Restricted vision increases sensorimotor cortex involvement in human walking

Anderson S Oliveira, Bryan R Schlink, W David Hairston, Peter König, Daniel P Ferris, Anderson S Oliveira, Bryan R Schlink, W David Hairston, Peter König, Daniel P Ferris

Abstract

This study aimed to determine whether there is electrocortical evidence of augmented participation of sensory brain areas in walking modulation during walking with eyes closed. Healthy subjects (n = 10) walked on a treadmill at 1 m/s while alternating 5 min of walking with the eyes open or closed while we recorded ground reaction forces (GRFs) and high-density scalp electroencephalography (EEG). We applied independent component analysis to parse EEG signals into maximally independent component (IC) processes and then computed equivalent current dipoles for each IC. We clustered cortical source ICs and analyzed event-related spectral perturbations synchronized to gait events. Our results indicated that walking with eyes closed reduced the first peak of the vertical GRFs and induced shorter stride duration. Regarding the EEG, we found that walking with eyes closed induced significantly increased relative theta desynchronization in the frontal and premotor cortex during stance, as well as greater desynchronization from theta to beta bands during transition to single support for both left and right somatosensory cortex. These results suggest a phase-specific increased participation of brain areas dedicated to sensory processing and integration when vision is not available for locomotor guidance. Furthermore, the lack of vision demands higher neural processing related to motor planning and execution. Our findings provide evidence supporting the use of eyes-closed tasks in clinical practice, such as gait rehabilitation and improvements in balance control, as there is higher demand for additional sensory integration for achieving postural control.NEW & NOTEWORTHY We measured electrocortical dynamics in sighted individuals while walking with eyes open and eyes closed to induce the participation of other sensory systems in postural control. Our findings show that walking with visual restriction increases the participation of brain areas dedicated to sensory processing, motor planning, and execution. These results confirm the essential participation of supraspinal inputs to postural control in human locomotion, supporting the use of eyes-closed tasks in clinical practice.

Keywords: EEG; eyes closed; independent component analysis; sensory reweighting; walking.

Copyright © 2017 the American Physiological Society.

Figures

Fig. 1.
Fig. 1.
A: ground reaction force (GRF) from illustrative subject while treadmill walking with eyes open and eyes closed. Thick traces represent averaged GRF, and shaded areas represent ±1 standard deviation for the right and left legs. B: stride duration and 1st GRF peak during walking with eyes open and eyes closed. *Significant difference in relation to eyes closed condition (P < 0.01).
Fig. 2.
Fig. 2.
Top: electrocortical clusters of independent components plotted on the MNI brain. Each blue sphere represents 1 independent component, and the red sphere represents the centroid location for the clusters representing medial prefrontal cortex (A), medial premotor and supplementary motor cortex (B), left somatosensory cortex (C), and right somatosensory cortex (D). Bottom: for each cluster we show grand-average, significance-masked (P < 0.05) ERSPs for eyes closed and eyes open conditions as well as for the subtraction eyes open − eyes closed condition. Nonsignificant values set to zero (green). All plots represent 1 gait cycle from right heel strike (RHS) to RHS, with left toe-off (LTO), left heel strike (RTO), and right toe-off (RTO) designated by dashed vertical lines.
Fig. 3.
Fig. 3.
Mean (SD) ERSP power during double-support phase from clusters located at the prefrontal cortex, premotor cortex, and left and right somatosensory cortex for the eyes open and eyes closed conditions. EEG power spectrum was segmented in 4 blocks representing 1–25% (25%), 26–50% (50%), 51–75% (75%), and 76–100% (100%) of total experiment duration. *Significant difference (P < 0.05) in relation to 100%; †significant difference (P < 0.05) in relation to 75%; ‡significant difference (P < 0.05) in relation to 50%.
Fig. 4.
Fig. 4.
Mean (SD) ERSP power during right stance phase from clusters located at the prefrontal cortex, premotor cortex, and left and right somatosensory cortex for the eyes open and eyes closed conditions. EEG power spectrum was segmented in 4 blocks representing 1–25% (25%), 26–50% (50%), 51–75% (75%), and 76–100% (100%) of total experiment duration. *Significant difference (P < 0.05) in relation to 100%; ‡significant difference (P < 0.05) in relation to 50%.

References

    1. Assländer L, Peterka RJ. Sensory reweighting dynamics in human postural control. J Neurophysiol 111: 1852–1864, 2014. doi:10.1152/jn.00669.2013.
    1. Bauby CE, Kuo AD. Active control of lateral balance in human walking. J Biomech 33: 1433–1440, 2000. doi:10.1016/S0021-9290(00)00101-9.
    1. Bernal B, Perdomo J. Brodmann’s Interactive Atlas [Online]. 2008. [3 Jan. 2016].
    1. Bolton DA, Brown KE, McIlroy WE, Staines WR. Transient inhibition of the dorsolateral prefrontal cortex disrupts somatosensory modulation during standing balance as measured by electroencephalography. Neuroreport 23: 369–372, 2012. doi:10.1097/WNR.0b013e328352027c.
    1. Bradford JC, Lukos JR, Ferris DP. Electrocortical activity distinguishes between uphill and level walking in humans. J Neurophysiol 115: 958–966, 2016. doi:10.1152/jn.00089.2015.
    1. Bruijn SM, Van Dieën JH, Daffertshofer A. Beta activity in the premotor cortex is increased during stabilized as compared to normal walking. Front Hum Neurosci 9: 593, 2015. doi:10.3389/fnhum.2015.00593.
    1. Chaumon M, Bishop DV, Busch NA. A practical guide to the selection of independent components of the electroencephalogram for artifact correction. J Neurosci Methods 250: 47–63, 2015. doi:10.1016/j.jneumeth.2015.02.025.
    1. Cho SY, Ryu YU, Je HD, Jeong JH, Ma SY, Kim HD. Effects of illumination on toe clearance and gait parameters of older adults when stepping over an obstacle: a pilot study. J Phys Ther Sci 25: 229–232, 2013. doi:10.1589/jpts.24.229.
    1. Collins SH, Kuo AD. Two independent contributions to step variability during over-ground human walking. PLoS One 8: e73597, 2013. doi:10.1371/journal.pone.0073597.
    1. Crone NE, Miglioretti DL, Gordon B, Sieracki JM, Wilson MT, Uematsu S, Lesser RP. Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. Brain 121: 2271–2299, 1998. doi:10.1093/brain/121.12.2271.
    1. Delorme A, Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 134: 9–21, 2004. doi:10.1016/j.jneumeth.2003.10.009.
    1. Gramann K, Gwin JT, Bigdely-Shamlo N, Ferris DP, Makeig S. Visual evoked responses during standing and walking. Front Hum Neurosci 4: 202, 2010. doi:10.3389/fnhum.2010.00202.
    1. Gwin JT, Gramann K, Makeig S, Ferris DP. Removal of movement artifact from high-density EEG recorded during walking and running. J Neurophysiol 103: 3526–3534, 2010. doi:10.1152/jn.00105.2010.
    1. Gwin JT, Gramann K, Makeig S, Ferris DP. Electrocortical activity is coupled to gait cycle phase during treadmill walking. Neuroimage 54: 1289–1296, 2011. doi:10.1016/j.neuroimage.2010.08.066.
    1. Hallemans A, Beccu S, Van Loock K, Ortibus E, Truijen S, Aerts P. Visual deprivation leads to gait adaptations that are age- and context-specific. II. Kinematic parameters. Gait Posture 30: 307–311, 2009. doi:10.1016/j.gaitpost.2009.05.017.
    1. Hallemans A, Ortibus E, Meire F, Aerts P. Low vision affects dynamic stability of gait. Gait Posture 32: 547–551, 2010. doi:10.1016/j.gaitpost.2010.07.018.
    1. Halsband U, Ito N, Tanji J, Freund HJ. The role of premotor cortex and the supplementary motor area in the temporal control of movement in man. Brain 116: 243–266, 1993. doi:10.1093/brain/116.1.243.
    1. Hüfner K, Stephan T, Flanagin VL, Deutschländer A, Stein A, Kalla R, Dera T, Fesl G, Jahn K, Strupp M, Brandt T. Differential effects of eyes open or closed in darkness on brain activation patterns in blind subjects. Neurosci Lett 466: 30–34, 2009. doi:10.1016/j.neulet.2009.09.010.
    1. Jung TP, Makeig S, McKeown MJ, Bell AJ, Lee TW, Sejnowski TJ. Imaging brain dynamics using independent component analysis. Proc IEEE Inst Electr Electron Eng 89: 1107–1122, 2001. doi:10.1109/5.939827.
    1. Kelly R, Mizelle JC, Wheaton LA. Distinctive laterality of neural networks supporting action understanding in left- and right-handed individuals: an EEG coherence study. Neuropsychologia 75: 20–29, 2015. doi:10.1016/j.neuropsychologia.2015.05.016.
    1. Kersting UG. Regulation of impact forces during treadmill running. Footwear Sci 3: 59–68, 2011. doi:10.1080/19424280.2011.552074.
    1. Kim TW, Kim YW. Treadmill sideways gait training with visual blocking for patients with brain lesions. J Phys Ther Sci 26: 1415–1418, 2014. doi:10.1589/jpts.26.1415.
    1. Kim YW, Moon SJ. Effects of treadmill training with the eyes closed on gait and balance ability of chronic stroke patients. J Phys Ther Sci 27: 2935–2938, 2015. doi:10.1589/jpts.27.2935.
    1. Koenraadt KL, Roelofsen EG, Duysens J, Keijsers NL. Cortical control of normal gait and precision stepping: an fNIRS study. Neuroimage 85: 415–422, 2014. doi:10.1016/j.neuroimage.2013.04.070.
    1. Lau TM, Gwin JT, Ferris DP. Walking reduces sensorimotor network connectivity compared to standing. J Neuroeng Rehabil 11: 14, 2014. doi:10.1186/1743-0003-11-14.
    1. Lloyd D. Scanning the Neurocracy: What Do Brodmann Areas Do? [Online]. 2007. [3 Jan. 2016].
    1. Maeda RS. O’Connor SM, Donelan JM, Marigold DS. Foot placement relies on state estimation during visually guided walking. J Neurophysiol 117: 480–491, 2017. doi:10.1152/jn.00015.2016.
    1. Makeig S. Auditory event-related dynamics of the EEG spectrum and effects of exposure to tones. Electroencephalogr Clin Neurophysiol 86: 283–293, 1993. doi:10.1016/0013-4694(93)90110-H.
    1. Makeig S, Bell JA, Jung TP, Sejnowski TJ. Independent component analysis of electroencephalographic data. Adv Neural Inf Process Syst 8: 145–151, 1996.
    1. Moon SJ, Kim YW. Effect of blocked vision treadmill training on knee joint proprioception of patients with chronic stroke. J Phys Ther Sci 27: 897–900, 2015. doi:10.1589/jpts.27.897.
    1. Nakamura T. Quantitative analysis of gait in the visually impaired. Disabil Rehabil 19: 194–197, 1997. doi:10.3109/09638289709166526.
    1. Nashner L, Berthoz A. Visual contribution to rapid motor responses during postural control. Brain Res 150: 403–407, 1978. doi:10.1016/0006-8993(78)90291-3.
    1. Oliveira AS, Farina D, Kersting UG. Biomechanical strategies to accommodate expected slips in different directions during walking. Gait Posture 36: 301–306, 2012a. doi:10.1016/j.gaitpost.2012.03.016.
    1. Oliveira AS, Gizzi L, Kersting UG, Farina D. Modular organization of balance control following perturbations during walking. J Neurophysiol 108: 1895–1906, 2012b. doi:10.1152/jn.00217.2012.
    1. Oliveira AS, Schlink BR, Hairston WD, König P, Ferris DP. Induction and separation of motion artifacts in EEG data using a mobile phantom head device. J Neural Eng 13: 036014, 2016. doi:10.1088/1741-2560/13/3/036014.
    1. Oliveira AS, Schlink BR, Hairston WD, König P, Ferris DP. A channel rejection method for attenuating motion-related artefacts in EEG recordings during walking. Front Neurosci 11: 225, 2017. doi:10.3389/fnins.2017.00225.
    1. Oostenveld R, Oostendorp TF. Validating the boundary element method for forward and inverse EEG computations in the presence of a hole in the skull. Hum Brain Mapp 17: 179–192, 2002. doi:10.1002/hbm.10061.
    1. Peterka RJ. Sensorimotor integration in human postural control. J Neurophysiol 88: 1097–1118, 2002.
    1. Peterka RJ, Benolken MS. Role of somatosensory and vestibular cues in attenuating visually induced human postural sway. Exp Brain Res 105: 101–110, 1995. doi:10.1007/BF00242186.
    1. Petersen TH, Willerslev-Olsen M, Conway BA, Nielsen JB. The motor cortex drives the muscles during walking in human subjects. J Physiol 590: 2443–2452, 2012. doi:10.1113/jphysiol.2012.227397.
    1. Radovanovic S, Korotkov A, Ljubisavljevic M, Lyskov E, Thunberg J, Kataeva G, Danko S, Roudas M, Pakhomov S, Medvedev S, Johansson H. Comparison of brain activity during different types of proprioceptive inputs: a positron emission tomography study. Exp Brain Res 143: 276–285, 2002. doi:10.1007/s00221-001-0994-4.
    1. Rossignol S, Dubuc R, Gossard JP. Dynamic sensorimotor interactions in locomotion. Physiol Rev 86: 89–154, 2006. doi:10.1152/physrev.00028.2005.
    1. Sadeghi H, Allard P, Prince F, Labelle H. Symmetry and limb dominance in able-bodied gait: a review. Gait Posture 12: 34–45, 2000. doi:10.1016/S0966-6362(00)00070-9.
    1. Schmid M, Nardone A, De Nunzio AM, Schmid M, Schieppati M. Equilibrium during static and dynamic tasks in blind subjects: no evidence of cross-modal plasticity. Brain 130: 2097–2107, 2007. doi:10.1093/brain/awm157.
    1. Seeber M, Scherer R, Wagner J, Solis-Escalante T, Müller-Putz GR. EEG beta suppression and low gamma modulation are different elements of human upright walking. Front Hum Neurosci 8: 485, 2014. [Erratum. Front Hum Neurosci 9: 542, 2015]. doi:10.3389/fnhum.2014.00485.
    1. Sinclair J, Hobbs SJ, Protheroe L, Edmundson CJ, Greenhalgh A. Determination of gait events using an externally mounted shank accelerometer. J Appl Biomech 29: 118–122, 2013. doi:10.1123/jab.29.1.118.
    1. Sipp AR, Gwin JT, Makeig S, Ferris DP. Loss of balance during balance beam walking elicits a multifocal theta band electrocortical response. J Neurophysiol 110: 2050–2060, 2013. doi:10.1152/jn.00744.2012.
    1. Snyder KL, Kline JE, Huang HJ, Ferris DP. Independent component analysis of gait-related movement artifact recorded using EEG electrodes during treadmill walking. Front Hum Neurosci 9: 639, 2015. doi:10.3389/fnhum.2015.00639.
    1. Suzuki M, Miyai I, Ono T, Oda I, Konishi I, Kochiyama T, Kubota K. Prefrontal and premotor cortices are involved in adapting walking and running speed on the treadmill: an optical imaging study. Neuroimage 23: 1020–1026, 2004. doi:10.1016/j.neuroimage.2004.07.002.
    1. Uematsu A, Inoue K, Hobara H, Kobayashi H, Iwamoto Y, Hortobágyi T, Suzuki S. Preferred step frequency minimizes veering during natural human walking. Neurosci Lett 505: 291–293, 2011. doi:10.1016/j.neulet.2011.10.057.
    1. Wagner J, Makeig S, Gola M, Neuper C, Müller-Putz G. Distinct β band oscillatory networks subserving motor and cognitive control during gait adaptation. J Neurosci 36: 2212–2226, 2016. doi:10.1523/JNEUROSCI.3543-15.2016.
    1. Wagner J, Solis-Escalante T, Grieshofer P, Neuper C, Müller-Putz G, Scherer R. Level of participation in robotic-assisted treadmill walking modulates midline sensorimotor EEG rhythms in able-bodied subjects. Neuroimage 63: 1203–1211, 2012. doi:10.1016/j.neuroimage.2012.08.019.
    1. Wagner J, Solis-Escalante T, Scherer R, Neuper C, Müller-Putz G. It’s how you get there: walking down a virtual alley activates premotor and parietal areas. Front Hum Neurosci 8: 93, 2014. doi:10.3389/fnhum.2014.00093.
    1. Wuehr M, Schniepp R, Schlick C, Huth S, Pradhan C, Dieterich M, Brandt T, Jahn K. Sensory loss and walking speed related factors for gait alterations in patients with peripheral neuropathy. Gait Posture 39: 852–858, 2014. doi:10.1016/j.gaitpost.2013.11.013.
    1. Zeni JA Jr, Richards JG, Higginson JS. Two simple methods for determining gait events during treadmill and overground walking using kinematic data. Gait Posture 27: 710–714, 2008. doi:10.1016/j.gaitpost.2007.07.007.

Source: PubMed

Sponsorer og samarbejdspartnere

Medicinske tilstande

Narkotikainterventioner

3
Abonner