How Posture and Previous Sensorimotor Experience Influence Muscle Activity during Gait Imagery in Young Healthy Individuals
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
IGA_FZV_2020_007
Internal institucional grant by Palacky University
PubMed
38002564
PubMed Central
PMC10670012
DOI
10.3390/brainsci13111605
PII: brainsci13111605
Knihovny.cz E-zdroje
- Klíčová slova
- gait, motor imagery, muscle activity, surface electromyography,
- Publikační typ
- časopisecké články MeSH
This study explores how gait imagery (GI) influences lower-limb muscle activity with respect to posture and previous walking experience. We utilized surface electromyography (sEMG) in 36 healthy young individuals aged 24 (±1.1) years to identify muscle activity during a non-gait imagery task (non-GI), as well as GI tasks before (GI-1) and after the execution of walking (GI-2), with assessments performed in both sitting and standing postures. The sEMG was recorded on both lower limbs on the tibialis anterior (TA) and on the gastrocnemius medialis (GM) for all tested tasks. As a result, a significant muscle activity decrease was found in the right TA for GI-1 compared to GI-2 in both sitting (p = 0.008) and standing (p = 0.01) positions. In the left TA, the activity decreased in the sitting posture during non-GI (p = 0.004) and GI-1 (p = 0.009) in comparison to GI-2. No differences were found for GM. The subjective level of imagination difficulty improved for GI-2 in comparison to GI-1 in both postures (p < 0.001). Previous sensorimotor experience with real gait execution and sitting posture potentiate TA activity decrease during GI. These findings contribute to the understanding of neural mechanisms beyond GI.
Zobrazit více v PubMed
Mulder T.H. Motor imagery and action observation: Cognitive tools for rehabilitation. J. Neural Transm. 2007;114:1265–1278. doi: 10.1007/s00702-007-0763-z. PubMed DOI PMC
Decety J., Grezes J. Neural mechanisms subserving the perception of human actions. Trends Cogn. Sci. 1999;3:172–178. doi: 10.1016/S1364-6613(99)01312-1. PubMed DOI
Jeannerod M. Neural simulation of action: A unifying mechanism for motor cognition. NeuroImage. 2001;14:103–109. doi: 10.1006/nimg.2001.0832. PubMed DOI
Hallett M., Fieldman J., Cohen L.G., Sadato N., Pascual-Leone A. Involvement of primary motor cortex in motor imagery and mental practice. Behav. Brain Sci. 1994;17:210. doi: 10.1017/S0140525X00034130. DOI
Nicholson V.P., Keogh J.W.L., Low Choy N.L. Can a single session of motor imagery promote motor learning of locomotion in older adults? A randomized controlled trial. Clin. Interv. Aging. 2018;13:713–722. doi: 10.2147/CIA.S164401. PubMed DOI PMC
Malouin F., Richards C.L., Jackson P.L., Dumas F., Doyon J. Brain activations during motor imagery of locomotor-related tasks: A PET study. Hum. Brain. Mapp. 2003;19:47–62. doi: 10.1002/hbm.10103. PubMed DOI PMC
Fleury L., Dreyer L., El Makkaoui R., Leroy E., Rossetti Y., Collet C. Inter-Task Transfer of Prism Adaptation through Motor Imagery. Brain Sci. 2023;13:114. doi: 10.3390/brainsci13010114. PubMed DOI PMC
Kim J.-S., Oh D.-W., Kim S.-Y., Choi J.-D. Visual and kinesthetic locomotor imagery training integrated with auditory step rhythm for walking performance of patients with chronic stroke. Clin. Rehabil. 2011;25:134–145. doi: 10.1177/0269215510380822. PubMed DOI
Bovonsunthonchai S., Aung N., Hiengkaew V., Tretriluxana J. A randomized controlled trial of motor imagery combined with structured progressive circuit class therapy on gait in stroke survivors. Sci. Rep. 2020;10:6945. doi: 10.1038/s41598-020-63914-8. PubMed DOI PMC
Oostra K.M., Oomen A., Vanderstraeten G., Vingerhoets G. Influence of motor imagery training on gait rehabilitation in sub-acute stroke: A randomized controlled trial. J. Rehabil. Med. 2015;47:204–209. doi: 10.2340/16501977-1908. PubMed DOI
Zaparolli L., Sacheli L.M., Seghezzi S., Preto M., Stucovitz E., Negrini F., Paulesu E. Motor imagery training speeds up gait recovery and decreases the risk of falls in patients submitted to total knee arthroplasty. Sci. Rep. 2020;10:8917. doi: 10.1038/s41598-020-65820-5. PubMed DOI PMC
Stippich C., Ochmann H., Sartor K. Somatotopic mapping of the human primary sensorimotor cortex during motor imagery and motor execution by functional magnetic resonance imaging. Neurosci. Lett. 2002;331:50–54. doi: 10.1016/S0304-3940(02)00826-1. PubMed DOI
Ehrsson H.H., Geyer S., Naito E. Imagery of voluntary movement of fingers, toes, and tongue activates corresponding body-part-specific motor representations. J. Neurophysiol. 2003;90:3304–3316. doi: 10.1152/jn.01113.2002. PubMed DOI
Hétu S., Grégoire M., Saimpont A., Coll M.-P., Eugène F., Michon P.-E., Jackson P.L. The neural network of motor imagery: An ALE meta-analysis. Neurosci. Biobehav. Rev. 2013;37:930–949. doi: 10.1016/j.neubiorev.2013.03.017. PubMed DOI
Vrana A., Hotz-Boendermaker S., Stämpfli P., Hänggi J., Seifritz E., Humphreys B.K., Meier M.L. Differential Neural Processing during Motor Imagery of Daily Activities in Chronic Low Back Pain Patients. PLoS ONE. 2015;10:e0142391. doi: 10.1371/journal.pone.0142391. PubMed DOI PMC
van der Meulen M., Allali G., Rieger S.W., Assal F., Vuilleumier P. The influence of individual motor imagery ability on cerebral recruitment during gait imagery. Hum. Brain Mapp. 2014;35:455–470. doi: 10.1002/hbm.22192. PubMed DOI PMC
Sharma N., Simmons L.H., Jones P.S., Day D.J., Carpenter T.A., Pomeroy V.M., Baron J.C. Motor imagery after subcortical stroke: A functional magnetic resonance imaging study. Stroke. 2009;40:1315–1324. doi: 10.1161/STROKEAHA.108.525766. PubMed DOI
Bonnet M., Decety J., Jeannerod M., Requin J. Mental simulation of an action modulates the excitability of spinal reflex pathways in man. Cogn. Brain Res. 1997;5:221–228. doi: 10.1016/S0926-6410(96)00072-9. PubMed DOI
Guillot A., Di Rienzo F., MacIntyre T., Moran A., Collet C. Imagining is Not Doing but Involves Specific Motor Commands: A Review of Experimental Data Related to Motor Inhibition. Front. Hum. Neurosci. 2012;6:247. doi: 10.3389/fnhum.2012.00247. PubMed DOI PMC
Roosink M., Zijdewind I. Corticospinal excitability during observation and imagery of simple and complex hand tasks: Implications for motor rehabilitation. Behav. Brain Res. 2010;213:35–41. doi: 10.1016/j.bbr.2010.04.027. PubMed DOI
Solodkin A., Hlustik P., Chen E.E., Small S.L. Fine modulation in network activation during motor execution and motor imagery. Cereb. Cortex. 2004;14:1246–1255. doi: 10.1093/cercor/bhh086. PubMed DOI
Dietz V., Duysens J. Significance of load receptor input during locomotion: A review. Gait Posture. 2000;11:102–110. doi: 10.1016/S0966-6362(99)00052-1. PubMed DOI
Dietz V. Spinal cord pattern generators for locomotion. Clin. Neurophysiol. 2003;114:1379–1389. doi: 10.1016/S1388-2457(03)00120-2. PubMed DOI
Dietz V. Behavior of spinal neurons deprived of supraspinal input. Nat. Rev. Neurol. 2010;6:167–174. doi: 10.1038/nrneurol.2009.227. PubMed DOI
MacKay-Lyons M. Central pattern generation of locomotion: A review of the evidence. Phys. Ther. 2002;82:69–83. doi: 10.1093/ptj/82.1.69. PubMed DOI
Bakker M., de Lange F.P., Stevens J.A., Toni I., Bloem B.R. Motor imagery of gait: A quantitative approach. Exp. Brain Res. 2007;179:497–504. doi: 10.1007/s00221-006-0807-x. PubMed DOI
Mizuguchi N., Sakamoto M., Muraoka T., Moriyama N., Nakagawa K., Nakata H., Kanosue K. Influence of somatosensory input on corticospinal excitability during motor imagery. Neurosci. Lett. 2012;514:127–130. doi: 10.1016/j.neulet.2012.02.073. PubMed DOI
Mizuguchi N., Sakamoto M., Muraoka T., Kanosue K. Influence of touching an object on corticospinal excitability during motor imagery. Exp. Brain Res. 2009;196:529–535. doi: 10.1007/s00221-009-1875-5. PubMed DOI
Guillot A., Lebon F., Rouffet D., Champely S., Doyon J., Collet C. Muscular responses during motor imagery as a function of muscle contraction types. Int. J. Psychophysiol. 2007;66:18–27. doi: 10.1016/j.ijpsycho.2007.05.009. PubMed DOI
Vargas C.D., Olivier E., Craighero L., Fadiga L., Duhamel J.R., Sirigu A. The influence of hand posture on corticospinal excitability during motor imagery: A transcranial magnetic stimulation study. Cereb. Cortex. 2004;14:1200–1206. doi: 10.1093/cercor/bhh080. PubMed DOI
Nakazawa K., Kawashima N., Obata H., Yamanaka K., Nozaki D., Akai M. Facilitation of both stretch reflex and corticospinal pathways of the tibialis anterior muscle during standing in humans. Neurosci. Lett. 2003;338:53–56. doi: 10.1016/S0304-3940(02)01353-8. PubMed DOI
Yao W.X., Ranganathan V.K., Allexandre D., Siemionow V., Yue G.H. Kinesthetic imagery training of forceful muscle contractions increases brain signal and muscle strength. Front. Hum. Neurosci. 2013;7:561. doi: 10.3389/fnhum.2013.00561. PubMed DOI PMC
Dos Anjos T., Guillot A., Kerautret Y., Daligault S., Di Rienzo F. Corticomotor Plasticity Underlying Priming Effects of Motor Imagery on Force Performance. Brain Sci. 2022;12:1537. doi: 10.3390/brainsci12111537. PubMed DOI PMC
Kobelt M., Wirth B., Schuster-Amft C. Muscle Activation During Grasping With and Without Motor Imagery in Healthy Volunteers and Patients After Stroke or With Parkinson’s Disease. Front. Psychol. 2018;9:597. doi: 10.3389/fpsyg.2018.00597. PubMed DOI PMC
Geiger D.E., Behrendt F., Schuster-Amft C. EMG Muscle Activation Pattern of Four Lower Extremity Muscles during Stair Climbing, Motor Imagery, and Robot-Assisted Stepping: A Cross-Sectional Study in Healthy Individuals. BioMed Res. Int. 2019;2019:9351689. doi: 10.1155/2019/9351689. PubMed DOI PMC
Lemos T., Souza N.S., Horsczaruk C.H., Nogueira-Campos A.A., de Oliveira L.A., Vargas C.D., Rodrigues E.C. Motor imagery modulation of body sway is task-dependent and relies on imagery ability. Front. Hum. Neurosci. 2014;8:290. doi: 10.3389/fnhum.2014.00290. PubMed DOI PMC
Kolářová B., Krobot A., Polehlová K., Hluštík P., Richards J. Effect of Gait Imagery Tasks on Lower Limb Muscle Activity With Respect to Body Posture. Percept. Mot. Skills. 2016;122:411–431. doi: 10.1177/0031512516640377. PubMed DOI
Bussel B., Roby-Brami A., Neris O.R., Yakovleff A. Evidence for a spinal stepping generator in man: An electrophysiological study. Acta Neurobiol. Exp. 1996;56:465–468. PubMed
Harkema S.J., Hurley S.L., Patel U.K., Requejo P.S., Dobkin B.H., Edgerton V.R. The human lumbosacral spinal cord interprets loading during stepping. J. Neurophysiol. 1997;77:797–811. doi: 10.1152/jn.1997.77.2.797. PubMed DOI
Takakusaki K., Habaguchi T., Ohtinata-Sugimoto J., Saitoh K., Sakamoto T. Basal ganglia efferents to the brainstem centers controlling postural muscle tone and locomotion: A new concept for understanding motor disorders in basal ganglia dysfunction. Neuroscience. 2003;119:293–308. doi: 10.1016/S0306-4522(03)00095-2. PubMed DOI
Saimpont A., Malouin F., Tousignant B., Jackson P.L. The influence of body configuration on motor imagery of walking in younger and older adults. Neuroscience. 2012;222:49–57. doi: 10.1016/j.neuroscience.2012.06.066. PubMed DOI
Shimba S., Kawashima N., Ohta Y., Yamamoto S., Nakazawa K. Enhanced stretch reflex excitability in the soleus muscle during passive standing posture in humans. J. Electromyogr. Kinesiol. 2010;20:406–412. doi: 10.1016/j.jelekin.2009.04.003. PubMed DOI
Beauchet O., Launay C., Sekhon H. Body position and motor imagery strategy effects on imagining gait in healthy adults: Results from a cross-sectional study. PLoS ONE. 2018;13:e0191513. doi: 10.1371/journal.pone.0191513. PubMed DOI PMC
Horslen B.C., Inglis J.T., Blouin J.S., Carpenter M.G. Both standing and postural threat decrease Achilles’ tendon reflex inhibition from tendon electrical stimulation. J. Physiol. 2017;595:4493–4506. doi: 10.1113/JP273935. PubMed DOI PMC
McCrea D.A. Spinal circuitry of sensorimotor control of locomotion. J. Physiol. 2001;533:41–50. doi: 10.1111/j.1469-7793.2001.0041b.x. PubMed DOI PMC
Mayer W.P., Murray A.J., Brenner-Morton S., Jessell T.M., Tourtellotte W.G., Akay T. Role of muscle spindle feedback in regulating muscle activity strength during walking at different speeds in mice. J. Neurophysiol. 2018;120:2484–2497. doi: 10.1152/jn.00250.2018. PubMed DOI PMC
Saimpont A., Malouin F., Durand A., Mercier C., di Rienzo F., Saruco E., Collet C., Guillot A., Jackson P.L. The effects of body position and actual execution on motor imagery of locomotor tasks in people with a lower-limb amputation. Sci. Rep. 2021;11:13788. doi: 10.1038/s41598-021-93240-6. PubMed DOI PMC
Hall C.R., Martin K.A. Measuring movement imagery abilities: A revision of the Movement Imagery Questionnaire. J. Ment. Imag. 1997;21:143–154.
Monsma E., Short S., Hall C., Gregg M., Sullivan P. Psychometric Properties of the Revised Movement Imagery Questionnaire (MIQ-R) J. Imag. Res. Sport Phys. Act. 2009;4 doi: 10.2202/1932-0191.1027. DOI
Stegeman D., Hermens H. Standards for surface electromyography: The European project Surface EMG for non-invasive assessment of muscles (SENIAM) J. Appl. Biomech. 2007:108–112.
Farina D., Merletti R., Enoka R.M. The extraction of neural strategies from the surface EMG: An update. J. Appl. Physiol. 2014;117:1215–1230. doi: 10.1152/japplphysiol.00162.2014. PubMed DOI PMC
Heckman C.J., Enoka R.M. Motor units. Compr. Physiol. 2012;2:2629–2682. doi: 10.1002/cphy.c100087. PubMed DOI
Heckman C.J., Mottram C., Quinlan K., Theiss R., Schuster J. Motoneuron excitability: The importance of neuromodulatory inputs. Clin. Neurophysiol. 2009;120:2040–2054. doi: 10.1016/j.clinph.2009.08.009. PubMed DOI PMC
Aoyama T., Kaneko F., Ohashi Y., Kohno Y. Dissociation between cortical and spinal excitability of the antagonist muscle during combined motor imagery and action observation. Sci. Rep. 2019;9:13120. doi: 10.1038/s41598-019-49456-8. PubMed DOI PMC
Faist M., Hoefer C., Hodapp M., Dietz V., Berger W., Duysens J. In humans Ib facilitation depends on locomotion while suppression of Ib inhibition requires loading. Brain Res. 2006;1076:87–92. doi: 10.1016/j.brainres.2005.12.069. PubMed DOI
Sheik A.A., Korn E.R. Imagery in Sports and Physical Performance. Baywood Publishing Company, Inc.; Amityville, NY, USA: 1994.
Lotze M., Cohen L.G. Volition and imagery in neurorehabilitation. Cogn. Behav. Neurol. 2006;19:135–140. doi: 10.1097/01.wnn.0000209875.56060.06. PubMed DOI
Kolářová B., Richards J., Haltmar H., Lippertová K., Connell L., Chohan A. The effect of motor imagery on quality of movement when performing reaching tasks in healthy subjects: A proof of concept. J. Bodyw. Mov. Ther. 2022;29:161–166. doi: 10.1016/j.jbmt.2021.10.004. PubMed DOI
Vigotsky A.D., Halperin I., Lehman G.J., Trajano G.S., Vieira T.M. Interpreting Signal Amplitudes in Surface Electromyography Studies in Sport and Rehabilitation Sciences. Front. Physiol. 2018;8:985. doi: 10.3389/fphys.2017.00985. PubMed DOI PMC
Milton J., Small S.L., Solodkin A. Imaging motor imagery: Methodological issues related to expertise. Methods. 2008;45:336–341. doi: 10.1016/j.ymeth.2008.05.002. PubMed DOI PMC
Gentili R., Papaxanthis C., Pozzo T. Improvement and generalization of arm motor performance through motor imagery practice. Neuroscience. 2006;137:761–772. doi: 10.1016/j.neuroscience.2005.10.013. PubMed DOI
Muñoz M.R., González-Sánchez M., Cuesta-Vargas A.I. Tibialis anterior analysis from a functional and architectural perspective during isometric foot dorsiflexion: A cross-sectional study of repeated measures. J. Foot Ankle Res. 2015;8:74. doi: 10.1186/s13047-015-0132-3. PubMed DOI PMC
Nadeau S., Gravel D., Arsenault A.B., Bourbonnais D. Plantarflexor weakness as a limiting factor of gait speed in stroke subjects and the compensating role of hip flexors. Clin. Biomech. 1999;14:125–135. doi: 10.1016/S0268-0033(98)00062-X. PubMed DOI