Corticospinal properties following short-term strength training of an intrinsic hand muscle
Introduction
The contributions of the central nervous system (CNS) to improvements in strength are well documented (Duchateau and Enoka, 2002, Duchateau et al., 2006, Folland and Williams, 2007). However, the mechanisms underlying these improvements are less well understood, particularly in the primary motor cortex (M1). While evidence for the muscle morphological changes that occur with strength training are clearly demonstrated through hypertrophy (Folland & Williams, 2007), the neural adaptations induced by strength training may be comprised of more subtle changes (Datta & Stephens, 1990) in many areas including supraspinal centers (Carroll et al., 2002, Farmer et al., 1993), descending neural tracts (Aagaard et al., 2002, Fimland et al., 2009), spinal circuitry (Cannon and Cafarelli, 1987, Del Balso and Cafarelli, 2007, Kamen, 2004), and the motor end plate connections between motoneurons and muscle fibers (Staron, Karapondo, & Kraemer, 1994). Several investigations have reported maximal force increases of up to 15% within days following an exercise session (Berg et al., 1997, Duchateau, 1995, Rogers and Evans, 1993, Schenck and Forward, 1965, Vandenborne et al., 1998, Yue et al., 1997), and up to 200% increase after 8 week, with no changes in the cross-sectional area of muscle (Folland & Williams, 2007). These results imply that the early stages of strength development may be due to some form of neural adaptation.
Although there is a general consensus that the CNS mediates this increase in strength following a period of strength training, there is considerable debate concerning the extent and nature of involvement of specific sites within the CNS. Recently, a number of studies have used transcranial magnetic stimulation (TMS) to determine whether the M1 contributes to strength development, providing a potential site for neural adaptations to strength training (Carroll et al., 2002, Griffin and Cafarelli, 2007, Hortobágyi et al., 2009, Jensen et al., 2005). Given that the M1 is heavily populated with corticospinal cells that descend onto motoneurons located within the spinal cord (Porter, 1985), the use of TMS enables the assessment of corticospinal excitability and inhibition following specific training interventions. For example, Carroll et al. (2002) examined the effect of heavy load (70–85% of MVC) isometric strength training on corticospinal excitability following 4 week strength training of the first dorsal interosseous (FDI) muscle. Although strength training resulted in a 33% increase in strength, the strength training program did not modify the size of the TMS produced motor-evoked potential (MEPs). Carroll et al. (2002) also used transcranial electrical stimulation (TES) to stimulate subcortical structures and concluded that strength training does not affect the organization of the M1, suggesting that adaptations are confined to the spinal cord. Similarly, Jensen et al. (2005) had participants perform heavy load (80% of MVC) dynamic strength training (five sets of six to 10 repetitions) of the biceps brachii three times per week for 4 week. MEP amplitude at 5% of MVC and stimulus–response curves were constructed prior to and after the 4 week training intervention. Following training, muscle strength increased by 31%, however, maximal MEP amplitude produced by TMS at rest was reduced, suggesting a minimal role for the M1 and corticospinal pathway in strength development. In contrast to these findings, Beck et al. (2007) demonstrated increased MEP amplitude produced by TMS following 4 week of ballistic strength training in the soleus muscle, while Griffin and Cafarelli (2007) found a 32% increase in MEP amplitude with no change in peripheral nerve excitability, suggesting that strength training leads to a task-specific adaptation within the corticospinal tract. Therefore, strength training studies using TMS show either increased (Beck et al., 2007, Griffin and Cafarelli, 2007), reduced (Jensen et al., 2005), unchanged (Carroll et al., 2002), or task-specific modulation of corticospinal excitability (Beck et al., 2007).
Although the above mentioned TMS studies have tried to determine the effects of strength training on corticospinal excitability (by measuring MEP amplitude produced by TMS), changes in cortical inhibition may also be an important neural adaptation that contributes to strength development. Cortical inhibition refers to the neural mechanisms by which output from M1 is attenuated by inhibitory γ-aminobutryic acid (GABA) receptor mediated interneuron transmission (McCormick, 1989). Inhibitory neurons located in the M1 use GABA as their neurotransmitter and the activity of these neurons can be investigated with paired pulse or single-pulse TMS (Inghilleri et al., 1993, Jones, 1993, Kujirai et al., 1993). The paired pulse technique measures short interval intracortical inhibition (SICI) that is mediated by GABAA receptors (Kujirai et al., 1993), whereas the single-pulse technique measures inhibition mediated by GABAB (Siebner, Dressnandt, Auer, & Conrad, 1998). Using the paired pulse technique, SICI can be measured and may be important for shaping the output from the M1 (Chen, 2004). For example, SICI is reduced during voluntary muscle contractions and has been proposed to improve corticospinal drive during intended movement by releasing corticospinal cells from inhibition, therefore improving subsequent excitatory drive to produce the desired movement (Floeter & Rothwell, 1999). Using single-pulse TMS, it has been demonstrated that there is a reduction in the duration of the SP during both slow and fast finger movements, illustrating a task dependant change in corticospinal inhibition mediated by GABAB interneuronal transmission (Pearce & Kidgell, in press). Currently, no studies have examined the effect of strength training on cortical inhibition, although changes in inhibition may be important in force production. Studies have demonstrated in M1 that prior to and during movement, there is not only an increase in corticospinal excitability, but also a reduction in corticospinal inhibition (Chen et al., 1998, Reynolds and Ashby, 1999, Ridding et al., 1995). Furthermore, the change in inhibition is specific to the intended agonist muscle, as MEPs in antagonist muscle remain unchanged (Reynolds and Ashby, 1999, Ridding et al., 1995). Therefore, changes in inhibition seem to be selective and act to focus the output from the MI by improving excitatory drive onto corticospinal cells that produce the intended movement (Ridding, Rothwell et al., 1995). In light of this, previous strength training studies that have used TMS have not included the analysis of SP duration, despite several investigations demonstrating changes in inhibition prior to and during movement (Reynolds and Ashby, 1999, Ridding et al., 1995). The novel aspect of the present study was that we investigated whether strength training of the FDI induces changes in corticospinal inhibition (SP duration) as previous TMS strength training studies have not addressed this issue.
The purpose of the present investigation was to extend upon previous work (Carroll et al., 2002, Jensen et al., 2005) by investigating the corticospinal responses, with particular interest on the effect of isometric strength training on the duration of the cortical SP. The specific aim of the investigation was to determine whether isometric strength training of the FDI altered corticospinal excitability and inhibition during moderate muscle activation. In order to investigate whether strength training causes adaptations along the corticospinal pathway, we determined the effect of isometric strength training on the magnitude of MEPs and the duration of the cortical SP produced by TMS at 5% and 20% MVC. It was hypothesized that strength training would increase the amplitude of the MEP, reflecting increased corticospinal excitability, reduce the duration of the cortical SP, reflecting a decrease in corticospinal inhibition and this would result in an increase in MVC force following training.
Section snippets
Participants
Sixteen healthy (24.12 ± 5.21 years, 13 males, and three females), right-handed university students were randomly allocated to either a strength training (seven males, one female) or a control group (six males, two females). All participants were right-handed, as assessed by the Edinburgh handedness inventory (Oldfield, 1971) and had not participated in any kind of strength training in the past 2 years. All participants gave written, informed consent to the experimental procedures, which conformed
Results
All participants in the training group completed all training sessions, and all participants in both groups completed the pre and post testing sessions.
Discussion
In the present study, we aimed to investigate the neural mechanisms contributing to strength development following short-term strength training of the FDI using TMS, observing a significant increase in MVC force in the training group and a reduction in cortical inhibition.
There was a 33.8% increase in MVC force in the trained participants and this increase was comparable to other short-term strength training studies that have exercised intrinsic muscles of the hand (Carroll et al., 2002,
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