.

Figure 4

Cortical projections of callosal fibers originating from CC3 obtained by probabilistic tractography (yellow: CC3; blue and light blue: traced fibers), represented on the fractional anisotropy map of a representative patient. (A) the selected callosal ROI, CC3; (B–D) obtained tracts displayed respectively on sagittal, coronal, and axial plane.