Motorcortical excitability and synaptic plasticity is enhanced in professional musicians

Abstract

Musicians not only have extraordinary motor and sensory skills, but they also have an increased ability to learn new tasks compared with non-musicians. We examined how these features are expressed in neurophysiological parameters of excitability and plasticity in the motor system by comparing the results of 11 professional musicians and 8 age-matched non-musicians. Parameters of motor excitability were assessed using transcranial magnetic stimulation (TMS) to measure motor-evoked potentials (MEPs) together with recruitment of corticospinal projections [input-output curve (IOcurve)] and of short-latency intracortical inhibition (SICIcurve). Plasticity, here defined as change of synaptic effectiveness, was tested by measuring MEPs and IOcurves after paired associative stimulation (PAS), which consists of an electric median nerve stimulus repeatedly paired (200 times at 0.25 Hz) with a TMS pulse over the hand motor area. Using an interstimulus interval of 25 ms (PAS25) or 10 ms (PAS10), this leads to long-term potentiation- or long-term depression-like plasticity, respectively. Musicians showed steeper recruitment of MEPs and SICI (IOcurve and SICIcurve). Additionally, PAS25 increased and PAS10 decreased the MEP amplitudes and the slope of the IOcurves significantly more in musicians than in non-musicians. This is consistent with a wider modification range of synaptic plasticity in musicians. Together with the steeper recruitment of corticospinal excitatory and intracortical inhibitory projections, this suggests that they regulate plasticity and excitability with a higher gain than normal. Because some of these changes depend on age at which instrumental playing commenced and on practice intensity, they may reflect an increase in number and modifiability of synapses within the motor area caused by long-term musical practice.

Figure 1.

Average MEP recordings from the APB of one representative non-musician and one musician. The TMS intensity was adjusted to evoke a baseline MEP with peak-to-peak amplitude of 1 mV in the APB as the main target muscle. After PAS25, the MEP amplitudes were enhanced, and after PAS10, they were reduced in both subjects. However, both effects were much larger in the musician than the non-musician.

Figure 2.

Mean MEP (±SE) in non-musicians and musicians for all three intrinsic hand muscles. Changes after PAS25 (gray) and PAS10 (black) are expressed as a percentage increase/decrease in the baseline MEP. The double-headed arrows show the mean total range of modulation by the PAS interventions. In both groups of subjects, PAS produced the largest effects on MEPs in the median nerve-innervated APB than the other two muscles. But comparing both groups, the effects were greater in musicians than in non-musicians.

Figure 3.

IOcurves in both groups before and after PAS. A–C, The mean MEP amplitude (±SE) as given on the y-axis against the stimulus intensity given on the x-axis (in percentage of SI1mV). A, B, IOcurves measured before and after PAS25 and PAS10, respectively, for non-musicians (A) and for musicians (B). Musicians showed a steeper increase in both of the IOcurves measured before PAS, as well as after PAS25. In both groups, the IOcurves measured before the PAS were not significantly different. C, Pooled IOcurves before PAS for each group separately. The slope of the curve has been calculated for the approximately linear part between 90 and 130% SI1mV and is shown in the inserted column graph for non-musicians (gray) and musicians (black). The mean MEP amplitudes were significantly higher in musicians at stimulus intensities of 110–130% SI1mV (t test, *p ≤ 0.05), as was the slope of the pooled IOcurve (t test, p = 0.01). D, The slopes for all IOcurves as shown in A and B for non-musicians and musicians. Statistical results of direct comparisons of the slopes before and after PAS within the groups as well as of direct comparisons between the groups are shown (t test; *p ≤ 0.05; **p ≤ 0.01). E, The slopes after PAS as a percentage of the slope measured before. Compared with non-musicians, the musicians showed a significantly stronger slope increase after PAS25 and decrease after PAS10 (t test; p values shown).

Figure 4.

The SICI obtained with a conditioning pulse intensity of 70, 80, and 90% aMT is shown as the percentage of MEP evoked by the test pulse alone (±SE). With a conditioning stimulus of 70% aMT, musicians showed less, with 90% aMT more SICI than non-musicians, whereas at 80% aMT the level of SICI was similar in both groups (t test, *p ≤ 0.015). The slope calculated for the SICIcurve described when displaying the amount of SICI against the conditioning stimulus intensity was significantly steeper in musicians (inserted column graph; t test, p = 0.0056).

Figure 5.

Correlation between musicians' performance parameter and measures of motor excitability and plasticity. Filled symbols represent pianists, and open symbols represent other instrumentalists (two brass players, one guitarist, one recorder player). A, B, The correlation between the age at which instrumental playing was commenced (x-axis) and the SICIslope (A) and the IOslope (B) before and after PAS. Musicians who started at a younger age had a steeper SICIslope and also a stronger IOslope increase after PAS25. However, because almost all early starters were pianists, instrument-specific effects cannot be completely excluded. C, The correlation between the practice intensity (hours/day) (x-axis) and the MEP range, showing that musicians who practice more intensively had a significantly higher MEP range, an effect that was unrelated to the instrument played. Pearson's r and the unbroken lines are given for significant correlations.

Figure 6.

Effect of the baseline slope of the IOcurve on the MEP effects of PAS25. The diagram shows hypothetical IOcurves of the two different groups of subjects (gray and black) that differ in slope. In this example, PAS25 causes an equivalent 20% increase in the effectiveness of a TMS stimulus. This leads to a 50% increase in MEP amplitude in the gray group but to a 100% increase in the black group. Thus, if the PAS25 effect was only measured by its effect on MEPs elicited at a single intensity of test stimulus (e.g., a preinterventional SI1mV), the result would suggest that PAS25 is more powerful in the black group than in the gray group. However, the difference may simply reflect a difference in initial IOcurves rather than a difference in synaptic plasticity. A more complete demonstration of increased synaptic plasticity involves showing that PAS increases the slope of the IOcurve (see text).