Loss of balance during balance beam walking elicits a multifocal theta band electrocortical response

Journal of Neurophysiology

Volumn 110, Issue 9, 2013, Pages 2050-2060

  Sipp, Amy R ^a   Gwin, Joseph T ^a   Makeig, Scott ^b   Ferris, Daniel P ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Eeg; Gait; Independent component analysis; Neural control; Source analysis

Indexed keywords

ADULT; ANTERIOR CINGULATE; ARTICLE; BALANCE IMPAIRMENT; BETA RHYTHM; ELECTROENCEPHALOGRAM; ELECTROENCEPHALOGRAPHY; FEMALE; GAIT; HUMAN; INDEPENDENT COMPONENT ANALYSIS; INSULA; MALE; MUSCLE CONTRACTION; NORMAL HUMAN; POSTERIOR CINGULATE; PREFRONTAL CORTEX; PRIORITY JOURNAL; SENSORIMOTOR CORTEX; STEADY STATE; THETA RHYTHM; TREADMILL; VISUAL CORTEX; WALKING;

EEG; GAIT; INDEPENDENT COMPONENT ANALYSIS; NEURAL CONTROL; SOURCE ANALYSIS;

ADOLESCENT; ADULT; FEMALE; HUMANS; MALE; MOTOR CORTEX; POSTURAL BALANCE; SOMATOSENSORY CORTEX; THETA RHYTHM; WALKING;

EID: 84886998076     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00744.2012     Document Type: Article

References (67)

1. Adkin AL, Quant S, Maki BE, McIlroy WE. Cortical responses associated with predictable and unpredictable compensatory balance reactions. Exp Brain Res 172: 85-93, 2006.
2. Ahmed AA, Ashton-Miller JA. Is a "loss of balance" a control error signal anomaly? Evidence for three-sigma failure detection in young adults. Gait Posture 19: 252-262, 2004.
3. Ahmed AA, Ashton-Miller JA. Effect of age on detecting a loss of balance in a seated whole-body balancing task. Clin Biomech (Bristol, Avon) 20: 767-775, 2005.
4. Ahmed AA, Ashton-Miller JA. On use of a nominal internal model to detect a loss of balance in a maximal forward reach. J Neurophysiol 97: 2439-2447, 2007.
5. Akalin Acar Z, Makeig S. Effects of forward model errors on EEG source localization. Brain Topogr 26: 378-396, 2013.
6. Anguera JA, Seidler RD, Gehring WJ. Changes in performance monitoring during sensorimotor adaptation. J Neurophysiol 102: 1868-1879, 2009.
7. Brown LA, Shumway-Cook A, Woollacott MH. Attentional demands and postural recovery: the effects of aging. J Gerontol A Biol Sci Med Sci 54: M165-M171, 1999.
8. Chase CA, Mann K, Wasek S, Arbesman M. Systematic review of the effect of home modification and fall prevention programs on falls and the performance of community-dwelling older adults. Am J Occup Ther 66: 284-291, 2012.
9. Chi YM, Wang YT, Wang Y, Maier C, Jung TP, Cauwenberghs G. Dry and noncontact EEG sensors for mobile brain-computer interfaces. IEEE Trans Neural Syst Rehabil Eng 20: 228-235, 2012.
10. Debener S, Ullsperger M, Siegel M, Fiehler K, von Cramon DY, Engel A. Trial-by-trial coupling of concurrent electroencephalogram and functional magnetic resonance imaging identifies the dynamics of performance monitoring. J Neurosci 25: 11730-11737, 2005.
11. Dehaene S, Posner M, Tucker D. Localization of a neural system for error detection and compensation. Psychol Sci 5: 303-305, 1994.
12. Deliagina TG, Zelenin PV, Orlovsky GN. Physiological and circuit mechanisms of postural control. Curr Opin Neurobiol 22: 646-652, 2012.
13. 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.
14. Delorme A, Palmer J, Onton J, Oostenveld R, Makeig S. Independent EEG sources are dipolar. PLoS One 7: e30135, 2012.
15. Diener HC, Ackermann H, Dichgans J, Guschlbauer B. Medium- and long-latency responses to displacements of the ankle joint in patients with spinal and central lesions. Electroencephalogr Clin Neurophysiol 60: 407-416, 1985.
16. Domingo A, Ferris DP. Effects of physical guidance on short-term learning of walking on a narrow beam. Gait Posture 30: 464-468, 2009.
17. Domingo A, Ferris DP. The effects of error augmentation on learning to walk on a narrow balance beam. Exp Brain Res 206: 359-370, 2010.
18. Faraldo-Garcia A, Santos-Perez S, Crujeiras-Casais R, Labella-Caballero T, Soto-Varela A. Influence of age and gender in the sensory analysis of balance control. Eur Arch Otorhinolaryngol 269: 673-677, 2012.
19. Gard SA, Miff SC, Kuo AD. Comparison of kinematic and kinetic methods for computing the vertical motion of the body center of mass during walking. Hum Mov Sci 22: 597-610, 2004.
20. Gehring W, Liu Y, Orr J, Carp J. The error-related negativity (ERN/Ne). In: The Oxford Handbook of Event-Related Potential Components, edited by Luck S, Kappenman E. New York: Oxford Univ. Press, 2012, p. 231-294.
21. Gramann K, Gwin JT, Ferris DP, Oie K, Jung TP, Lin CT, Liao LD, Makeig S. Cognition in action: imaging brain/body dynamics in mobile humans. Rev Neurosci 22: 593-608, 2011.
22. Gwin JT, Gramann K, Makeig S, Ferris DP. Removal of movement artifact from high-density EEG recorded during walking and running. J Neuro-physiol 103: 3526-3534, 2010.
23. Gwin JT, Gramann K, Makeig S, Ferris DP. Electrocortical activity is coupled to gait cycle phase during treadmill walking. Neuroimage 54: 1289-1296, 2011.
24. Jacobs JV, Fujiwara K, Tomita H, Furune N, Kunita K, Horak FB. Changes in the activity of the cerebral cortex relate to postural response modification when warned of a perturbation. Clin Neurophysiol 119: 1431-1442, 2008.
25. Jacobs JV, Horak FB. Cortical control of postural responses. J Neural Transm 114: 1339-1348, 2007.
26. Jahn K, Zwergal A. Imaging supraspinal locomotor control in balance disorders. Restor Neurol Neurosci 28: 105-114, 2010.
27. Jeka JJ. Light touch contact as a balance aid. Phys Ther 77: 476-487, 1997.
28. Jung TP, Makeig S, Humphries C, Lee TW, McKeown MJ, Iragui V, Sejnowski TJ. Removing electroencephalographic artifacts by blind source separation. Psychophysiology 37: 163-178, 2000a.
29. Jung TP, Makeig S, Westerfield M, Townsend J, Courchesne E, Sejnowski TJ. Removal of eye activity artifacts from visual event-related potentials in normal and clinical subjects. Clin Neurophysiol 111: 1745-1758, 2000b.
30. Kao PC, Lewis CL, Ferris DP. Joint kinetic response during unexpectedly reduced plantar flexor torque provided by a robotic ankle exoskeleton during walking. J Biomech 43: 1401-1407, 2010.
31. Kim H. A dual-subsystem model of the brain's default network: self-referential processing, memory retrieval processes and autobiographical memory retrieval. Neuroimage 61: 966-977, 2012.
32. Lakie M, Loram ID. Manually controlled human balancing using visual, vestibular and proprioceptive senses involves a common, low frequency neural process. J Physiol 577: 403-416, 2006.
33. Liao LD, Wang IJ, Chen SF, Chang JY, Lin CT. Design, fabrication and experimental validation of a novel dry-contact sensor for measuring elec-troencephalography signals without skin preparation. Sensors (Basel) 11: 5819-5834, 2011.
34. Lopez C, Blanke O, Mast FW. The human vestibular cortex revealed by coordinate-based activation likelihood estimation meta-analysis. Neurosci-ence 212: 159-179, 2012.
35. Loram ID, Lakie M. Human balancing of an inverted pendulum: position control by small, ballistic-like, throw and catch movements. J Physiol 540: 1111-1124, 2002.
36. Loram ID, Lakie M, Gawthrop PJ. Visual control of stable and unstable loads: what is the feedback delay and extent of linear time-invariant control? J Physiol 587: 1343-1365, 2009.
37. Luu P, Tucker DM, Derryberry D, Reed M, Poulsen C. Electrophysiolog-ical responses to errors and feedback in the process of action regulation. Psychol Sci 14: 47-53, 2003.
38. Luu P, Tucker DM, Makeig S. Frontal midline theta and the error-related negativity: neurophysiological mechanisms of action regulation. Clin Neu-rophysiol 115: 1821-1835, 2004.
39. Mak MK, Yang F, Pai YC. Limb collapse, rather than instability, causes failure in sit-to-stand performance among patients with Parkinson disease. Phys Ther 91: 381-391, 2011.
40. Makeig S. Auditory event-related dynamics of the EEG spectrum and effects of exposure to tones. Electroencephalogr Clin Neurophysiol 86: 283-293, 1993.
41. Makeig S, Gramann K, Jung TP, Sejnowski TJ, Poizner H. Linking brain, mind and behavior. Int J Psychophysiol 73: 95-100, 2009.
42. Makeig S, Jung TP, Bell AJ, Ghahremani D, Sejnowski TJ. Blind separation of auditory event-related brain responses into independent components. Proc Natl Acad Sci USA 94: 10979-10984, 1997.
43. Maki BE, McIlroy WE. Cognitive demands and cortical control of human balance-recovery reactions. J Neural Transm 114: 1279-1296, 2007.
44. Merfeld DM, Zupan L, Peterka RJ. Humans use internal models to estimate gravity and linear acceleration. Nature 398: 615-618, 1999.
45. Mochizuki G, Sibley KM, Esposito JG, Camilleri JM, McIlroy WE. Cortical responses associated with the preparation and reaction to full-body perturbations to upright stability. Clin Neurophysiol 119: 1626-1637, 2008.
46. Mochizuki G, Sibley KM, Cheung HJ, Camilleri JM, McIlroy WE. Generalizability of perturbation-evoked cortical potentials: independence from sensory, motor and overall postural state. Neurosci Lett 451: 40-44, 2009a.
47. Mochizuki G, Sibley KM, Cheung HJ, McIlroy WE. Cortical activity prior to predictable postural instability: is there a difference between self-initiated and externally-initiated perturbations? Brain Res 1279: 29-36, 2009b.
48. National Center for Injury Prevention and Control. CDC Injury Fact Book. Atlanta, GA: Centers for Disease Control and Prevention, 2006.
49. National Center for Injury Prevention and Control. Preventing Falls: How to Develop Community-Based Fall Prevention Programs for Older Adults. Atlanta, GA: Centers for Disease Control and Prevention, 2008.
50. Onton J, Makeig S. Information-based modeling of event-related brain dynamics. Prog Brain Res 159: 99-120, 2006.
51. 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.
52. Palmer JA, Kreutz-Delgado K, Makeig S. Super-Gaussian mixture source model for ICA. In: Lecture Notes in Computer Science, edited by Rosca J, Erdogmus D, Principe JC, Haykin S. Berlin: Springer, 2006, p. 854-861.
53. Palmer JA, Makeig S, Kreutz-Delgado K, Rao BD. Newton method for the ICA mixture model. In: IEEE International Conference on Acoustics and Signal Processing, p. 1805-1808, 2008.
54. Quant S, Adkin AL, Staines WR, McIlroy WE. Cortical activation following a balance disturbance. Exp Brain Res 155: 393-400, 2004.
55. Rankin JK, Woollacott MH, Shumway-Cook A, Brown LA. Cognitive influence on postural stability: a neuromuscular analysis in young and older adults. J Gerontol A Biol Sci Med Sci 55: M112-M119, 2000.
56. Romo R, de Lafuente V. Conversion of sensory signals into perceptual decisions. Prog Neurobiol 103: 41-75, 2013.
57. Saini M, Kerrigan DC, Thirunarayan MA, Duff-Raffaele M. The vertical displacement of the center of mass during walking: a comparison of four measurement methods. J Biomech Eng 120: 133-139, 1998.
58. Serrien DJ, Ivry RB, Swinnen SP. Dynamics of hemispheric specialization and integration in the context of motor control. Nat Rev Neurosci 7: 160-166, 2006.
59. Shubert TE. Evidence-based exercise prescription for balance and falls prevention: a current review of the literature. J Geriatr Phys Ther 34: 100-108, 2011.
60. Slobounov S, Cao C, Jaiswal N, Newell KM. Neural basis of postural instability identified by VTC and EEG. Exp Brain Res 199: 1-16, 2009.
61. Slobounov S, Hallett M, Cao C, Newell K. Modulation of cortical activity as a result of voluntary postural sway direction: an EEG study. Neurosci Lett 442: 309-313, 2008.
62. Slobounov S, Hallett M, Stanhope S, Shibasaki H. Role of cerebral cortex in human postural control: an EEG study. Clin Neurophysiol 116: 315-323, 2005.
63. Slobounov S, Tutwiler R, Slobounova E, Rearick M, Ray W. Human oscillatory brain activity within gamma band (30-50 Hz) induced by visual recognition of non-stable postures. Brain Res Cogn Brain Res 9: 177-192, 2000.
64. Slobounov S, Wu T, Hallett M. Neural basis subserving the detection of postural instability: an fMRI study. Motor Control 10: 69-89, 2006.
65. Sozzi S, Do MC, Monti A, Schieppati M. Sensorimotor integration during stance: processing time of active or passive addition or withdrawal of visual or haptic information. Neuroscience 212: 59-76, 2012.
66. Wagner J, Solis-Escalante T, Grieshofer P, Neuper C, Muller-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.
67. Yang F, Bhatt T, Pai YC. Limits of recovery against slip-induced falls while walking. J Biomech 44: 2607-2613, 2011.