Chronic low-frequency rTMS of primary motor cortex diminishes exercise training-induced gains in maximal voluntary force in humans

Abstract

Although there is consensus that the central nervous system mediates the increases in maximal voluntary force (maximal voluntary contraction, MVC) produced by resistance exercise, the involvement of the primary motor cortex (M1) in these processes remains controversial. We hypothesized that 1-Hz repetitive transcranial magnetic stimulation (rTMS) of M1 during resistance training would diminish strength gains. Forty subjects were divided equally into five groups. Subjects voluntarily (Vol) abducted the first dorsal interosseus (FDI) (5 bouts x 10 repetitions, 10 sessions, 4 wk) at 70-80% MVC. Another group also exercised but in the 1-min-long interbout rest intervals they received rTMS [Vol+rTMS, 1 Hz, FDI motor area, 300 pulses/session, 120% of the resting motor threshold (rMT)]. The third group also exercised and received sham rTMS (Vol+Sham). The fourth group received only rTMS (rTMS_only). The 37.5% and 33.3% gains in MVC in Vol and Vol+Sham groups, respectively, were greater (P = 0.001) than the 18.9% gain in Vol+rTMS, 1.9% in rTMS_only, and 2.6% in unexercised control subjects who received no stimulation. Acutely, within sessions 5 and 10, single-pulse TMS revealed that motor-evoked potential size and recruitment curve slopes were reduced in Vol+rTMS and rTMS_only groups and accumulated to chronic reductions by session 10. There were no changes in rMT, maximum compound action potential amplitude (M(max)), and peripherally evoked twitch forces in the trained FDI and the untrained abductor digiti minimi. Although contributions from spinal sources cannot be excluded, the data suggest that M1 may play a role in mediating neural adaptations to strength training.

Fig. 1.

Chronic effects: % change in maximal voluntary force (maximal voluntary contraction, MVC)of the right first dorsal interosseus (FDI) after 500 MVCs at 70–80% intensity over 10 sessions. Vol, voluntary training; Vol+Sham, voluntary training combined with sham transcranial magnetic stimulation (TMS) at 1 Hz; Vol+rTMS, voluntary training combined with repetitive TMS (rTMS) at 1 Hz; rTMS_only, rTMS at 1 Hz only. Values are means ± SE. *rTMS_only and control significantly different from Vol, Vol+Sham, and Vol+rTMS, P < 0.05; †significantly different from all other groups, P < 0.05.

Fig. 2.

Acute effects of 4 interventions on the size of motor-evoked potentials (MEPs) in session 1, session 5, and session 10. The interventions were voluntary strength training of the right FDI (Vol), voluntary strength training combined with sham rTMS at 1 Hz (Vol+Sham), voluntary strength training combined with 1 Hz rTMS (Vol+rTMS), and rTMS only without strength training (rTMS_only). •, Data collected before an intervention; ○, data collected immediately after the completion of an intervention within a given session. x-Axis: TMS stimulation intensity normalized to the individual MEP threshold determined before a given intervention in session 1. y-Axis: MEP amplitude (means ± SE) normalized to individual maximum action potential amplitude (M_max) established before a given intervention in each session. There were no changes in the control group, and these data are not shown. *P < 0.05 based on Tukey's post hoc contrast. These data compare the acute effects of a particular intervention within a session.

Fig. 3.

Chronic effects of 4 interventions on size of MEPs in session 1 (black circles), session 5 (white circles), and session 10 (gray circles). Interventions were voluntary strength training of the right FDI (Vol), voluntary strength training combined with sham rTMS at 1 Hz (Vol+Sham), voluntary strength training combined with 1 Hz rTMS (Vol+rTMS), and rTMS only without strength training (rTMS_only). x-Axis, TMS stimulation intensity normalized to the individual MEP threshold determined before a given intervention in session 1. y-Axis, MEP amplitude (mean ± SE) normalized to individual M_max established before a given intervention in each session. There were no changes in the control group, and these data are not shown. *P < 0.05 based on Tukey's post hoc contrast relative to sessions 1 and 5. These data compare the chronic effects of a particular intervention across sessions 1, 5, and 10.