Elsevier

Brain Research

Volume 1179, 7 November 2007, Pages 51-60
Brain Research

Research Report
Task-specific changes in motor evoked potentials of lower limb muscles after different training interventions

https://doi.org/10.1016/j.brainres.2007.08.048Get rights and content

Abstract

This study aimed to identify sites and mechanisms of long-term plasticity following lower limb muscle training. Two groups performing either a postural stability maintenance training (SMT) or a ballistic ankle strength training (BST) were compared to a non-training group. The hypothesis was that practicing of a self-initiated voluntary movement would facilitate cortico-spinal projections, while practicing fast automatic adjustments during stabilization of stance would reduce excitatory influence from the primary motor cortex. Training effects were expected to be confined to the practiced task. To test for training specificity, motor evoked potentials (MEP) induced by transcranial magnetic stimulation (TMS) were recorded at rest and during motor tasks that were similar to each training. Intracortical, cortico-spinal, as well as spinal parameters were assessed at rest and during these tasks. The results show high task and training specificity. Training effects were only observable during performance of the trained task. While MEP size was decreased in the SMT group for the trained tasks, MEP recruitment was increased in the BST group in the trained task only. The control group did not show any changes. Background electromyogram levels, M. soleus H-reflex amplitudes and intracortical parameters were unaltered. In summary, it is suggested that the changes of MEP parameters in both training groups, but not in the control group, reflect cortical motor plasticity. While cortico-spinal activation was enhanced in the BST group, SMT may be associated with improved motor control through increased inhibitory trans-cortical effects. Since spinal excitability remained unaltered, changes most likely occur on the supraspinal level.

Introduction

Control of leg movements, such as balance and gait, plays an important role in human everyday life. A great number of empiric training interventions have been developed for rehabilitation purposes and in sports science in order to improve postural control and leg motor performance. The acquisition of motor skills in the first 4 to 6 weeks of training primarily relies on neural plasticity rather than on changes in muscle structure (Enoka, 1997, Komi, 1986, Ploutz et al., 1994). With respect to lesion sites within the central nervous system (e.g. spinal or cortical), it is important to understand whether a particular training preferentially induces plastic changes in spinal or cortical sensory–motor circuits. It is also crucial to know under which conditions this can best be observed.

So far, most studies were focused on acute training-induced effects, exploring just minutes to hours after a training intervention. For such immediate effects, transcranial magnetic stimulation (TMS) studies identified predominantly cortical plasticity such as increased motor cortex excitability and enlargement of motor cortical representation (Classen et al., 1998, Pascual-Leone et al., 1994, Pascual-Leone et al., 1995). Analogous to hand function, gait and postural control are highly adaptable and underlie specific cortical control (Bonnard et al., 2002, Camus et al., 2004, Christensen et al., 2001, Schubert et al., 1999, Taube et al., 2006). Likewise, short-term motor skill training in the leg muscles induces increased motor cortex excitability, which is consistent with findings in the upper limb suggesting a similar underlying principle (Perez et al., 2004).

In contrast to acute adaptation, the effects of long-term execution of specific motor interventions are less well known and only a few electrophysiological studies have addressed this issue so far (Carroll et al., 2002, Jensen et al., 2005, Taube et al., 2007). While functional brain imaging studies have shown that the main focus of activity shifts from cortical towards subcortical motor regions including cerebellar dentate nucleus, thalamus and putamen during the time course of training (Doyon and Benali, 2005, Floyer-Lea and Matthews, 2004, Wu et al., 2004), they did not assess the role of spinal plasticity. Findings from TMS experiments have shown a decrease in cortico-spinal excitability correspondingly. This was a common finding in two studies on strength training of upper limb muscles (Carroll et al., 2002, Jensen et al., 2005). However, the motor conditions under which this was detected were not really comparable. While changes were exclusively reported at rest in one study (Jensen et al., 2005), they were observed only during tonic activation in the other (Carroll et al., 2002). Still another recent study on balance training showed a selective reduction of cortico-spinal excitability only during perturbation of stance, a task resembling the one which was performed during the training (Taube et al., 2007). Thus, apparently the motor condition under which training effects are assessed may be as influential for the result as the training itself. Furthermore, it has been shown that different motor training regimen induce disparate forms of neurophysiologic changes in different anatomic motor areas (Adkins et al., 2006, Jensen et al., 2005).

The goal of this study was to identify sites and mechanisms of long-term plasticity following lower limb muscle training by comparing two different training interventions. Both training regimens are widely used for athletic training and in rehabilitation. They have a similar effect on developing explosive muscle strength (Gruber et al., 2007a, Taube et al., 2007). However, the build-up of rapid force increment (i.e. explosive strength) is attained in different ways. While postural stability maintenance training (SMT) consists of fast automatic movements, leaving no time to consider or prepare the required move, ballistic ankle strength training (BST) strongly emphasizes mental preparation preceding each move to deliberately initiate muscle contraction. It was hypothesized that cortical plasticity is involved in long-term training and that training effects would best be observable in the corresponding active state as training is known to be rather specific for the particular trained task (Voigt et al., 1998). Therefore, cortico-spinal (motor evoked potential (MEP) size and MEP recruitment), intracortical (short intracortical inhibition (SICI) and intracortical facilitation (ICF)) and spinal (M. soleus H-reflex) measures were taken at rest and during motor tasks similar to each type of training. MEP recruitment was expected to be enhanced after BST paralleling the known increase of EMG and force development (Aagaard et al., 2002, Adkins et al., 2006). Cortical excitability was assumed to be reduced after SMT, as shown in a current study (Taube et al., 2007). A control group also underwent testing in order to distinguish training-specific effects from task-induced activation. Better knowledge about specific and generalized effects induced by each type of training may allow goal-oriented application and thereby improve motor outcome.

Section snippets

Background EMG

Amplitudes or force levels for all movements were individually adjusted before training to evoke similar levels and slopes at the first peak of EMG (see Fig. 1). The latency of EMG onset and the first peak of EMG in M. tibialis anterior and M. soleus, representing the point in the time course of movement, at which electrical and magnetic stimulation were applied, were neither different before and after training nor between groups. Motor tasks, in which the muscles were targeted (DFL and PERf

Discussion

The purpose of this study was to assess adaptive changes after long-term training of lower limb muscles. In order to identify the sites and specificity of induced plasticity, two different well-established training regimens were studied. While both trainings are known to increase explosive muscle strength (Gruber et al., 2007a, Gruber et al., 2007b, Taube et al., 2007), the mechanisms were expected to be different. Postural stability maintenance training (SMT, termed sensorimotor training in

Participants

Twenty-seven healthy subjects aged 20–38 years (ten females, seventeen males) participated in this study. Participants gave their informed consent to the experiments, which were approved by the local ethics committee according to the Declaration of Helsinki. Care was taken to screen subjects for any medication usage with potential effects on cortical excitability, history of seizures, neurosurgery, metal implants or injuries affecting the ankle joint. Participants were randomly allocated to one

Acknowledgments

We thank Dr. Franz Aiple, Tom Günther, Florian Pfister and Frank Huethe for technical assistance. This work was supported by the Deutsche Forschungsgemeinschaft (SCHU 1487/1-2).

References (44)

  • J. Doyon et al.

    Reorganization and plasticity in the adult brain during learning of motor skills

    Curr. Opin. Neurobiol.

    (2005)
  • R.M. Enoka

    Neural adaptations with chronic physical activity

    J. Biomech.

    (1997)
  • J. Liepert et al.

    Motor cortex plasticity during constraint-induced movement therapy in stroke patients

    Neurosci. Lett.

    (1998)
  • P. Aagaard et al.

    Increased rate of force development and neural drive of human skeletal muscle following resistance training

    J. Appl. Physiol.

    (2002)
  • D.L. Adkins et al.

    Motor training induces experience-specific patterns of plasticity across motor cortex and spinal cord

    J. Appl. Physiol.

    (2006)
  • C. Bonato et al.

    Cortical output modulation after rapid repetitive movements

    Ital. J. Neurol. Sci.

    (1994)
  • C. Bonato et al.

    Activity-dependent modulation of synaptic transmission in the intact human motor cortex revealed with transcranial magnetic stimulation

    Cereb. Cortex

    (2002)
  • M. Bonnard et al.

    Task-induced modulation of motor evoked potentials in upper-leg muscles during human gait: a TMS study

    Eur. J. Neurosci.

    (2002)
  • C.M. Butefisch et al.

    Enhancing encoding of a motor memory in the primary motor cortex by cortical stimulation

    J. Neurophysiol.

    (2004)
  • M. Camus et al.

    Cognitive tuning of corticospinal excitability during human gait: adaptation to the phase

    Eur. J. Neurosci.

    (2004)
  • T.J. Carroll et al.

    The sites of neural adaptation induced by resistance training in humans

    J. Physiol.

    (2002)
  • R. Chen et al.

    Intracortical inhibition and facilitation in different representations of the human motor cortex

    J. Neurophysiol.

    (1998)
  • L.O.D. Christensen et al.

    Transcranial magnetic stimulation and stretch reflexes in the tibialis anterior muscle during human walking

    J. Physiol. (Lond)

    (2001)
  • J. Classen et al.

    Rapid plasticity of human cortical movement representation induced by practice

    J. Neurophysiol.

    (1998)
  • W.G. Darling et al.

    Variability of motor potentials evoked by transcranial magnetic stimulation depends on muscle activation

    Exp. Brain Res.

    (2006)
  • H. Devanne et al.

    Input–output properties and gain changes in the human corticospinal pathway

    Exp. Brain Res.

    (1997)
  • J. Duchateau et al.

    Isometric or dynamic training: differential effects on mechanical properties of a human muscle

    J. Appl. Physiol.

    (1984)
  • A. Floyer-Lea et al.

    Changing brain networks for visuomotor control with increased movement automaticity

    J. Neurophysiol.

    (2004)
  • M. Gruber et al.

    Differential effects of ballistic versus sensorimotor training on rate of force development and neural activation in humans

    J. Strength Cond. Res.

    (2007)
  • M. Gruber et al.

    Training-specific adaptations of H- and stretch reflexes in human soleus muscle

    J. Mot. Behav.

    (2007)
  • K.M. Jacobs et al.

    Reshaping the cortical motor map by unmasking latent intracortical connections

    Science

    (1991)
  • J.L. Jensen et al.

    Motor skill training and strength training are associated with different plastic changes in the central nervous system

    J. Appl. Physiol.

    (2005)
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