Visual Attention and Motion Visibility Modulate Motor Resonance during Observation of Human Walking in Different Manners
Abstract
:1. Introduction
2. Materials and Methods
2.1. Participants
2.2. Electromyography (EMG)
2.3. TMS Procedure
2.4. Stimulation Protocol
2.5. Experimental Conditions
- (1)
- In the observation condition of multiple-joint movements (MJ observation), the observers were instructed to closely observe the movements of the walker’s right lower limb while they were watching the monitor projecting the complete image of the demonstrator’s gait.
- (2)
- In the observation condition of single-joint movements (SJ observation), to elucidate the effect of visual attention on the motor system, the observers were instructed to closely observe the movements of the walker’s right ankle joint while they were watching the monitor projecting the complete image of the demonstrator’s gait.
- (3)
- In the observation condition of restricted single-joint movements (R-SJ observation), to elucidate the effect of motion visibility on the motor system, the observers were instructed to closely observe the movements of the walker’s right lower limb while they were watching the monitor projecting the same video, as aforementioned, which was zoomed to include only the area below the knee joints.
2.6. Assessment of Degree of Attention
2.7. Data and Statistical Analyses
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Caspers, S.; Zilles, K.; Laird, A.R.; Eickhoff, S.B. ALE meta-analysis of action observation and imitation in the human brain. Neuroimage 2010, 50, 1148–1167. [Google Scholar] [CrossRef] [Green Version]
- Hardwick, R.M.; Caspers, S.; Eickhoff, S.B.; Swinnen, S.P. Neural correlates of action: Comparing meta-analyses of imagery, observation, and execution. Neurosci. Biobehav. Rev. 2018, 94, 31–44. [Google Scholar] [CrossRef]
- Naish, K.R.; Houston-Price, C.; Bremner, A.J.; Holmes, N.P. Effects of action observation on corticospinal excitability: Muscle specificity, direction, and timing of the mirror response. Neuropsychologia 2014, 64, 331–348. [Google Scholar] [CrossRef]
- Sarasso, E.; Gemma, M.; Agosta, F.; Filippi, M.; Gatti, R. Action observation training to improve motor function recovery: A systematic review. Arch. Physiother. 2015, 5, 14. [Google Scholar] [CrossRef] [Green Version]
- Caligiore, D.; Mustile, M.; Spalletta, G.; Baldassarre, G. Action observation and motor imagery for rehabilitation in Parkinson’s disease: A systematic review and an integrative hypothesis. Neurosci. Biobehav. Rev. 2017, 72, 210–222. [Google Scholar] [CrossRef]
- Borges, L.R.; Fernandes, A.B.; Melo, L.P.; Guerra, R.O.; Campos, T.F. Action observation for upper limb rehabilitation after stroke. Cochrane Database Syst. Rev. 2018, 10, CD011887. [Google Scholar] [CrossRef] [PubMed]
- Peng, T.H.; Zhu, J.D.; Chen, C.C.; Tai, R.Y.; Lee, C.Y.; Hsieh, Y.W. Action observation therapy for improving arm function, walking ability, and daily activity performance after stroke: A systematic review and meta-analysis. Clin. Rehabil. 2019, 33, 1277–1285. [Google Scholar] [CrossRef]
- Zhang, B.; Kan, L.; Dong, A.; Zhang, J.; Bai, Z.; Xie, Y.; Liu, Q.; Peng, Y. The effects of action observation training on improving upper limb motor functions in people with stroke: A systematic review and meta-analysis. PLoS ONE 2019, 14, e0221166. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Buchignani, B.; Beani, E.; Pomeroy, V.; Iacono, O.; Sicola, E.; Perazza, S.; Bieber, E.; Feys, H.; Klingels, K.; Cioni, G.; et al. Action observation training for rehabilitation in brain injuries: A systematic review and meta-analysis. BMC Neurol. 2019, 19, 344. [Google Scholar] [CrossRef] [PubMed]
- Buccino, G. Action observation treatment: A novel tool in neurorehabilitation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2014, 369, 20130185. [Google Scholar] [CrossRef]
- Dalla Volta, R.; Fasano, F.; Cerasa, A.; Mangone, G.; Quattrone, A.; Buccino, G. Walking indoors, walking outdoors: An fMRI study. Front. Psychol. 2015, 6, 1502. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fadiga, L.; Fogassi, L.; Pavesi, G.; Rizzolatti, G. Motor facilitation during action observation: A magnetic stimulation study. J. Neurophysiol. 1995, 73, 2608–2611. [Google Scholar] [CrossRef] [PubMed]
- Strafella, A.P.; Paus, T. Modulation of cortical excitability during action observation: A transcranial magnetic stimulation study. Neuroreport 2000, 11, 2289–2292. [Google Scholar] [CrossRef]
- Borroni, P.; Montagna, M.; Cerri, G.; Baldissera, F. Cyclic time course of motor excitability modulation during the observation of a cyclic hand movement. Brain Res. 2005, 1065, 115–124. [Google Scholar] [CrossRef] [PubMed]
- Montagna, M.; Cerri, G.; Borroni, P.; Baldissera, F. Excitability changes in human corticospinal projections to muscles moving hand and fingers while viewing a reaching and grasping action. Eur. J. Neurosci. 2005, 22, 1513–1520. [Google Scholar] [CrossRef]
- Romani, M.; Cesari, P.; Urgesi, C.; Facchini, S.; Aglioti, S.M. Motor facilitation of the human cortico-spinal system during observation of bio-mechanically impossible movements. Neuroimage 2005, 26, 755–763. [Google Scholar] [CrossRef]
- Urgesi, C.; Candidi, M.; Fabbro, F.; Romani, M.; Aglioti, S.M. Motor facilitation during action observation: Topographic mapping of the target muscle and influence of the onlooker’s posture. Eur. J. Neurosci. 2006, 23, 2522–2530. [Google Scholar] [CrossRef]
- Catmur, C.; Walsh, V.; Heyes, C. Sensorimotor learning configures the human mirror system. Curr. Biol. 2007, 17, 1527–1531. [Google Scholar] [CrossRef] [Green Version]
- Alaerts, K.; Senot, P.; Swinnen, S.P.; Craighero, L.; Wenderoth, N.; Fadiga, L. Force requirements of observed object lifting are encoded by the observer’s motor system: A TMS study. Eur. J. Neurosci. 2010, 31, 1144–1153. [Google Scholar] [CrossRef] [Green Version]
- Cavallo, A.; Becchio, C.; Sartori, L.; Bucchioni, G.; Castiello, U. Grasping with tools: Corticospinal excitability reflects observed hand movements. Cereb. Cortex 2012, 22, 710–716. [Google Scholar] [CrossRef] [Green Version]
- Tidoni, E.; Borgomaneri, S.; di Pellegrino, G.; Avenanti, A. Action simulation plays a critical role in deceptive action recognition. J. Neurosci. 2013, 33, 611–623. [Google Scholar] [CrossRef] [Green Version]
- Mc Cabe, S.I.; Villalta, J.I.; Saunier, G.; Grafton, S.T.; Della-Maggiore, V. The relative influence of goal and kinematics on corticospinal excitability depends on the information provided to the observer. Cereb. Cortex 2015, 25, 2229–2237. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gangitano, M.; Mottaghy, F.M.; Pascual-Leone, A. Phase-specific modulation of cortical motor output during movement observation. Neuroreport 2001, 12, 1489–1492. [Google Scholar] [CrossRef] [PubMed]
- Gangitano, M.; Mottaghy, F.M.; Pascual-Leone, A. Modulation of premotor mirror neuron activity during observation of unpredictable grasping movements. Eur. J. Neurosci. 2004, 20, 2193–2202. [Google Scholar] [CrossRef] [Green Version]
- Takahashi, M.; Kamibayashi, K.; Nakajima, T.; Akai, M.; Nakazawa, K. Changes in corticospinal excitability during observation of walking in humans. Neuroreport 2008, 19, 727–731. [Google Scholar] [CrossRef] [PubMed]
- Ito, T.; Tsubahara, A.; Shiraga, Y.; Yoshimura, Y.; Kimura, D.; Suzuki, K.; Hanayama, K. Motor activation is modulated by visual experience during cyclic gait observation: A transcranial magnetic stimulation study. PLoS ONE 2020, 15, e0228389. [Google Scholar] [CrossRef]
- Amoruso, L.; Finisguerra, A. Low or high-level motor coding? The role of stimulus complexity. Front. Hum. Neurosci. 2019, 13, 332. [Google Scholar] [CrossRef]
- Donaldson, P.H.; Gurvich, C.; Fielding, J.; Enticott, P.G. Exploring associations between gaze patterns and putative human mirror neuron system activity. Front. Hum. Neurosci. 2015, 9, 396. [Google Scholar]
- Wright, D.J.; Wood, G.; Franklin, Z.C.; Marshall, B.; Riach, M.; Holmes, P.S. Directing visual attention during action observation modulates corticospinal excitability. PLoS ONE 2018, 13, e0190165. [Google Scholar]
- D’Innocenzo, G.; Nowicky, A.V.; Bishop, D.T. Dynamic task observation: A gaze-mediated complement to traditional action observation treatment? Behav. Brain Res. 2020, 379, 112351. [Google Scholar] [CrossRef]
- D’Innocenzo, G.; Gonzalez, C.C.; Nowicky, A.V.; Williams, A.M.; Bishop, D.T. Motor resonance during action observation is gaze-contingent: A TMS study. Neuropsychologia 2017, 103, 77–86. [Google Scholar] [CrossRef] [PubMed]
- Oldfield, R.C. The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 1971, 9, 97–113. [Google Scholar] [CrossRef]
- Homan, R.W.; Herman, J.; Purdy, P. Cerebral location of international 10–20 system electrode placement. Electroencephalogr. Clin. Neurophysiol. 1987, 66, 376–382. [Google Scholar] [CrossRef]
- Perry, J.; Burnfield, J.M. Ankle-foot complex. In Gait Analysis: Normal and Pathological Function, 2nd ed.; Perry, J., Burnfield, J.M., Eds.; SLACK: West Deptford, NJ, USA, 2010; pp. 51–84. [Google Scholar]
- Bijur, P.E.; Silver, W.; Gallagher, E.J. Reliability of the visual analog scale for measurement of acute pain. Acad. Emerg. Med. 2001, 8, 1153–1157. [Google Scholar] [CrossRef] [PubMed]
- Suso-Martí, L.; León-Hernández, J.V.; La Touche, R.; Paris-Alemany, A.; Cuenca-Martínez, F. Motor imagery and action observation of specific neck therapeutic exercises induced hypoalgesia in patients with chronic neck pain: A randomized single-blind placebo trial. J. Clin. Med. 2019, 8, 1019. [Google Scholar] [CrossRef] [Green Version]
- Mateo, S.; Reilly, K.T.; Collet, C.; Rode, G. Descriptive pilot study of vividness and temporal equivalence during motor imagery training after quadriplegia. Ann. Phys. Rehabil. Med. 2018, 61, 300–308. [Google Scholar] [CrossRef]
- Devanne, H.; Lavoie, B.A.; Capaday, C. Input-output properties and gain changes in the human corticospinal pathway. Exp. Brain Res. 1997, 114, 329–338. [Google Scholar] [CrossRef]
- Leonetti, A.; Puglisi, G.; Siugzdaite, R.; Ferrari, C.; Cerri, G.; Borroni, P. What you see is what you get: Motor resonance in peripheral vision. Exp. Brain Res. 2015, 233, 3013–3022. [Google Scholar] [CrossRef]
- Betti, S.; Castiello, U.; Guerra, S.; Sartori, L. Overt orienting of spatial attention and corticospinal excitability during action observation are unrelated. PLoS ONE 2017, 12, e0173114. [Google Scholar] [CrossRef]
- Puglisi, G.; Leonetti, A.; Cerri, G.; Borroni, P. Attention and cognitive load modulate motor resonance during action observation. Brain Cogn. 2018, 128, 7–16. [Google Scholar] [CrossRef] [PubMed]
- Maranesi, M.; Ugolotti Serventi, F.; Bruni, S.; Bimbi, M.; Fogassi, L.; Bonini, L. Monkey gaze behaviour during action observation and its relationship to mirror neuron activity. Eur. J. Neurosci. 2013, 38, 3721–3730. [Google Scholar] [CrossRef] [PubMed]
- Chong, T.T.; Williams, M.A.; Cunnington, R.; Mattingley, J.B. Selective attention modulates inferior frontal gyrus activity during action observation. Neuroimage 2008, 40, 298–307. [Google Scholar] [CrossRef]
- Muthukumaraswamy, S.D.; Singh, K.D. Modulation of the human mirror neuron system during cognitive activity. Psychophysiology 2008, 45, 896–905. [Google Scholar] [CrossRef] [PubMed]
- Woodruff, C.C.; Klein, S. Attentional distraction, μ-suppression and empathic perspective-taking. Exp. Brain Res. 2013, 229, 507–515. [Google Scholar] [CrossRef]
- Pineda, J.A. The functional significance of mu rhythms: Translating “seeing” and “hearing” into “doing”. Brain Res. Rev. 2005, 50, 57–68. [Google Scholar] [CrossRef] [PubMed]
- Schubert, M.; Curt, A.; Jensen, L.; Dietz, V. Corticospinal input in human gait: Modulation of magnetically evoked motor responses. Exp. Brain Res. 1997, 115, 234–246. [Google Scholar] [CrossRef]
- Capaday, C.; Lavoie, B.A.; Barbeau, H.; Schneider, C.; Bonnard, M. Studies on the corticospinal control of human walking. I. Responses to focal transcranial magnetic stimulation of the motor cortex. J. Neurophysiol. 1999, 81, 129–139. [Google Scholar] [CrossRef]
- Artoni, F.; Fanciullacci, C.; Bertolucci, F.; Panarese, A.; Makeig, S.; Micera, S.; Chisari, C. Unidirectional brain to muscle connectivity reveals motor cortex control of leg muscles during stereotyped walking. Neuroimage 2017, 159, 403–416. [Google Scholar] [CrossRef]
- Byrne, C.A.; O’Keeffe, D.T.; Donnelly, A.E.; Lyons, G.M. Effect of walking speed changes on tibialis anterior EMG during healthy gait for FES envelope design in drop foot correction. J. Electromyogr. Kinesiol. 2007, 17, 605–616. [Google Scholar] [CrossRef] [PubMed]
- Behrendt, F.; Wagner, H.; de Lussanet, M.H. Phase-dependent reflex modulation in tibialis anterior during passive viewing of walking. Acta Psychol. 2013, 142, 343–348. [Google Scholar] [CrossRef]
- Bunday, K.L.; Lemon, R.N.; Kilner, J.M.; Davare, M.; Orban, G.A. Grasp-specific motor resonance is influenced by the visibility of the observed actor. Cortex 2016, 84, 43–54. [Google Scholar] [CrossRef] [PubMed]
Stimulus Conditions | ||||||||
---|---|---|---|---|---|---|---|---|
Baseline | MJ Observation | SJ Observation | R-SJ Observation | Post- Observation | ||||
IC | TO | IC | TO | IC | TO | |||
Median | 0.119 | 0.118 | 0.119 | 0.118 | 0.116 | 0.116 | 0.118 | 0.114 |
(IQR) | (0.112–0.145) | (0.112–0.147) | (0.111–0.147) | (0.111–0.150) | (0.110–0.153) | (0.112–0.147) | (0.113–0.138) | (0.110–0.147) |
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Ito, T.; Kamiue, M.; Kihara, T.; Ishimaru, Y.; Kimura, D.; Tsubahara, A. Visual Attention and Motion Visibility Modulate Motor Resonance during Observation of Human Walking in Different Manners. Brain Sci. 2021, 11, 679. https://doi.org/10.3390/brainsci11060679
Ito T, Kamiue M, Kihara T, Ishimaru Y, Kimura D, Tsubahara A. Visual Attention and Motion Visibility Modulate Motor Resonance during Observation of Human Walking in Different Manners. Brain Sciences. 2021; 11(6):679. https://doi.org/10.3390/brainsci11060679
Chicago/Turabian StyleIto, Tomotaka, Masanori Kamiue, Tomonori Kihara, Yuta Ishimaru, Daisuke Kimura, and Akio Tsubahara. 2021. "Visual Attention and Motion Visibility Modulate Motor Resonance during Observation of Human Walking in Different Manners" Brain Sciences 11, no. 6: 679. https://doi.org/10.3390/brainsci11060679
APA StyleIto, T., Kamiue, M., Kihara, T., Ishimaru, Y., Kimura, D., & Tsubahara, A. (2021). Visual Attention and Motion Visibility Modulate Motor Resonance during Observation of Human Walking in Different Manners. Brain Sciences, 11(6), 679. https://doi.org/10.3390/brainsci11060679