Motor learning and cross-limb transfer rely upon distinct neural adaptation processes

Abstract

Performance benefits conferred in the untrained limb after unilateral motor practice are termed cross-limb transfer. Although the effect is robust, the neural mechanisms remain incompletely understood. In this study we used noninvasive brain stimulation to reveal that the neural adaptations that mediate motor learning in the trained limb are distinct from those that underlie cross-limb transfer to the opposite limb. Thirty-six participants practiced a ballistic motor task with their right index finger (150 trials), followed by intermittent theta-burst stimulation (iTBS) applied to the trained (contralateral) primary motor cortex (cM1 group), the untrained (ipsilateral) M1 (iM1 group), or the vertex (sham group). After stimulation, another 150 training trials were undertaken. Motor performance and corticospinal excitability were assessed before motor training, pre-and post-iTBS, and after the second training bout. For all groups, training significantly increased performance and excitability of the trained hand, and performance, but not excitability, of the untrained hand, indicating transfer at the level of task performance. The typical facilitatory effect of iTBS on MEPs was reversed for cM1, suggesting homeostatic metaplasticity, and prior performance gains in the trained hand were degraded, suggesting that iTBS interfered with learning. In stark contrast, iM1 iTBS facilitated both performance and excitability for the untrained hand. Importantly, the effects of cM1 and iM1 iTBS on behavior were exclusive to the hand contralateral to stimulation, suggesting that adaptations within the untrained M1 contribute to crosslimb transfer. However, the neural processes that mediate learning in the trained hemisphere vs. transfer in the untrained hemisphere appear distinct. ballistic motor learning; interlimb transfer; noninvasive brain stimulation; corticospinal excitability; motor performance

Motor cortical circuits contribute to crossed facilitation of trunk muscles induced by rhythmic arm movement

“…Our findings are also in agreement with evidence showing that a single session of repetitive upper-limb movements (e.g. wrist flexion) can induce acute neural plasticity in corticospinal tract projections to the contralateral, relaxed muscle 13,31,32 . We suggest that it is possible to induce short-term plasticity in the corticospinal projections to the trunk muscles by the use of upper limbs.…”

“…This result is consistent with several lines of evidence suggesting that intracortical circuits contribute to the neural adaptations within the relaxed, untrained muscle 30 , 33 . The finding is also in keeping with previous studies showing that using repetitive TMS over the M1 contralateral to the untrained muscle can modulate the effect of cross-transfer gained in the untrained muscle 10 , 32 , highlighting motor cortical involvement in the cross-transfer effect observed in the untrained muscle. Corticospinal neurons arising within the M1 project to arm muscles through dorsolateral column of the spinal cord 34 , 35 .…”

“…Its aftereffects are polarity-specific, with anodal and cathodal tDCS inducing facilitatory and inhibitory effects on the stimulated cortical region, respectively. Studies using rTMS or tDCS over the untrained M1 have shown modulation of the cross-transfer effect in the untrained muscle 10,32 . Evidence has also shown reduced interhemispheric inhibition from the trained M1to the untrained M1, together with decreased intracortical inhibition in the untrained M1 after the unilateral strength training 15 , suggesting the contribution of transcallosal inhibition to the cross-transfer effect.…”

The use of transcranial magnetic stimulation to evaluate cortical excitability of lower limb musculature: Challenges and opportunities

“…During LE TMS targeting one leg, these bilateral MEP responses are observed often, but rarely systematically documented (Ackermann, Scholz, Koehler, & Dichgans, 1991; Smith et al, 2017). Proximity of the left and right M1 representations for LE muscles may impose a challenge to the study of neural processes mediating cross-limb transfer of training- or neuromodulation-related plasticity (Ruddy & Carson, 2013; Stockel, Carroll, Summers, & Hinder, 2016), and neural mechanisms of bilateral LE training (Hinder, Carroll, & Summers, 2013). …”

A robot-aided visuomotor wrist training induces gains in proprioceptive and movement accuracy in the contralateral wrist

“…Numerous studies established the notion of interlimb transfer of motor learning 12 – 15 . That is to say, the untrained contralateral limb exhibits signs of motor learning without practice.…”