Emerging evidence that exercise-induced improvements in muscular strength are partly due to adaptations in the brain

Abstract

When people perform exercise against heavy loads, their capacity to produce force with the relevant muscles increases. It is well established that these improvements in strength are partly because of adaptive changes within the trained muscles, such as increased muscle fibre diameter. However, it has been recognized for some time that central nervous system (CNS) adaptations also contribute to enhanced strength, especially in the early phase of training. The exact form of these CNS changes has been the subject of considerable attention over the last 10 years, because non-invasive methods of probing the connections between the brain and muscles, such as transcranial magnetic stimulation (TMS), have become widely available. Nevertheless, much of the available evidence regarding the neural mechanisms of strength gains obtained from TMS studies is conflicting and difficult to interpret (Carroll et al. 2011). In the current issue of Acta Physiologica, Weier et al. (2012) report a large increase in the size of responses to TMS and associated reductions in the efficacy of inhibitory circuits within the motor cortex. The data add to recent evidence that strength training can induce the adaptation in the motor cortex that contributes to enhanced performance. The main novel aspect of the study by Weier et al. (2012) was the use of a paired-pulse TMS paradigm to assess the responsiveness of intracortical inhibitory interneurons. In this method, a TMS pulse that is subthreshold for eliciting a motor-evoked response (MEP) is used to condition the MEP produced by a subsequent (2-3ms later) test TMS pulse (Kujirai et al. 1993). The first pulse activates GABAergic inhibitory interneurons in the motor cortex (Ilic et al. 2002), which attenuate the excitatory response to the second pulse. The proportional reduction in the test pulse response when compared to control is taken as a measure of short-interval intracortical inhibition (SICI). The observation that SICI was released in the Weier et al. (2012) study implies a reduction in the responsiveness of the intracortical inhibitory interneurons as a consequence of strength training or a reduction in the synaptic efficacy of their synapses. In either case, the results indicate that strength training affects the cortical circuitry, which is an advance on previous studies that measured MEP size alone, because MEP amplitude can be modulated at both cortical and subcortical sites. Moreover, previous evidence on the effect of strength training on MEP size is mixed. In different studies, MEPs have been reported to increase, decrease or remain unchanged [see (Carroll et al. 2011) for review]. The large increase in MEP size reported by Weier et al. is striking and begs speculation as to why it differs from previous results. A likely possibility is that the nature of the training task was more complex that many previous types of training studied with TMS. The task (squat lift) required synergistic activation of multiple multi-articular muscles in a dynamic, multi-joint action and was paced to an external signal. These features may have provided a stimulus for reorganization within the motor cortex that exceeded that provided by previous studies that typically involved relatively constrained, single-joint tasks and thereby resulted in larger changes in the response to TMS. While the results of Weier et al. (2012) indicate that strength training causes adaptations within motor cortex, they do not necessarily imply that the adaptations directly contribute to improved strength. However, Hortobagyi et al. (2009) recently provided evidence for such a causal link, by demonstrating that strength gains were attenuated when the motor cortex was repetitively stimulated to interfere with post-training cortical processing. This type of repetitive TMS protocol has been shown previously to prevent the consolidation of newly acquired motor skill (Muellbacher et al. 2002). Furthermore, Selvanayagam et al. (2011) reported that the direction of mechanical twitches evoked by TMS shifted towards the direction of motion involved in a strength training session, which implies that corticospinal connections that favour the production of force produced during training are reinforced. Taken together, it seems likely that repetitive muscle actions against high loads alter motor cortical connectivity to facilitate the specific patterns of muscle activity required to produce maximal force in the training context. The results of Weier et al. (2012) are based on a relatively small sample and do not identify which additional areas in the CNS, besides the intracortical inhibitory interneurons, contribute to the large increases in MEP size. Nevertheless, they provide additional support for the view that improved strength relies at least partly on adaptations in motor cortex. The important challenge that remains is to characterize the links between specific training characteristics, neural adaptations and functional improvements. There is no conflict of interest to report.