Motor cortical plasticity induced by motor learning through mental practice

Abstract

Several investigations suggest that actual and mental actions trigger similar neural substrates. Motor learning via physical practice results in long-term potentiation (LTP)-like plasticity processes, namely potentiation of M1 and a temporary occlusion of additional LTP-like plasticity. However, whether this neuroplasticity process contributes to improve motor performance through mental practice remains to be determined. Here, we tested skill learning-dependent changes in primary motor cortex (M1) excitability and plasticity by means of transcranial magnetic stimulation (TMS) in subjects trained to physically execute or mentally perform a sequence of finger opposition movements. Before and after physical practice and motor-imagery practice, M1 excitability was evaluated by measuring the input-output (IO) curve of motor evoked potentials. M1 LTP and long-term depression (LTD)-like plasticity was assessed with paired-associative stimulation (PAS) of the median nerve and motor cortex using an interstimulus interval of 25 ms (PAS25) or 10 ms (PAS10), respectively. We found that even if after both practice sessions subjects significantly improved their movement speed, M1 excitability and plasticity were differentially influenced by the two practice sessions. First, we observed an increase in the slope of IO curve after physical but not after MI practice. Second, there was a reversal of the PAS25 effect from LTP-like plasticity to LTD-like plasticity following physical and MI practice. Third, LTD-like plasticity (PAS10 protocol) increased after physical practice, whilst it was occluded after MI practice. In conclusion, we demonstrated that MI practice lead to the development of neuroplasticity, as it affected the PAS25- and PAS10- induced plasticity in M1. These results, expanding the current knowledge on how MI training shapes M1 plasticity, might have a potential impact in rehabilitation.

Keywords: cortical plasticity; long term depression; long term potentiation; motor imagery; motor learning.

Figure 1

Experimental protocol. By means of transcranial magnetic stimulation (TMS), we tested the effect of physical practice (physical) and motor imagery practice (imagery) on corticospinal excitability and on Paired associative stimulation (PAS) protocol induced effects. Participants were divided into two groups, each participating in a set of experiments, testing the effect of PAS25 and PAS10 separately. All experiments and sessions of physical practice or motor-imagery (MI) practice were performed in the morning. MEPs, motor evoked potentials; IO, input-output curve.

Figure 2

Behavioral data, showing the rate of execution of sequential finger tapping movements before (pre-test) and after (post-test) the different types of training (physical practice and motor-imagery practice) (panel A). Data of both GROUP_PAS10 (left side) and GROUP_PAS25 (right side) are shown. Vertical bars indicate SE. Panel (B) shows the correlation between individual changes in movement rate induced by motor-imagery (MI) practice and individual scores at the MIQ-R questionnaire. Changes in movement rate (Y-axis) were evaluated as follows:(post-test − pre-test)/post-test × 100) (r = 0.85; p < 0.001).

Figure 3

IO curves measured in the abductor pollicis brevis (APB) muscle, before and after physical practice (A,B) and before and after motor-imagery practice (C,D). Data of both GROUP_PAS25 (A,C) and GROUP_PAS10 (B,D) are shown. Trend lines indicate the linear fit applied to the range from 90% to 130% S1mV above RMT as indicated by the shaded area. The slopes of the IO curves are depicted in the inferior part of each panel (A,D). The slope was estimated from the linear part of the IO curve between 90% and 130% S1mV above RMT. Vertical bars indicate SE. Asterisks indicate the level of significance (* p < 0.05).

Figure 4

PAS effects on MEPs amplitude in different experimental sessions (first session, physical practice and motor-imagery practice). Raw MEPs obtained from two single representative subjects belonging the GROUP_PAS25 and GROUP_PAS10 are shown.

Figure 5

PAS effects on mean MEPs amplitude in different experimental sessions (first session, physical practice and motor-imagery practice) for both GROUP_PAS25 (A) and GROUP_PAS10 (B). Data obtained before and after practice and after PAS protocol administration are shown. Vertical bars indicate SE. Asterisks indicate significant difference between MEPs before PAS and MEPs after PAS when interaction of SESSION * TIME was statistically significant (*p < 0.05; **p < 0.01).