EEG beta suppression and low gamma modulation are different elements of human upright walking

Frontiers in Human Neuroscience

Volumn 8, Issue JULY, 2014, Pages

  Seeber, Martin ^a,b   Scherer, Reinhold ^a,b,c   Wagner, Johanna ^a,b   Solis Escalante, Teodoro ^a,b,d   Müller Putz, Gernot R ^a,b  

^a UNIVERSITY OF GRAZ   (Austria)

^b BIOTECHMED GRAZ   (Austria)

^c Judendorf Strassengel   (Austria)

^d DELFT UNIVERSITY OF TECHNOLOGY   (Netherlands)

Author keywords

Brain mapping; Electroencephalography (EEG); Gait; Magnetic resonance imaging; Motor cortex

Indexed keywords

ADULT; AMPLITUDE MODULATION; ARTICLE; BRAIN REGION; CONTROLLED STUDY; ELECTROENCEPHALOGRAPHY; ELECTROENCEPHALOGRAPHY PHASE SYNCHRONIZATION; EVOKED RESPONSE; FEMALE; FUNCTIONAL NEUROIMAGING; GAIT PHASE MODULATION; HUMAN; HUMAN EXPERIMENT; MALE; NEUROMODULATION; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OSCILLATION; STANDING; TASK PERFORMANCE; WALKING;

EID: 84904036918     PISSN: None     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2014.00485     Document Type: Article

References (49)

1. Baillet, S., Mosher, J. C., and Leahy, R. M. (2001). Electromagnetic brain mapping. IEEE Signal Process. Mag. 18, 14-30. doi: 10.1109/79.962275
2. Brodbeck, V., Spinelli, L., Lascano, A. M., Wissmeier, M., Vargas, M. I., Vulliemoz, S., et al. (2011). Electroencephalographic source imaging: a prospective study of 152 operatedepileptic patients. Brain 134, 2887-2897. doi: 10.1093/brain/awr243
3. Brown, P. (2007). Abnormal oscillatory synchronisation in the motor system leads to impaired movement. Curr. Opin. Neurobiol. 17, 656-664. doi: 10.1016/j.conb.2007.12.001
4. Buzsaki, G., and Draguhn, A. (2004). Neuronal oscillations in cortical networks. Science 304, 1926-1929. doi: 10.1126/science.1099745
5. Canolty, R. T., Edwards, E., Dalal, S. S., Soltani, M., Nagarajan, S. S., Kirsch, H. E., et al. (2006). High gamma power is phase-locked to theta oscilla tions in human neocortex. Science 313, 1626-1628. doi: 10.1126/science. 1128115
6. Canolty, R. T., Ganguly, K., Kennerley, S. W., Cadieu, C. F., Koepsell, K., Wallis, J. D., et al. (2010). Oscillatory phase coupling coordinates anatomically dispersed functional cell assemblies. Proc. Natl. Acad. Sci. U.S.A. 107, 17356-17361. doi: 10.1073/pnas.1008306107
7. Castermans, T., Duvinage, M., Cheron, G., and Dutoit, T. (2014). About the cortical origin of the low-delta and high-gamma rhythms observed in EEG signals dur ing treadmill walking. Neurosci. Lett. 561, 166-170. doi: 10.1016/j.neulet.2013. 12.059
8. Crone, N. E., Miglioretti, D. L., Gordon, B., Sieracki, J. M., Wilson, M. T., Uematsu, S., et al. (1998). Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event- related desynchronization. Brain 121, 2271-2299. doi: 10.1093/brain/121. 12.2301
9. Dale, A., Fischl, B., and Sereno, M. I. (1999). Cortical surface-based analy sis. I. Segmentation and surface reconstruction. Neuroimage 9, 179-194. doi: 10.1006/nimg.1998.0395
10. Darvas, F., Pantazis, D., Kucukaltun-Yildirim, E., and Leahy, R. M. (2004). Mapping human brain function with MEG and EEG: methods and validation. Neuroimage 23, 289-299. doi: 10.1016/j.neuroimage.2004.07.014
11. Engel, A. K., and Fries, P. (2010). Beta-band oscillations: signalling the status quo? Curr. Opin. Neurobiol. 20, 156-165. doi: 10.1016/j.conb.2010.02.015
12. Fischl, B. (2012). FreeSurfer. Neuroimage 62, 774-781. doi: 10.1016/j.neuroimage. 2012.01.021
13. Fries, P. (2009). Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu. Rev. Neurosci. 32, 209-224. doi: 10.1146/annurev.neuro.051508.135603
14. Fries, P., Nikolic, D., and Singer, W. (2007). The gamma cycle. Trends Neurosci. 30, 309-316. doi: 10.1016/j.tins.2007.05.005
15. Gilbertson, T., Lalo, E., Doyle, L., Di Lazzaro, V., Cioni, B., and Brown, P. (2005). Existing motor state is favored at the expense of new movement during 13 35 Hz oscillatory synchrony in the human corticospinal system. J. Neurosci. 25, 7771-7779. doi: 10.1523/JNEUR0SCI.1762-05.2005
16. Gramfort, A., Papadopoulo, T., Olivi, E., and Clerc, M. (2010). OpenMEEG: open- sourcesoftwareforquasistaticbioelectromagnetics. Biomed. Eng. Online 45, 1-20. doi: 10.1186/1475-925X-9-45
17. Gwin, J. T., and Ferris, D. P. (2012). Beta- and gamma-range human lower limb corticomuscular coherence. Front. Hum. Neurosci. 6:258. doi: 10.3389/fnhum.2012.00258
18. Gwin, J. T., Gramann, K., Makeig, S., and Ferris, D. P. (2011). Electrocortical activity is coupled to gait cycle phase during treadmill walking. Neuroimage 54, 1289-1296. doi: 10.1016/j.neuroimage.2010.08.066
19. Hidler, J. M., and Wall, A. E. (2005). Alterations in muscle activation pat terns during robotic-assisted walking. Clin. Biomech. 20, 184-193. doi: 10.1016/j.clinbiomech.2004.09.016
20. Hidler, J. M., Wisman, W., and Neckel, N. (2008). Kinematic trajectories while walk ing within the Lokomat robotic gait-orthosis. Clin. Biomech. 23, 1251-1259. doi: 10.1016/j.clinbiomech.2008. 08.004
21. Jasper, H., and Penfield, W. (1949). Electrocorticograms in man: effect of volun tary movement upon the electrical activity of the precentral gyrus. Eur. Arch. Psychiatry Clin. Neurol. 183, 163-174.
22. Jenkinson, N., and Brown, P. (2011). New insights into the relationship between dopamine, beta oscillations and motor function. Trends Neurosci. 34, 611-618. doi: 10.1016/j.tins.2011.09.003
23. Kybic, J., Clerc, M., Abboud, T., Faugeras, O., Keriven, R., and Papadopoulo, T. (2005). A common formalism for the integral formulations of the forward EEG problem. IEEE Trans. Med. Imaging 24, 12-28. doi: 10.1109/TMI.2004. 837363
24. Maris, E., and Oostenveld, R. (2007). Nonparametric statistical test ing of EEG and MEG-data. J. Neurosci. Methods 164, 177-190. doi: 10.1016/j.jneumeth.2007.03.024
25. Marsden, J. F., Werhahn, K. J., Ashby, P., Rothwell, J., Noachtar, S., and Brown, P. (2000). Organization of cortical activities related to movement in humans. J. Neurosci. 20, 2307-2314.
26. Michel, C. M., and Murray, M. M. (2012). Towards the utilization of EEG as a brain imaging tool. Neuroimage 61, 371-385. doi: 10.1016/j.neuroimage.2011. 12.039
27. Michel, C. M., Murray, M. M., Lantz, G., Gonzalez, S., Spinelli, L., and Grave de Peralta, R. (2004). EEG source imaging. Clin. Neurophysiol. 115, 2195-2222. doi: 10.1016/j.clinph.2004.06.001
28. Miller, K. J., Leuthardt, E. C., Schalk, G., Rao, R. P. N., Anderson, N. R., Moran, D. W., et al. (2007). Spectral changes in cortical surface potentials during motor movement. J. Neurosci. 27, 2424-2432. doi: 10.1523/JNEUROSCI.3886- 06.2007
29. Morlet, J., Arens, G., Fourgenau, E., and Glard, D. (1982). Wave propagation and sampling theory-Part I: complex signal and scattering in multilayered media. Geophysics 47, 222-236. doi: 10.1190/1.1441328
30. Müller-Putz, G. R., Zimmermann, D., Grainmann, B., Nestinger, K., Korisek, G., and Pfurtscheller, G. (2007). Event-related beta EEG-changes during passive and attempted foot movements in paraplegic patients. Brain Res. 1137, 84-91. doi: 10.1016/j.brainres.2006.12.052
31. Nichols, T. E., and Holmes, A. P. (2001). Nonparametric permutation tests for functional neuroimaging: a primer with examples. Hum. Brain Mapp. 15, 1-25. doi: 10.1002/hbm.1058
32. Omlor, W., Patino, L., Hepp-Reymond, M. C., and Kristeva, R. (2007). Gamma range corticomuscular coherence during dynamic force output. Neuroimage 34, 1191-1198. doi: 10.1016/j.neuroimage.2006.10.018
33. Oostenveld, R., and Praamstra, P. (2001). The five percent electrode system for high-resolution EEG and ERP measurements. Clin. Neurophysiol. 112, 713-719. doi: 10.1016/S1388-2457(00)00527-7
34. Pascual-Marqui, R. D. (2002). Standardized low resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find. Exp. Clin. Pharmacol. 24(Suppl. D), 5-12.
35. Petersen, T. H., Willerslev-Olsen, M., Conway, B. A., and Nielsen, J. B. (2012). The motor cortex drives the muscles during walking in human subjects. J. Physiol. 590, 2443-2452. doi: 10.1113/jphysiol.2012.227397
36. Pfurtscheller, G., and Aranibar, A. (1977). Event-related cortical desynchroniza tion detected by power measurements of scalp EEG. Electroencephalogr. Clin. Neurophysiol. 42, 817-826. doi: 10.1016/0013-4694(77)90235-8
37. Pfurtscheller, G., and Lopes da Silva, F. H. (1999). Event-related EEG/MEG syn chronization and desynchronization: basic principles. Clin. Neurophysiol. 110, 1842-1857. doi: 10.1016/S1388-2457(99)00141-8
38. Pfurtscheller, G., and Neuper, C. (1997). Motor imagery activates primary sensorimotor area in humans. Neurosci. Lett. 239, 65-68. doi: 10.1016/S0304- 3940(97)00889-6
39. Pfurtscheller, G., Neuper, C., Andrew, C., and Edlinger, G. (1997). Foot and hand area mu rhythms. Int. J. Psychophysiol. 26, 121-135. doi: 10.1016/S0167- 8760(97)00760-5
40. Pfurtscheller, G., Stancak, A. Jr., and Neuper, C. (1996). Post-movement beta synchronization. A correlate of an idling motor area? Electroencephalogr. Clin. Neurophysiol. 98, 281-293. doi: 10.1016/0013-4694(95)00258-8
41. Pogosyan, A., Gaynor, L. D., Eusebio, A., and Brown, P. (2009). Boosting cortical activity at beta-band frequencies slows movement in humans. Curr. Biol. 19, 1637-1641. doi: 10.1016/j.cub.2009.07.074
42. Severens, M., Nienhuis, B., Desain, P., and Duysens, J. (2012). Feasibility of measuring event related desynchronization with electroencephalography dur ing walking. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2012, 2764-2767. doi: 10.1109/EMBC.2012.6346537
43. Schnitzler, A., and Gross, J. (2005). Normal and pathological oiscillatory com munication in the brain. Nat. Rev. Neurosci. 6, 285-296. doi: 10.1038/ nrn1650
44. Siegel, M., Donner, T. H., and Engel, A. K. (2012). Spectral fingerprints of large- scale neuronal interactions. Nat. Rev. Neurosci. 13, 121-134. doi: 10.1038/ nrn3137
45. Solis-Escalante, T., Müller-Putz, G. R., Pfurtscheller, P., and Neuper, C. (2012). Cue-induced beta rebound during withholding of overt and covert foot movement. Clin. Neurophysiol. 123, 1182-1190. doi: 10.1016/j.clinph.2012. 01.013
46. Tadel, F., Baillet, S., Mosher, J. C., Pantazis, D., and Leahy, R. M.(2011). Brainstorm: a user-friendly application for MEG/EEG analysis. Comput. Intell. Neurosci. 2011:879716. doi: 10.1155/2011/879716
47. Tallon-Baudry, C., and Bertrand, O. (1999). Oscillatory gamma activityin humans and its role in object representation. Trends Cogn. Sci. 3, 151-162. doi: 10.1016/S1364-6613(99)01299-1
48. Wagner, J., Solis-Escalante, T., Grieshofer, P., Neuper, C., Müller-Putz, G. R., and Scherer, R. (2012). Level of participation in robotic-assisted treadmill walking modulates midline sensorimotor EEG rhythms in able bodied subjects. Neuroimage 63, 1203-1211. doi: 10.1016/j.neuroimage.2012. 08.019
49. Wagner, J., Solis-Escalante, T., Scherer, R., Neuper, C., and Mller-Putz, G. R. (2014). It's howyou get there: walking downavirtual alleyactivates premotor andparietal areas. Front. Hum. Neurosci. 8:93. doi: 10.3389/fnhum.2014.00093