Vertebral level specific modulation of paraspinal muscle activity based on vestibular signals during walking.
balance control
electrical vestibular stimulation
gait stability
paraspinal muscles
Journal
The Journal of physiology
ISSN: 1469-7793
Titre abrégé: J Physiol
Pays: England
ID NLM: 0266262
Informations de publication
Date de publication:
22 Jan 2024
22 Jan 2024
Historique:
received:
24
10
2023
accepted:
02
01
2024
medline:
22
1
2024
pubmed:
22
1
2024
entrez:
22
1
2024
Statut:
aheadofprint
Résumé
Evoking muscle responses by electrical vestibular stimulation (EVS) may help to understand the contribution of the vestibular system to postural control. Although paraspinal muscles play a role in postural stability, the vestibulo-muscular coupling of these muscles during walking has rarely been studied. This study aimed to investigate how vestibular signals affect paraspinal muscle activity at different vertebral levels during walking with preferred and narrow step width. Sixteen healthy participants were recruited. Participants walked on a treadmill for 8 min at 78 steps/min and 2.8 km/h, at two different step width, either with or without EVS. Bipolar electromyography was recorded bilaterally from the paraspinal muscles at eight vertebral levels from cervical to lumbar. Coherence, gain, and delay of EVS and EMG responses were determined. Significant EVS-EMG coupling (P < 0.01) was found at ipsilateral and/or contralateral heel strikes. This coupling was mirrored between left and right relative to the midline of the trunk and between the higher and lower vertebral levels, i.e. a peak occurred at ipsilateral heel strike at lower levels, whereas it occurred at contralateral heel strike at higher levels. EVS-EMG coupling only partially coincided with peak muscle activity. EVS-EMG coherence slightly, but not significantly, increased when walking with narrow steps. No significant differences were found in gain and phase between the vertebral levels or step width conditions. In summary, vertebral level specific modulation of paraspinal muscle activity based on vestibular signals might allow a fast, synchronized, and spatially co-ordinated response along the trunk during walking. KEY POINTS: Mediolateral stabilization of gait requires an estimate of the state of the body, which is affected by vestibular afference. During gait, the heavy trunk segment is controlled by phasic paraspinal muscle activity and in rodents the medial and lateral vestibulospinal tracts activate these muscles. To gain insight in vestibulospinal connections in humans and their role in gait, we recorded paraspinal surface EMG of cervical to lumbar paraspinal muscles, and characterized coherence, gain and delay between EMG and electrical vestibular stimulation, during slow walking. Vestibular stimulation caused phasic, vertebral level specific modulation of paraspinal muscle activity at delays of around 40 ms, which was mirrored between left, lower and right, upper vertebral levels. Our results indicate that vestibular afference causes fast, synchronized, and spatially co-ordinated responses of the paraspinal muscles along the trunk, that simultaneously contribute to stabilizing the centre of mass trajectory and to keeping the head upright.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Chinese Government Scholarship
ID : 202108520034
Organisme : Aard- en Levenswetenschappen, Nederlandse Organisatie voor Wetenschappelijk Onderzoek
ID : 016.Vidi.178.014
Informations de copyright
© 2024 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society.
Références
Ali, A. S., Rowen, K. A., & Iles, J. F.(2003). Vestibular actions on back and lower limb muscles during postural tasks in man. The Journal of Physiology, 546(2), 615-624.
Anders, C., Wagner, H., Puta, C., Grassme, R., Petrovitch, A., & Scholle, H.-C.(2007). Trunk muscle activation patterns during walking at different speeds. Journal of Electromyography and Kinesiology, 17(2), 245-252.
Arvin, M., Mazaheri, M., Hoozemans, M. J. M., Pijnappels, M., Burger, B. J., Verschueren, S. M. P., & Van Dieën, J. H.(2016). Effects of narrow base gait on mediolateral balance control in young and older adults. Journal of Biomechanics, 49(7), 1264-1267.
Balter, S. G. T., Stokroos, R. J., Eterman, R. M. A., Paredis, S. A. B., Orbons, J., & Kingma, H.(2004). Habituation to galvanic vestibular stimulation. Acta Oto-Laryngologica, 124(8), 941-945.
Basaldella, E., Takeoka, A., Sigrist, M., & Arber, S.(2015). Multisensory signaling shapes vestibulo-motor circuit specificity. Cell, 163(2), 301-312.
Blouin, J.-S., Dakin, C. J., Van Den Doel, K., Chua, R., Mcfadyen, B. J., & Inglis, J. T.(2011). Extracting phase-dependent human vestibular reflexes during locomotion using both time and frequency correlation approaches. Journal of Applied Physiology (1985), 111(5), 1484-1490.
Bruijn, S. M., Meijer, O. G., Beek, P. J., & Van Dieën, J. H.(2013). Assessing the stability of human locomotion: A review of current measures. Journal of the Royal Society, Interface, 10(83), 20120999.
Bruijn, S. M., & Van Dieën, J. H.(2018). Control of human gait stability through foot placement. Journal of the Royal Society, Interface, 15(143), 20170816.
Callaghan, J. P., Patla, A. E., & Mcgill, S. M.(1999). Low back three-dimensional joint forces, kinematics, and kinetics during walking. Clinical Biomechanics (Bristol, Avon), 14(3), 203-216.
Cullen, K. E.(2012). The vestibular system: Multimodal integration and encoding of self-motion for motor control. Trends in Neuroscience (Tins), 35(3), 185-196.
Dakin, C. J., Inglis, J. T., Chua, R., & Blouin, J.-S.(2013). Muscle-specific modulation of vestibular reflexes with increased locomotor velocity and cadence. Journal of Neurophysiology, 110(1), 86-94.
Dakin, C. J., Luu, B. L., Van Den Doel, K., Inglis, J. T., & Blouin, J.-S.(2010). Frequency-specific modulation of vestibular-evoked sway responses in humans. Journal of Neurophysiology, 103(2), 1048-1056.
Day, B. L.(1999). Galvanic vestibular stimulation: New uses for an old tool. The Journal of Physiology, 517(Pt 3), 631.
De Leva, P.(1996). Adjustments to Zatsiorsky-Seluyanov's segment inertia parameters. Journal of Biomechanics, 29(9), 1223-1230.
De Sèze, M., Falgairolle, M., Viel, S., Assaiante, C., & Cazalets, J.-R.(2008). Sequential activation of axial muscles during different forms of rhythmic behavior in man. Experimental Brain Research, 185(2), 237-247.
Deshpande, N., Hewston, P., & Yoshikawa, M.(2015). Age-associated differences in global and segmental control during dual-task walking under sub-optimal sensory conditions. Human Movement Science, 40, 211-219.
Dichgans, J., & Diener, H. C.(1989). The contribution of vestibulo-spinal mechanisms to the maintenance of human upright posture. Acta Oto-Laryngologica, 107(5-6), 338-345.
Fitzpatrick, R. C., & Day, B. L.(2004). Probing the human vestibular system with galvanic stimulation. Journal of Applied Physiology (1985), 96(6), 2301-2316.
Forbes, P. A., Dakin, C. J., Vardy, A. N., Happee, R., Siegmund, G. P., Schouten, A. C., & Blouin, J.-S.(2013). Frequency response of vestibular reflexes in neck, back, and lower limb muscles. Journal of Neurophysiology, 110(8), 1869-1881.
Forbes, P. A., Fice, J. B., Siegmund, G. P., & Blouin, J.-S.(2018). Electrical vestibular stimuli evoke robust muscle activity in deep and superficial neck muscles in humans. Frontiers in Neurology, 9, 535.
Forbes, P. A., Kwan, A., Rasman, B. G., Mitchell, D. E., Cullen, K. E., & Blouin, J.-S.(2020). Neural mechanisms underlying high-frequency vestibulocollic reflexes in humans and monkeys. Journal of Neuroscience, 40(9), 1874-1887.
Forbes, P. A., Vlutters, M., Dakin, C. J., Van Der Kooij, H., Blouin, J.-S., & Schouten, A. C.(2017). Rapid limb-specific modulation of vestibular contributions to ankle muscle activity during locomotion. The Journal of Physiology, 595(6), 2175-2195.
Fukushima, K., Peterson, B. W., & Wilson, V. J.(1979). Vestibulospinal, reticulospinal and interstitiospinal pathways in the cat. Progress in Brain Research, 50, 121-136.
Goldberg, J. M., & Cullen, K. E.(2011). Vestibular control of the head: Possible functions of the vestibulocollic reflex. Experimental Brain Research, 210(3-4), 331-345.
Goldberg, J. M., Ferna´Ndez, C., & Smith, C. E.(1982). Responses of vestibular-nerve afferents in the squirrel monkey to externally applied galvanic currents. Brain Research, 252(1), 156-160.
Grillner, S., & Hongo, T.(1972). Vestibulospinal effects on motoneurones and interneurones in the lumbosacral cord. Progress in Brain Research, 37, 243-262.
Guillaud, E., Faure, C., Doat, E., Bouyer, L. J., Guehl, D., & Cazalets, J.-R.(2020). Ancestral persistence of vestibulospinal reflexes in axial muscles in humans. Journal of Neurophysiology, 123(5), 2010-2023.
Hak, L., Houdijk, H., Steenbrink, F., Mert, A., Van Der Wurff, P., Beek, P. J., & Van Dieën, J. H.(2012). Speeding up or slowing down?: Gait adaptations to preserve gait stability in response to balance perturbations. Gait & Posture, 36(2), 260-264.
Halliday, D. M., & Farmer, S. F.(2010). On the need for rectification of surface EMG. Journal of Neurophysiology, 103(6), 3547.
Hannan, K. B., Todd, M. K., Pearson, N. J., Forbes, P. A., & Dakin, C. J.(2021). Vestibular attenuation to random-waveform galvanic vestibular stimulation during standing and treadmill walking. Scientific Reports, 11(1), 8127.
Hof, A.t L.(2007). The equations of motion for a standing human reveal three mechanisms for balance. Journal of Biomechanics, 40(2), 451-457.
Ivanenko, Y. P., Poppele, R. E., & Lacquaniti, F.(2004). Five basic muscle activation patterns account for muscle activity during human locomotion. The Journal of Physiology, 556(1), 267-282.
Ivanenko, Y. P., Poppele, R. E., & Lacquaniti, F.(2006). Spinal cord maps of spatiotemporal alpha-motoneuron activation in humans walking at different speeds. Journal of Neurophysiology, 95(2), 602-618.
Jiang, X., Bian, G. B., & Tian, Z.(2019). Removal of artifacts from EEG signals: A review. Sensors (Basel), 19.
Kasumacic, N., Glover, J. C., & Perreault, M.-C.(2010). Segmental patterns of vestibular-mediated synaptic inputs to axial and limb motoneurons in the neonatal mouse assessed by optical recording. The Journal of Physiology, 588(24), 4905-4925.
Kasumacic, N., Lambert, F. M., Coulon, P., Bras, H., Vinay, L., Perreault, M.-C., & Glover, J. C.(2015). Segmental organization of vestibulospinal inputs to spinal interneurons mediating crossed activation of thoracolumbar motoneurons in the neonatal mouse. Journal of Neuroscience, 35(21), 8158-8169.
Kwan, A., Forbes, P. A., Mitchell, D. E., Blouin, J.-S., & Cullen, K. E.(2019). Neural substrates, dynamics and thresholds of galvanic vestibular stimulation in the behaving primate. Nature Communications, 10(1), 1904.
Magnani, R. M., Bruijn, S. M., Van Dieën, J. H., & Forbes, P. A.(2021). Stabilization demands of walking modulate the vestibular contributions to gait. Scientific Reports, 11(1), 13736.
Magnani, R. M., Van Dieën, J. H., & Bruijn, S. M.(2023). Effects of vestibular stimulation on gait stability when walking at different step widths. Experimental Brain Research, 241(1), 49-58.
Maris, E., Schoffelen, J.-M., & Fries, P.(2007). Nonparametric statistical testing of coherence differences. Journal of Neuroscience Methods, 163(1), 161-175.
Markham, C. H.(1987). Vestibular control of muscular tone and posture. Canadian Journal of Neurological Sciences, 14(S3), 493-496.
Mazaheri, M., Coenen, P., Parnianpour, M., Kiers, H., & Van Dieën, J. H.(2013). Low back pain and postural sway during quiet standing with and without sensory manipulation: A systematic review. Gait & Posture, 37(1), 12-22.
Mcclelland, V. M., Cvetkovic, Z., & Mills, K. R.(2014). Inconsistent effects of EMG rectification on coherence analysis. The Journal of Physiology, 592(1), 249-250.
Murray, A. J., Croce, K., Belton, T., Akay, T., & Jessell, T. M.(2018). Balance control mediated by vestibular circuits directing limb extension or antagonist muscle co-activation. Cell Reports, 22(5), 1325-1338.
Myers, L. J., Lowery, M., O'malley, M., Vaughan, C. L., Heneghan, C., St Clair Gibson, A., Harley, Y. X. R., & Sreenivasan, R.(2003). Rectification and non-linear pre-processing of EMG signals for cortico-muscular analysis. Journal of Neuroscience Methods, 124(2), 157-165.
Neto, O. P., & Christou, E. A.(2010). Rectification of the EMG signal impairs the identification of oscillatory input to the muscle. Journal of Neurophysiology, 103(2), 1093-1103.
Pataky, T. C., Robinson, M. A., & Vanrenterghem, J.(2016). Region-of-interest analyses of one-dimensional biomechanical trajectories: Bridging 0D and 1D theory, augmenting statistical power. PeerJ, 4, e2652.
Peterson, B. W., Maunz, R. A., & Fukushima, K.(1978). Properties of a new vestibulospinal projection, the caudal vestibulospinal tract. Experimental Brain Research, 32(2), 287-292.
Potvin, J. R., & Brown, S. H. M. (2004). Less is more: High pass filtering, to remove up to 99% of the surface EMG signal power, improves EMG-based biceps brachii muscle force estimates. Journal of Electromyography and Kinesiology, 14(3), 389-399.
Roerdink, M., Coolen, B. (H.), Clairbois, B. (H.)E., Lamoth, C. J. C., & Beek, P. J.(2008). Online gait event detection using a large force platform embedded in a treadmill. Journal of Biomechanics, 41(12), 2628-2632.
Shiavi, R.(1985). Electromyographic patterns in adult locomotion: A comprehensive review. Journal of Rehabilitation Research and Development, 22(3), 85-98.
Sprenger, A., Wojak, J. F., Jandl, N. M., & Helmchen, C.(2017). Postural control in bilateral vestibular failure: Its relation to visual, proprioceptive, vestibular, and cognitive input. Frontiers in Neurology, 8, 444.
St George, R. J., & Fitzpatrick, R. C.(2011). The sense of self-motion, orientation and balance explored by vestibular stimulation. The Journal of Physiology, 589(4), 807-813.
Van Asseldonk, E. H. F., Campfens, S. F., Verwer, S. J. F., Van Putten, M. J. A. M., & Stegeman, D. F.(2014). Reliability and agreement of intramuscular coherence in tibialis anterior muscle. PLoS ONE, 9(2), e88428.
Van Leeuwen, M., Bruijn, S., & Van Dieën, J.(2022). Mechanisms that stabilize human walking. Brazilian Journal of Motor Behavior, 16(5), 326-351.
Van Schooten, K. S., Sloot, L. H., Bruijn, S. M., Kingma, H., Meijer, O. G., Pijnappels, M., & Van Dieën, J. H.(2011). Sensitivity of trunk variability and stability measures to balance impairments induced by galvanic vestibular stimulation during gait. Gait & Posture, 33(4), 656-660.
Ward, N. J., Farmer, S. F., Berthouze, L., & Halliday, D. M.(2013). Rectification of EMG in low force contractions improves detection of motor unit coherence in the beta-frequency band. Journal of Neurophysiology, 110(8), 1744-1750.
Wilson, V. J., Boyle, R., Fukushima, K., Rose, P. K., Shinoda, Y., Sugiuchi, Y., & Uchino, Y.(1995). The vestibulocollic reflex. Journal of Vestibular Research, 5(3), 147-170.
Wilson, V. J., & Maeda, M.(1974). Connections between semicircular canals and neck motorneurons in the cat. Journal of Neurophysiology, 37(2), 346-357.
Wilson, V. J., & Yoshida, M.(1969). Comparison of effects of stimulation of Deiters' nucleus and medial longitudinal fasciculus on neck, forelimb, and hindlimb motoneurons. Journal of Neurophysiology, 32(5), 743-758.
Wilson, V. J., Yoshida, M., & Schor, R. H.(1970). Supraspinal monosynaptic excitation and inhibition of thoracic back montoneurons. Experimental Brain Research, 11(3), 282-295.
Zhan, Y., Halliday, D., Jiang, P., Liu, X., & Feng, J.(2006). Detecting time-dependent coherence between non-stationary electrophysiological signals-a combined statistical and time-frequency approach. Journal of Neuroscience Methods, 156(1-2), 322-332.