Immediate increases in quadriceps corticomotor excitability during an electromyography biofeedback intervention

https://doi.org/10.1016/j.jelekin.2014.11.007Get rights and content

Abstract

The purpose of the study was to determine the effects of EMG-BF on vastus lateralis corticomotor excitability, measured via motor evoked potential (MEP) amplitudes elicited using Transcranial Magnetic Stimulation (TMS) during a maximal voluntary isometric contraction (MVIC). We also determined the effect of EMG-BF on isometric knee extensor strength. Fifteen healthy participants volunteered for this crossover study with two sessions held one-week apart. Participants were randomly assigned to condition order, during which five intervention MVICs were performed with or without EMG-BF. MEP amplitudes were collected with TMS during five knee extension contractions (5% of MVIC) at baseline and again during intervention MVICs within each session. During the control condition, participants were instructed to perform the same number of MVICs without any EMG-BF. Percent change scores were used to calculate the change in peak-to-peak MEP amplitudes that occurred during EMG-BF and Control MVICs compared to the baseline MEPs. Peak knee extension torque was recorded during MVICs prior to TMS for each condition. EMG-BF produced significantly increased MEP change scores and significantly greater torque than the control condition. The results of the current study suggest that EMG-BF may be a viable clinical method for targeting corticomotor excitability.

Introduction

Biofeedback is a common clinical modality used to provide real-time information regarding a physiological event or series of events that would typically not be perceived by the user (Prinsloo et al., 2014, Mirelman et al., 2011, Wood and Kipp, 2014, Crowell et al., 2010). Surface electromyographic biofeedback (EMG-BF) externally focuses the attention of the user away from the exclusive attempt to contract the intended muscle, and toward an outward cue that represents the underlying muscle activation (Giggins et al., 2013, McNevin et al., 2003). Shifting an individual’s focus away from the muscle contraction itself, toward an external cue, is hypothesized to improve acquisition and retention of motor skills (McNevin et al., 2003, Pascua et al., 2015). One possible explanation for improved muscle function following the use of EMG-BF is the increase in the excitability from descending neural pathways associated with brain centers involved with voluntary muscle activation.

There is not overwhelming evidence that augmenting resistance training with EMG-BF for the purpose of improving muscle activation will benefit strength development in healthy participants (Lepley et al., 2012). The strongest effects for strength development following the augmentation of EMG-BF with therapeutic exercise has been reported in patients with knee osteoarthritis, anterior knee pain, patellofemoral pain and healthy participants (Lepley et al., 2012). EMG-BF may be beneficial for improving strength in patients with knee pathology, as EMG-BF may specifically target the neuromuscular activation deficits that perpetuate muscle weakness in patients with muscle inhibition (Hart et al., 2010). Muscle strength development is predicted by an increase in voluntary quadriceps activation in patients with knee osteoarthritis (Pietrosimone and Saliba, 2012). Previous hypotheses have attributed changes in voluntary quadriceps activation following knee injury to alterations in spinal reflex excitability,(Hopkins and Ingersoll, 2000) yet changes in corticomotor quadriceps excitability have recently been demonstrated following knee joint injury (Pietrosimone et al., 2012a, Pietrosimone et al., in press, Heroux and Tremblay, 2006, On et al., 2004). The majority of interventions developed to increase voluntary activation following knee injury have focused on targeting spinal reflexive pathways and little research has been conducted to target activation of descending corticomotor pathways with disinhibitory interventions (Harkey et al., 2014). While EMG-BF has been found to improve strength in patients with anterior knee pain and osteoarthritis, there is a gap in our understanding of the neuromuscular mechanisms that play a role in how EMG-BF improves strength in specific patient populations. Knowledge of the effect that EMG-BF has on corticomotor excitability pathways would be important for the future development and optimization of treatments that target corticomotor excitability. Furthermore, elucidating a mechanism by which EMG-BF elicits strength gains may help predict specific patients that respond to EMG-BF.

Therefore the purpose of the current study was to determine the effects of EMG-BF on vastus lateralis corticomotor excitability, which was measured via motor evoked potential (MEP) amplitudes elicited with TMS during a maximal voluntary isometric contraction (MVIC) in healthy individuals. Understanding if corticomotor excitability pathways are immediately affected by EMG-BF in healthy participants will provide important evidence needed to target specific patient populations that would benefit most from an EMG-BF intervention. We also determined the effect of EMG-BF on isometric knee extensor strength in healthy individuals. We hypothesized that EMG-BF would increase vastus lateralis corticomotor excitability and knee extensor strength measured during a MVIC compared to a condition during which no EMG-BF was provided and MVICs were performed.

Section snippets

Methods

We employed a crossover study design consisting of two sessions where participants performed one of two interventions including: (1) MVIC with EMG-BF (experimental condition), and (2) MVIC without EMG-BF (control condition) was employed. The two sessions were conducted at the same time of day, seven days apart and the order of conditions was randomized. The randomized condition order was concealed from the investigator, whom was conducting the outcome measures and applying the MVIC

Results

There was strong reliability with the AMT data (ICC2,1 = 0.96, P < 0.001, SEM = 1.98) and means were not statistically different at the beginning of the control (47.67 ± 7.67% 2 T) vs. the EMG-BF sessions (48.07 ± 7.09% 2 T; t14 = −0.74, P = 0.47). The MEP:M ratios data had excellent reliability (ICC2,1 = 0.9, P < 0.001) and means were not statistically different at the beginning of the control (0.096 ± 0.003) vs. the EMG-BF sessions (0.01 ± 0.003) (t14 = −1.83, P = 0.09). The SEM for MEP:M at baseline were 0.0007 for

Discussion

The goal of the current study was to evaluate the immediate effects of EMG-BF applied during an MVIC on vastus lateralis corticomotor excitability and knee extensor strength. Understanding how healthy participants respond to EMG –BF during and MVIC may be an important initial step in developing future intervention strategies to improve muscle activation in patient populations that have altered corticomotor excitability following joint injury (On et al., 2004, Heroux and Tremblay, 2006). The

Conclusion

A single EMG-BF intervention produced immediate increases in motor evoked potentials during an EMG-BF and increases in knee extension torque production compared to knee extension MVICs without EMG-BF. Therefore, EMG-BF may be a viable method for increasing vastus lateralis corticomotor excitability.

Conflicts of interest

The authors involved in this paper do not have any conflicts of interest.

Brian Pietrosimone is an Assistant Professor in the Department of Exercise and Sports Science at the University of North Carolina at Chapel Hill. His research seeks to decrease disability related to knee injury with a focus on maximizing long-term joint health following traumatic joint injury. Much of his previous and current research has evaluated the neuromuscular mechanisms related to disability following lower extremity joint injury.

References (37)

  • Harkey M, Gribble P, Pietrosimone B. Disinhibitory interventions and voluntary quadriceps activation: a systematic...
  • J. Hart et al.

    Quadriceps activation failure following knee injuries: a systematic review

    J Athletic Train

    (2010)
  • M. Heroux et al.

    Corticomotor excitability associated with unilateral knee dysfunction secondary to anterior cruciate ligament injury

    Knee Surg Sports Traumatol Arthrosc

    (2006)
  • J.T. Hopkins et al.

    Arthrogenic muscle inhibition: a limiting factor in joint rehabilitation

    J Sport Rehab

    (2000)
  • J. Hopkins et al.

    Cryotherapy and transcutaneous electric neuromuscular stimulation decrease arthrogenic muscle inhibition of the vastus medialis after knee joint effusion

    J Athletic Train

    (2002)
  • F.J. Keefe et al.

    Electromyographic biofeedback: behavioral treatment of neuromuscular disorders

    J Behav Med

    (1978)
  • M. Kernodle et al.

    Information feedback and the learning multiple-degree-of-freedom activities

    J Motor Behavior

    (1992)
  • A. Lepley et al.

    Effects of electromyographic biofeedback on quadriceps strength: a systematic review

    J Strength Condition Res

    (2012)
  • Cited by (30)

    • Steadiness training improves the quadriceps strength and self-reported outcomes in persistent quadriceps weakness following nine months of anterior cruciate ligament reconstruction and failed conventional physiotherapy

      2022, Clinical Biomechanics
      Citation Excerpt :

      The cortical and corticospinal tracts excitability also may play a role as an underlying mechanism in the torque improvements because persistent quadriceps weakness has been directly associated with abnormal cortical activity (Bodkin et al., 2021; Gabler et al., 2013; Pietrosimone et al., 2013; Pietrosimone et al., 2015a; Sonnery-Cottet et al., 2019), and the excitability of cortical tracts was directly associated with the quadriceps function (Rush et al., 2021), the isometric strength inhibition (Zarzycki et al., 2021), and synchronization of motor units (Semmler, 2002). Finally, visuomotor integration also might help in strength improvements of our patients because the visuomotor information helps to adjust the internal error through the motor system (Gaveau et al., 2018; Lepley et al., 2012; Park et al., 2018; Pietrosimone et al., 2015b). Our study has inherent limitations; unfortunately, we did not have access to EMG data, cortical measurement techniques, and electrostimulation devices for central and peripheral nervous adaptation measurements.

    • Effects of electromyography biofeedback for patients after knee surgery: A systematic review and meta-analysis

      2021, Journal of Biomechanics
      Citation Excerpt :

      It enables the patients to improve muscle strength and voluntary control by converting electrical muscle potentials into meaningful signals in real-time (Frank et al., 2010). EMG-biofeedback can intricately connect the afferent and efferent impulses, and the continuous repetition of the two stimuli can effectively help the functional reconstruction of the patient's cerebral cortex (Pietrosimone et al., 2015; Yu et al., 2015). The combination of passive movement caused by EMG feedback and active movement of patients can strengthen the autonomous contractile ability of skeletal muscles, to improve the ROM and help the gradual recovery of motor function (Eid et al., 2016).

    • Systematic reviews evaluating the effectiveness of motor control exercises in patients with non-specific low back pain do not consider its principles – A review

      2021, Journal of Bodywork and Movement Therapies
      Citation Excerpt :

      For example, it has been shown that deep abdominal muscle training using real-time ultrasound feedback reverses neuronal reorganization and not general walking exercises (Tsao et al., 2010). Other work has shown that feedback is required along with exercises to facilitate cortical changes (Pietrosimone et al., 2015) and an external feedback has been shown to be superior compared to internal feedback (van Vliet and Wulf, 2006) in improving motor performance. The exercise dosage provided was quite heterogeneous.

    • Visuomotor therapy modulates corticospinal excitability in patients following anterior cruciate ligament reconstruction: A randomized crossover trial

      2021, Clinical Biomechanics
      Citation Excerpt :

      Incorporation of visuomotor therapy into personalized post-operative ACLR rehabilitation plans is an important area of future research. This study used a sample size similar to prior research assessing corticospinal excitability modulation of the quadriceps (Pietrosimone et al., 2015b). An increase in quadriceps motor response was observed following a single session of visuomotor therapy with strong effect sizes.

    View all citing articles on Scopus

    Brian Pietrosimone is an Assistant Professor in the Department of Exercise and Sports Science at the University of North Carolina at Chapel Hill. His research seeks to decrease disability related to knee injury with a focus on maximizing long-term joint health following traumatic joint injury. Much of his previous and current research has evaluated the neuromuscular mechanisms related to disability following lower extremity joint injury.

    Michelle McLeod received her bachelor’s degree in Athletic Training from the University of Northern Iowa, a master’s degree in Exercise and Sport Science from the University of North Carolina at Chapel Hill and her PhD in Exercise Science from the University of Toledo. She is currently an Assistant Professor in the Department of Health and Human Performance at the College of Charleston. Her main research interests are neuromuscular consequences of lower extremity injury and the prevention post-traumatic knee joint osteoarthritis.

    David Florea completed his Master of Science in Athletic Training from the University of Toledo in 2013. During his time at the University of Toledo he worked in the Joint Injury and Muscle Activation Laboratory. He earned a Bachelor of Science degree from Bowling Green State University in 2011. He is currently working as an Assistant Athletic Trainer at the United States Naval Academy.

    Phillip Gribble is an Associate Professor in the Division of Athletic Training at the University of Kentucky. His research interests have focused on understanding the neuromuscular consequences of ankle and knee injuries and developing intervention strategies to alleviate the health care burden from these injuries.

    Michael A. Tevald, PT, PhD, is currently an assistant professor of Physical Therapy in the Department of Rehabilitation Sciences at the University of Toledo. His research focuses on neuromuscular function in the elderly and clinical populations.

    View full text