Mechanisms controlling motor output to a transfer hand after learning a sequential pinch force skill with the opposite hand

Abstract

Objective: Training to perform a serial reaction-time task (procedural motor learning) with one hand results in performance improvements in the untrained as well as in the trained hand, a phenomenon referred to as intermanual transfer. The aim of this study was to investigate the neurophysiological changes associated with intermanual transfer associated with learning to perform an eminently different task involving fine force control within the primary motor cortex (M1). We hypothesized that intermanual transfer of learning such a task would reveal intracortical changes within M1.

Methods: Speed (time to complete each sequence) and accuracy (% of accuracy errors) of motor performance were measured in both hands before and after right (dominant) hand practice. Transcranial magnetic stimulation (TMS) was used to characterize recruitment curves (RC), short intracortical inhibition (SICI), intracortical facilitation (ICF) and interhemispheric inhibition (IHI) from the left to the right M1.

Results: Practice resulted in significant improvements in both speed and accuracy in the right trained hand and in the left untrained hand. RC increased in the left M1, SICI decreased in both M1s, and IHI from the left to the right M1 decreased. No changes were identified in ICF nor in RC in the right M1.

Conclusions: Our results suggest that some neurophysiological mechanisms operating in the M1 controlling performance of an untrained hand may contribute to optimize the procedure for selecting and implementing correct pinch force levels.

Significance: These results raise the hypothesis of a contribution of modulation of SICI and IHI, or an interaction between both to intermanual transfer after learning a sequential pinch force task.

Figure 1. Experimental design

A, Diagram showing the testing procedure. Cortical excitability (TMS) was tested at the beginning of the experiment. Measures of baseline performance for the right (R-pre) and the left (L-pre) hand were taken before the right hand training session (Right hand training, 1, 2, 3, 4, 5, and 6). After the right hand training session, left untrained hand performance was determined (L-post). Motor cortical excitability (TMS) was tested at the end of the experiment. B, Diagram showing the different measures of motor cortical excitability tested bilaterally before and after the right hand training (RC, recruitment curve; SICI, short intracortical inhibition; ICF, intra cortical facilitation; RMT, resting motor threshold and IHI, interhemispheric inhibition tested from the left to the right M1).

Figure 2. Behavioral results

A, Time to perform the sequential pinch force task with the right trained and left untrained hand before (right-pre and left-pre), and after (left hand only, left-post) training with the right hand (1, 2, 3, 4, 5, and 6). The black curve indicates the percentage of errors. Note that the time required to perform the task and the percentage of errors of the left untrained hand decreased significantly after right hand training (left-post compared to left-pre). B, Time to perform the task with the right and left hand “before” (right-pre and left-pre), and “after” (left hand only, left-post) a no-training period (No-training). Note the comparable times to perform the task and percentage of errors in the absence of training (left-pre compared to left-post).

Figure 3. MEP recruitment curves

A, B, MEP amplitudes from FDI muscles (A, B) before (Pre) and after (Post) training. The abscissa shows the TMS stimulus intensity relative to the RMT in each subject, and the ordinate shows MEP amplitudes (mV). Note the increase in recruitment curve in the right FDI in the absence of changes in the left FDI.

Figure 4. Short intracortical inhibition

SICI (3ms) in FDI (A, B) measured before (Pre) and after (Post) training with the right hand in the left (A) and right (B) hemisphere. Note the presence of disinhibition in both left (A) and right (B) hemispheres. ICF (10ms) in FDI (C, D) measured before (Pre) and after (Post) training with the right hand in the left (C) and right (D) hemisphere.

Figure 5. Interhemispheric inhibition

A, Amplitude of the test (TS) and conditioned (CS+TS) MEP before (pre) and after (post) training with the right hand as recorded from left FDI muscle (untrained hand). Note the comparable test MEP amplitudes before and after training (TS pre and TS post). B, Note that training led to a significant decrease in IHI.

Figure 6. Right and left hand EMG activity

EMG activity recorded in the right (upper trace) and left (lower trace) FDI's while a subject was performing the training task with the right hand. Note that while the level of EMG activity for the training hand (right) is well modulated according to the level of force required to reach the different target locations (indicated by 1, 2, 3, 4, and 5), the level of EMG activity of the resting hand (left) remains at rest.