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

Abstract

Hortobágyi T, Richardson SP, Lomarev M, Shamim E, Meunier S, Russman H, Dang N, Hallett M. Chronic low-frequency rTMS of primary motor cortex diminishes exercise training-induced gains in maximal voluntary force in humans. J Appl Physiol 106: 403-411, 2009. First published November 13, 2008 doi:10.1152/japplphysiol.90701.2008Although 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 ϫ 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 [VolϩrTMS, 1 Hz, FDI motor area, 300 pulses/ session, 120% of the resting motor threshold (rMT)]. The third group also exercised and received sham rTMS (VolϩSham). The fourth group received only rTMS (rTMS_only). The 37.5% and 33.3% gains in MVC in Vol and VolϩSham groups, respectively, were greater (P ϭ 0.001) than the 18.9% gain in VolϩrTMS, 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 VolϩrTMS 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. muscle; transcranial magnetic stimulation; cortical excitability IT IS WELL ESTABLISHED that neural mechanisms mediate the initial gains in maximal voluntary strength in response to chronic resistance exercise (9,16,19,20,39). However, there is disagreement concerning the magnitude and nature of involvement of specific structures of the central nervous system in neuronal adaptations to chronic exercise. A handful of studies used transcranial magnetic stimulation (TMS) to determine whether the primary motor cortex (M1) contributes to neuronal adaptations to resistance training-induced increases in voluntary force (9,25,30). Carroll et al. (9) found that resistance training did not modify the size of the TMSproduced motor-evoked potentials (MEPs) at rest, but the force of the first dorsal interosseus muscle (FDI) at which maximum MEP amplitude occurred significantly shifted from ϳ50% maximal voluntary force (maximal voluntary contraction, MVC) before training to ϳ35% MVC after training. Coupled with data produced by transcranial ele...

Changes in Functional Magnetic Resonance Imaging Cortical Activation with Cross Education to an Immobilized Limb

“…The results for the trained limb in the current study suggest that strength training is associated with adaptation at the cortical level and is not restricted to motor cortex alone and may involve both cortical hemispheres. These data add to the ongoing controversy whether motor cortex is included (20) or not (21,26,35) in the neural adaptation to strength training, giving weight to the argument that motor cortex is involved to some extent in such adaptations even if a simple motor skill is used.…”

“…In contrast, Hortobágyi et al (20) showed that repetitive TMS applied to motor cortex during strength training diminished strength gains after the training period, which provides convincing evidence that cortical mechanisms are involved in performance gains with strength training. The tlVIRI data presented here suggest that unilateral handgrip training is associated with an increase in the volume of activation in the trained motor cortex (Fig.…”

Inter- and intra-subject variability of motor cortex plasticity following continuous theta-burst stimulation

“…These studies all report significant MEP suppression at the upper end of the IO curve (150 -170% RMT) following low frequency rTMS (1 Hz) (Gangitano et al 2002;Hortobagyi et al 2009;Muellbacher et al 2000). Pharmacological studies show that both cTBS and 1 Hz rTMS induce NMDA receptor-dependant LTD-like plasticity (Chen et al 1997;Huang et al 2007), albeit via the modulation of different cortical circuits; studies recording descending volleys from the epidural space show that cTBS primarily suppresses the I1 wave (Di Lazzaro et al 2005), while 1 Hz rTMS primarily suppresses late I waves (Hill et al 1996;Makowiecki et al 2014).…”

Neurophysiological Responses After Short-Term Strength Training of the Biceps Brachii Muscle

“…Elevated H-reflexes and V-wave amplitudes have been reported after maximal dynamic and isometric strength training (7,11), suggesting enhanced neural excitability in descending corticospinal tracts. However, adjustments in H-reflex and V-wave amplitude after strength training may arise as a result of changes in the intrinsic properties of Ia afferents, such as presynaptic inhibition, intrinsic motoneuron properties, and changes in motoneuron firing rate (23). A limitation of these techniques is the difficulty in quantifying the site of adaptation (e.g., supraspinal or spinal) because neither technique directly measures the involvement of the primary motor cortex (M1) or corticospinal tract.…”

“…Transcranial magnetic stimulation enables the assessment of corticospinal excitability during voluntary contractions in humans and has recently been used in strength training research (6,13,16,23,26,36). The TMS applied over the M1 can induce a series of descending volleys in the corticospinal tract, which in turn, causes a muscle response referred to as a motor-evoked potential (MEP).…”