Abstract

Cortical reorganization within the primary motor cortex (M1) contralateral to a practicing hand has been extensively investigated. The extent to which the ipsilateral M1 participates in these plastic changes is not known. Here, we evaluated the influence of unilateral hand practice on the organization of the M1 ipsilateral and contralateral to the practicing hand in healthy human subjects. Index finger movements elicited by single-pulse transcranial magnetic stimulation (TMS) delivered to each M1 were evaluated before and after practice of unilateral voluntary index finger abduction motions. Practice increased the proportion and acceleration of TMS-evoked movements in the trained direction and the amplitude of motor-evoked potentials (MEPs) in the abduction agonist first dorsal interosseous (FDI) muscle in the practicing hand and decreased the proportion and acceleration of TMS-evoked abduction movements and MEP amplitudes in the abduction agonist FDI in the opposite resting hand. Our findings indicate that unilateral hand practice specifically weakened the representation of the practiced movement in the ipsilateral M1 to an extent proportional to the strengthening effect in the contralateral M1, a result that varied with the practicing hand's position. These results suggest a more prominent involvement of interacting bilateral motor networks in motor memory formation and probably acquisition of unimanual motor skills than previously thought.

inhibition, ipsilateral M1, motor learning, plasticity, TMS, training
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Introduction

Skill acquisition is accomplished through repetition, which in turn leads to performance improvements (Shadmehr and Mussa-Ivaldi 1994; Nudo, Milliken, et al. 1996; Bays and Wolpert 2007). Encoding of motor memories in the primary motor cortex (M1) may represent one of the steps preliminary to the acquisition of a motor skill (Donchin et al. 2002; Krakauer and Shadmehr 2006). For example, practice of finger movements in a particular direction leaves a short-lasting memory trace in the contralateral M1, as evidenced by an increased probability, at the end of the training period, that transcranial magnetic stimulation (TMS) applied over M1 will elicit movements in the practiced direction (Classen et al. 1998). This cortical reorganization associated with practice (Nudo, Wise, et al. 1996; Classen et al. 1998) is thought to engage long-term potentiation-like mechanisms (Butefisch et al. 2000) that could support learning and memory processes (Rioult-Pedotti et al. 1998; Sawaki et al. 2002).

In addition to changes in the M1 contralateral to a practicing hand, it has been reported that the M1 ipsilateral to a hand performing a novel motor task is active to various degrees (Kawashima et al. 1994; Chen et al. 1997) and that this activity decreases progressively as the task becomes overlearned (Daselaar et al. 2003; Rossini et al. 2003; Bischoff-Grethe et al. 2004). This activation has been interpreted, depending on the context, as a possible epiphenomenon of task complexity (Chen et al. 1997; Hummel et al. 2003; Rossini et al. 2003; Verstynen et al. 2005), as erroneous localization of a predominantly dorsal premotor activation (Hanakawa et al. 2005), or as an active contribution to the learning effort (Grafton et al. 2002).

Besides, previous studies evaluated changes in corticomotor excitability of the ipsilateral M1 during performance of a unilateral motor task by means of TMS and reported both inhibitory (Leocani et al. 2000; Duque, Mazzocchio, et al. 2005; Koch et al. 2006) and facilitatory (Muellbacher et al. 2000; Hortobagyi et al. 2003) effects. A possible explanation for these conflicting results during task performance is that the relative net effect of performing a unilateral hand movement on corticomotor excitability of the other hand varies from inhibitory to facilitatory depending on the behavioral set (Liepert et al. 2001; Sohn et al. 2003; Perez et al. 2007; Perez et al. forthcoming). It remains to be determined whether changes in the organization of M1 ipsilateral to a moving hand, so far identified during unilateral movements, persist after the end of a training period. In other words, it would be useful to determine if unilateral hand training, in addition to encoding a memory trace in the contralateral M1 (Classen et al. 1998), elicits reorganizational changes in the ipsilateral M1 and if so the characteristics or specificity of this form of use-dependent plasticity. Understanding these characteristics could potentially strengthen the design of emerging neurorehabilitative interventions in the clinical arena (Whitall et al. 2000; Wolf et al. 2006).

In summary, the functional details of reorganizational changes in the ipsilateral M1 after motor training are incompletely understood. To address this issue, we utilized an experimental protocol that permits the evaluation of movement kinematics and motor-evoked responses elicited by single-pulse TMS applied over the human M1 (Classen et al. 1998). Our main findings were that unilateral motor practice encodes reciprocal memory traces in both M1s, characterized by strengthening of the representation of the practiced movement in the M1 contralateral to the practicing hand and by reduction of the mirror movement representation in the opposite M1, an effect that varied in magnitude with the practicing hand's position.