• Users Online: 398
  • Print this page
  • Email this page

 
Table of Contents
ORIGINAL ARTICLE
Year : 2020  |  Volume : 63  |  Issue : 2  |  Page : 85-89

Muscle activation and intermuscular coherence during forward and backward pedaling


1 Department of Physical Therapy and Assistive Technology, National Yang-Ming University, Taipei, Taiwan
2 Department of Physical Medicine and Rehabilitation, Taipei Veterans General Hospital, Taipei, Taiwan
3 Department of Sports Medicine, China Medical University, Taichung, Taiwan
4 Department of Physical Therapy, Fooyin University, Kaohsiung, Taiwan
5 Department of Physical Therapy and Assistive Technology, National Yang-Ming University; Preventive Medicine Research Center, National Yang-Ming University, Taipei, Taiwan

Date of Submission22-Oct-2019
Date of Acceptance25-Feb-2020
Date of Web Publication27-Apr-2020

Correspondence Address:
Dr. Yea-Ru Yang
Department of Physical Therapy and Assistive Technology, National Yang-Ming University, 155, Section 2, Linong Street, Beitou, Taipei 11221
Taiwan
Login to access the Email id

Source of Support: This study was financially supported by the Ministry of Science and Technology (MOST 105.2314.B.010.059.MY2)., Conflict of Interest: None


DOI: 10.4103/CJP.CJP_82_19

Rights and Permissions
  Abstract 

The purpose of this study was to investigate muscle activity and intermuscular coherence of the rectus femoris (RF) and biceps femoris (BF) during forward (FW) and backward (BW) pedaling. Sixteen healthy volunteers performed FW and BW pedaling in 30, 45, and 60 revolutions per minute (RPM), while electromyographic (EMG) signals of the RF and BF were recorded bilaterally to determine integral EMG and intermuscular coherence. BW pedaling showed a statistically significant larger EMG activity on the left BF (P = 0.023) in 30 RPM; on the left BF (P = 0.01), right BF (P = 0.05), and right RF (P = 0.006) in 45 RPM, and on the left BF (P = 0.014) and right RF (P = 0.011) in 60 RPM than FW pedaling. In 45 RPM, higher coherence was demonstrated on the left leg (P = 0.011) during the left flexor and right extensor phases and on the right leg (P = 0.043) during the right flexor and left extensor phases in BW compared with FW pedaling. In 60 RPM, higher coherence was observed on both legs (left, P = 0.037; right, P < 0.001) during the left flexor and right extensor phases in BW compared with FW pedaling. Our results suggest that BW pedaling increased the muscle activity of both biarticular muscles and intermuscular coherence.

Keywords: Backward pedaling, electromyography, intermuscular coherence, knee extensors, knee flexors


How to cite this article:
Lee MY, Wang RY, Hsu SS, Yang WW, Chen SS, Yang YR. Muscle activation and intermuscular coherence during forward and backward pedaling. Chin J Physiol 2020;63:85-9

How to cite this URL:
Lee MY, Wang RY, Hsu SS, Yang WW, Chen SS, Yang YR. Muscle activation and intermuscular coherence during forward and backward pedaling. Chin J Physiol [serial online] 2020 [cited 2020 May 29];63:85-9. Available from: http://www.cjphysiology.org/text.asp?2020/63/2/85/283349


  Introduction Top


Pedaling is one of the exercises to promote overall physical health in healthy adults.[1] Furthermore, it is one of the rehabilitation programs to improve the ambulatory function in individuals with neurological diseases.[2],[3],[4] During pedaling, quadriceps, hamstrings, gluteus maximus, tibialis anterior, gastrocnemius, and soleus are activated to generate power.[5] Among these muscles, both quadriceps and hamstrings are the major contributors to articular loading at the knee during normal gait.[6] The strength of the knee extensors is one of the important factors for decline in walking speed in healthy adults.[7] A significant correlation between strength of the knee flexors and extensors and gait performance has been reported in individuals with stroke.[8] Furthermore, muscle activity of the rectus femoris (RF) and biceps femoris (BF) has been shown to correlate with balance performance in people with stroke.[9] The current study, therefore, focused on biarticular muscles, the RF and BF, to investigate their role in pedaling.

Both forward (FW) and backward (BW) pedaling have been suggested to be used as a rehabilitation tool. Potential differences in neuromuscular demands have been demonstrated while pedaling in the FW and BW directions.[10],[11],[12] Previous studies have shown a phase shift of muscle activity in biarticular muscles, the RF and BF, between FW and BW pedaling, and no change in the phasing of uniarticular muscles.[10],[12] These results suggested that the RF and BF are directionally sensitive and those muscles with no change in phasing are directionally insensitive.[11],[12] RF exhibited a major muscle activity during the transition from flexion to extension in FW pedaling and during the transition from extension to flexion in BW pedaling.[11],[12] BF showed a major muscle activity during the transition from extension to flexion in FW pedaling and during the transition from flexion to extension in BW pedaling.[11],[12] The phase shift of muscle activity of the RF and BF is reasonable because these two muscles contribute to specific biomechanical function in order to move crank smoothly.

With regard to the comparison of muscle activity between the FW and BW pedaling, the research evidence is limited. Bressel et al. quantified the amplitude of muscle activity for each half-cycle ( first 180° and second 180° of crank angle).[10] Their results showed that the amplitude of the RF significantly increased in the first half-cycle and significantly decreased in the second half-cycle during BW pedaling compared to FW pedaling.[10] The amplitude of the BF during BW pedaling showed smaller activity in the first half-cycle and greater activity in the second half-cycle compared to FW pedaling.[10] These results regarding the change of amplitude for the RF and BF in the first and second half-cycles were consistent with the phase shift of muscle activity in the biarticular muscles during BW pedaling.[10] Another study found that the amplitude of muscle activity of the BF significantly decreased during BW pedaling compared with FW pedaling.[12] Muscle activity of the RF exhibited no change during BW pedaling compared with FW pedaling.[12] It cannot find a conclusion for the comparison of muscle activity between the two pedaling directions according to those previous limited results.

In addition to the muscle activation pattern and amplitude of muscle activity, muscle coordination is essential for performing motor tasks. A means to understand muscle coordination is to measure intermuscular coherence. Coherence is a measure of correlation between two signals in the frequency domain. Intermuscular coherence has been shown to characterize correlated muscles by sharing a common neural drive.[13],[14] While executing functional tasks, proper coordination of task-relevant muscles including agonists and antagonists would be crucial. Intermuscular coherence could reflect mechanisms that solve synergistic muscle coordination. Previous studies have reported that significant intermuscular coherence was observed during the precision grip task, pinch task, or ankle dorsiflexion task.[14],[15] As for the pedaling task, De Marchis et al. found the presence of intermuscular coherence only for the synergistic muscles acting on knee extension but not for the nonsynergistic muscles during FW pedaling.[16] The function of this synergy is related to power production and crank propelling during the pedaling cycle.[16] To date, no study compared intermuscular coherence between FW and BW pedaling. Therefore, the purpose of the present study was to compare muscle activity and intermuscular coherence of the RF and BF between FW and BW pedaling.


  Materials and Methods Top


Participants

Participants were recruited from the Taipei City. They had to satisfy the following criteria:(1) age between 20 and 75 years;(2) ability to perform pedaling at least 60 min, and (3) free from any neurological disease or lower limb injury. Sixteen healthy volunteers (seven males) with an average age of 46.5 years (standard deviation [SD]: 16.0) participated in the study. The right leg of all participants was the dominant leg. All participants provided written informed consent prior to the study. The experimental procedures were approved by the Institutional Review Board, Taipei Veterans General Hospital (approval number 2015-11-003C and approval date: January 21, 2016) and were performed according to the ethical standards laid down in the Declaration of Helsinki.

Experimental procedure

This study was cross-sectional in nature. Before pedaling, maximal voluntary isometric contractions (MVICs) of bilateral RF and BF were measured using surface electromyography (EMG). The measurements were taken in the supine position for the RF and in the prone position for the BF.[17] MVIC of each muscle was measured for 5 s in three trials. The highest EMG value from the three trials of each muscle was averaged and used for data normalization.

The participants performed FW and BW pedaling in the same day. The order of FW pedaling and BW pedaling was counterbalanced across the participants. A 5 to 10-min warm-up and cool-down of stretching exercise was performed before and after pedaling, respectively. The Rehabilitation Recumbent Bike (MR100, Dyaco International Inc., Taipei, Taiwan) was used for pedaling in the present study. Seat height of the bike was adjusted by keeping the knee to be bent slightly when the foot was at the lowest point while pedaling. The isokinetic program was used to provide accommodating resistance for maintaining a constant cadence. For both FW and BW pedaling, three trials of 60-s duration in the desired rate of 30, 45, or 60 revolutions per minute (RPM) with a 1-min recovery period between trials were performed. The testing order of the three pedaling rates was administered in a random manner. The EMG signals were recorded during pedaling. Middle 40-s EMG signals of each pedaling trial were captured and used for integral EMG (iEMG) and intermuscular coherence analysis. All participants were tested by the same researcher on the three trials for both FW and BW pedaling. This researcher also administered the EMG measures and analysis.

Electromyography recording and analysis

In order to capture EMG signals, the skin was first shaved and prepped with alcohol swabs to reduce skin impedance. Ag/AgCl bipolar surface EMG sensors with 10 mm diameter (Brain Products GmbH, Munich, Germany) were placed on the motor points of bilateral RF and BF according to the suggestion by Perotto.[18] EMG signals were recorded using the QuickAmp amplifier and BrainVision Recorder software (Brain Products GmbH, Munich, Germany). EMG data were exported to MATLAB (MathWorks Inc., Natick, MA, USA) for data analysis. The raw EMG signals were sampled at a rate of 1000 Hz, band pass filtered between 40 and 400 Hz, and processed using a full-wave rectification. A Butterworth low-pass filter with 6 Hz cutoff frequency was used to create a linear envelope EMG. The iEMG was calculated.

Intermuscular coherence analysis

The EMG data were offline processed using BrainVision Analyzer software 2.1 (Brain Products GmbH, Munich, Germany). EMG signals of five consecutive crank revolutions during each pedaling trial were used for intermuscular coherence analysis. The fast Fourier transforms were computed. Phase-controlled functional group analysis was used to divide pedaling into two functional phases.[11],[19] During FW pedaling, the extensor (from flexion to extension) and flexor (from extension to flexion) regions were defined from 0° to 180° and 180° to 360°, respectively. During BW pedaling, the flexor (from extension to flexion) and extensor (from flexion to extension) regions were defined from 0° to 180° and 180° to 360°, respectively. The cross-spectra of EMG and EMG were calculated using the coherence analysis in the BrainVision Analyzer software 2.1 (Brain Products GmbH, Munich, Germany). Coherence is a frequency-domain extension of correlation coefficient and is bounded between 0 and 1 for each frequency of interest. A value of 1 represents a perfect temporal correlation, whereas 0 represents no correlation.[20] Intermuscular coherence between the RF and BF (RF-BF) was analyzed.

Statistical analysis

Statistical analyses were performed using the Statistical Package for Social Sciences 20.0 software (SPSS Inc., Chicago, IL, USA). Descriptive statistics were generated for all variables, and distributions of variables were expressed as mean ± SD. Two-way repeated-measures analysis of variance with two levels of condition (FW and BW) and four levels of muscle (left RF, left BF, right RF, and right BF) was used. When an effect of condition was detected, post hoc Tukey's test was applied. Statistical significance was set at P ≤ 0.05.


  Results Top


A total of 16 healthy individuals were recruited and included in the analyses examining EMG and intermuscular coherence during FW and BW pedaling. The dominant leg of all participants was the right leg. Analysis of variance showed that BW pedaling demonstrated a statistically significant larger EMG activity on the left BF (P = 0.023) in 30 RPM [Figure 1]a, on the left BF (P = 0.01), right BF (P = 0.05), and right RF (P = 0.006) in 45 RPM [Figure 1]b; and on the left BF (P = 0.014) and right RF (P = 0.011) in 60 RPM [Figure 1]c, compared with FW pedaling.
Figure 1: Normalized integral electromyography of the left (L) and right (R) rectus femoris (RF) and biceps femoris (BF) during forward (four bars on the left) and backward pedaling (four bars on the right) in 30 revolutions per minute (a), 45 revolutions per minute (b), and 60 revolutions per minute (c). The data of forward and backward pedaling are presented in the white and gray histograms, respectively. *P < 0.05

Click here to view


Analysis of variance showed that BW pedaling demonstrated a statistically significant higher RF-BF beta-band coherence on the left leg (P = 0.011) during the left flexor and right extensor phases and on the right leg (P = 0.043) during the right flexor and left extensor phases in 45 RPM compared to FW pedaling [Figure 2]b. BW pedaling also showed a statistically significantly higher RF-BF beta-band coherence on both legs (left, P = 0.037; right, P < 0.001) during the left flexor and right extensor phases in 60 RPM compared to FW pedaling [Figure 2]c. However, there was no significant difference in RF-BF beta-band coherence in any phase between FW and BW pedaling in 30 RPM [Figure 2]a.
Figure 2: Beta-band intermuscular coherence between the rectus femoris and biceps femoris in 30 revolutions per minute (a), 45 revolutions per minute (b), and 60 revolutions per minute (c) during forward (FW) and backward (BW) pedaling. *P < 0.05

Click here to view



  Discussion Top


Our results suggest that BW pedaling in 30, 45, and 60 RPM exhibited a greater amplitude of muscle activity in biarticular muscles, the RF and BF, compared with FW pedaling. Little previous study investigates the total amplitude of muscle activity during pedaling. From the training point of view, it is important to understand the total amplitude of muscle activity during pedaling for choosing an appropriate training program. Ting et al. measured the total iEMG during FW and BW pedaling in near 60 RPM among young healthy adults.[12] Their results showed a decreased iEMG of the BF and no change iEMG of the RF during BW pedaling.[12] However, they reported a large variability across participants in muscle activity of the BF during BW pedaling.[12] The conflicting results between the results of study by Ting et al. and those of the current study could be explained by a difference in the age of participants and the pedaling protocol (constant cadence or constant frictional workload). Similar to our finding, Schindler-Ivens et al. recruited middle-aged healthy participants and found that total EMG of the RF and BF increased during BW compared with FW pedaling in 39 RPM.[21] These results suggest that BW pedaling may be more applicable to enhance muscle activation of the biarticular muscles than FW pedaling in middle-aged adults. Moreover, BW pedaling seems causing a greater muscle activity of the knee flexors and extensors than FW pedaling, especially pedaling in 45 RPM.

Pedaling rate has been suggested to be one of the important factors that affects cycling performance.[22] Previous studies have demonstrated increased muscle activity on various lower limb muscles as the pedaling rate increased.[19],[23] However, muscle activity level for the RF and BF showed no significant cadence effect, especially the pedaling rate lower than 60 RPM.[19],[23] Consistently, our observations of muscle activity for the RF and BF among the pedaling rate with 30, 45, and 60 RPM also showed no significant cadence effect.

This is the first study to compare intermuscular coherence between FW and BW pedaling. Our finding regarding intermuscular coherence is that higher RF-BF beta-band coherence presented on both legs during BW pedaling in 45 and 60 RPM compared to those during FW pedaling. Beta-band intermuscular coherence has been indicated to be a reflection for binding of synergistically activated muscles.[24] It has been suggested that synergistically activated muscles bind into a functional synergy and share beta-band cortical drive.[25],[26] Beta-band intermuscular coherence was dependent on supraspinal control and reduced or disappeared after a stroke or complete spinal cord injury.[27],[28],[29] Our results show that the direction-dependent differences presented during both pedaling functional phases while pedaling in 45 RPM. BW pedaling exhibited a greater RF-BF beta-band coherence on the flexor side of both functional phases than FW pedaling. However, the direction-dependent differences in RF-BF beta-band coherence presented during the left flexor and right extensor phases only while pedaling in 60 RPM. Taken our observations from the amplitude of muscle activity and intermuscular coherence together, BW pedaling in 45 RPM would not only increase muscle activation of the majority of measured muscles but also enhance intermuscular coherence during both pedaling functional phases. Therefore, it seems to be an appropriate training for neurologically impaired individuals.

Some limitations of the present study should be noticed. First, the sample size is small. The small sample limits generalizability to the population. Second, the intermuscular coherence was measured only in biarticular muscles around the knee joint. Synergistic muscles around ankle joints should be further studied.


  Conclusion Top


The current study compared muscle activity and intermuscular coherence of biarticular muscles, the RF and BF, during FW and BW pedaling in 30, 45, and 60 RPM. The results of this study suggest that BW pedaling may be the better way to enhance muscle activity and intermuscular coherence, especially pedaling in 45 RPM.

Acknowledgments

This work was supported partly by the Ministry of Science and Technology (MOST 105-2314-B-010-059-MY2). The authors would like to acknowledge the Rehabilitation Recumbent Bike (MR100, Dyaco Inc., Taiwan) for partly supporting the cycling equipment.

Financial support and sponsorship

This study was financially supported by the Ministry of Science and Technology (MOST 105-2314-B-010-059-MY2).

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Bouaziz W, Schmitt E, Kaltenbach G, Geny B, Vogel T. Health benefits of cycle ergometer training for older adults over 70: A review. Eur Rev Aging Phys Act 2015;12:8.  Back to cited text no. 1
    
2.
Kautz SA, Duncan PW, Perera S, Neptune RR, Studenski SA. Coordination of hemiparetic locomotion after stroke rehabilitation. Neurorehabil Neural Repair 2005;19:250-8.  Back to cited text no. 2
    
3.
Tang A, Sibley KM, Thomas SG, Bayley MT, Richardson D, McIlroy WE, et al. Effects of an aerobic exercise program on aerobic capacity, spatiotemporal gait parameters, and functional capacity in subacute stroke. Neurorehabil Neural Repair 2009;23:398-406.  Back to cited text no. 3
    
4.
Nadeau A, Lungu O, Duchesne C, Robillard MÈ, Bore A, Bobeuf F, et al. A 12-week cycling training regimen improves gait and executive functions concomitantly in people with Parkinson's disease. Front Hum Neurosci 2016;10:690.  Back to cited text no. 4
    
5.
Hug F, Dorel S. Electromyographic analysis of pedaling: A review. J Electromyogr Kinesiol 2009;19:182-98.  Back to cited text no. 5
    
6.
Winby CR, Lloyd DG, Besier TF, Kirk TB. Muscle and external load contribution to knee joint contact loads during normal gait. J Biomech 2009;42:2294-300.  Back to cited text no. 6
    
7.
Ko SU, Stenholm S, Metter EJ, Ferrucci L. Age-associated gait patterns and the role of lower extremity strength – Results from the Baltimore Longitudinal Study of Aging. Arch Gerontol Geriatr 2012;55:474-9.  Back to cited text no. 7
    
8.
Flansbjer UB, Downham D, Lexell J. Knee muscle strength, gait performance, and perceived participation after stroke. Arch Phys Med Rehabil 2006;87:974-80.  Back to cited text no. 8
    
9.
Jiang L, Dou ZL, Wen HM, Lan Y, Qiu WH, Li K, et al. Relationship between the changes of surface electromyographic signal of thigh muscle and balance function in stroke patients. Zhonghua Yi Xue Za Zhi 2010;90:917-20.  Back to cited text no. 9
    
10.
Bressel E, Heise GD, Bachman G. A neuromuscular and metabolic comparison between forward and reverse pedaling. J Appl Biomech 1998;14:401-11.  Back to cited text no. 10
    
11.
Raasch CC, Zajac FE. Locomotor strategy for pedaling: Muscle groups and biomechanical functions. J Neurophysiol 1999;82:515-25.  Back to cited text no. 11
    
12.
Ting LH, Kautz SA, Brown DA, Zajac FE. Phase reversal of biomechanical functions and muscle activity in backward pedaling. J Neurophysiol 1999;81:544-51.  Back to cited text no. 12
    
13.
Farmer SF. Rhythmicity, synchronization and binding in human and primate motor systems. J Physiol 1998;509(Pt 1):3-14.  Back to cited text no. 13
    
14.
Laine CM, Valero-Cuevas FJ. Intermuscular coherence reflects functional coordination. J Neurophysiol 2017;118:1775-83.  Back to cited text no. 14
    
15.
Fisher KM, Zaaimi B, Williams TL, Baker SN, Baker MR. Beta-band intermuscular coherence: A novel biomarker of upper motor neuron dysfunction in motor neuron disease. Brain 2012;135:2849-64.  Back to cited text no. 15
    
16.
De Marchis C, Severini G, Castronovo AM, Schmid M, Conforto S. Intermuscular coherence contributions in synergistic muscles during pedaling. Exp Brain Res 2015;233:1907-19.  Back to cited text no. 16
    
17.
Konrad P. The ABC of EMG: A Practical Introduction to Kinesiological Electromyography Version 1. 4th ed. Arizona: Noraxon U.S.A. Inc.; 2006.  Back to cited text no. 17
    
18.
Perotto AO. Anatomical Guide for the Electromyographer: The Limb and Trunk. 5th ed. Springfield: Charles C Thomas Pub Ltd.; 2011.  Back to cited text no. 18
    
19.
Neptune RR, Kautz SA, Hull ML. The effect of pedaling rate on coordination in cycling. J Biomech 1997;30:1051-8.  Back to cited text no. 19
    
20.
Myers LJ, Erim Z, Lowery MM. Time and frequency domain methods for quantifying common modulation of motor unit firing patterns. J Neuroeng Rehabil 2004;1:2.  Back to cited text no. 20
    
21.
Schindler-Ivens S, Brown DA, Brooke JD. Direction-dependent phasing of locomotor muscle activity is altered post-stroke. J Neurophysiol 2004;92:2207-16.  Back to cited text no. 21
    
22.
Faria EW, Parker DL, Faria IE. The science of cycling: Factors affecting performance-part 2. Sports Med 2005;35:313-37.  Back to cited text no. 22
    
23.
Ericson M. On the biomechanics of cycling. A study of joint and muscle load during exercise on the bicycle ergometer. Scand J Rehabil Med Suppl 1986;16:1-43.  Back to cited text no. 23
    
24.
Reyes A, Laine CM, Kutch JJ, Valero-Cuevas FJ. Beta band corticomuscular drive reflects muscle coordination strategies. Front Comput Neurosci 2017;11:17.  Back to cited text no. 24
    
25.
Gray CM. Synchronous oscillations in neuronal systems: Mechanisms and functions. J Comput Neurosci 1994;1:11-38.  Back to cited text no. 25
    
26.
Boonstra TW. The potential of corticomuscular and intermuscular coherence for research on human motor control. Front Hum Neurosci 2013;7:855.  Back to cited text no. 26
    
27.
Hansen NL, Conway BA, Halliday DM, Hansen S, Pyndt HS, Biering-Sørensen F, et al. Reduction of common synaptic drive to ankle dorsiflexor motoneurons during walking in patients with spinal cord lesion. J Neurophysiol 2005;94:934-42.  Back to cited text no. 27
    
28.
Kamper DG, Fischer HC, Conrad MO, Towles JD, Rymer WZ, Triandafilou KM. Finger-thumb coupling contributes to exaggerated thumb flexion in stroke survivors. J Neurophysiol 2014;111:2665-74.  Back to cited text no. 28
    
29.
Nielsen JB, Brittain JS, Halliday DM, Marchand-Pauvert V, Mazevet D, Conway BA. Reduction of common motoneuronal drive on the affected side during walking in hemiplegic stroke patients. Clin Neurophysiol 2008;119:2813-8.  Back to cited text no. 29
    


    Figures

  [Figure 1], [Figure 2]



 

Top
 
  Search
 
    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

 
  In this article
Abstract
Introduction
Materials and Me...
Results
Discussion
Conclusion
References
Article Figures

 Article Access Statistics
    Viewed147    
    Printed2    
    Emailed0    
    PDF Downloaded35    
    Comments [Add]    

Recommend this journal