Brain activation associated with active and passive lower limb stepping

Frontiers in Human Neuroscience

Volumn 8, Issue October, 2014, Pages

  Michels, Lars ^c,d   Marchal Crespo, Laura ^a,b   Wolf, Peter ^a,b   Riener, Robert ^a,b   Kollias, Spyros ^c  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

^c UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^d UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

Author keywords

fMRI; Locomotion; Lower limb; MARCOS; Motor control; Robot; Stepping; Supraspinal

Indexed keywords

ADULT; ANTERIOR CINGULATE; ARTICLE; BOLD SIGNAL; BRAIN FUNCTION; FEASIBILITY STUDY; FEMALE; FRONTAL CORTEX; FUNCTIONAL MAGNETIC RESONANCE IMAGING; GAIT; HUMAN; HUMAN EXPERIMENT; JOINT MOBILITY; LEG MOVEMENT; MALE; MOTOR CONTROL; MOTOR PERFORMANCE; NEUROIMAGING; NORMAL HUMAN; PASSIVE MOVEMENT; SENSORIMOTOR CORTEX; SUBCORTEX; TASK PERFORMANCE;

EID: 84933679372     PISSN: None     EISSN: 16625161     Source Type: Journal    
DOI: 10.3389/fnhum.2014.00828     Document Type: Article

References (70)

1. Andersson, J. L., Hutton, C., Ashburner, J., Turner, R., and Friston, K. (2001). Modeling geometric deformations in EPI time series. Neuroimage 13, 903-919. doi: 10.1006/nimg.2001.0746
2. Badesa, F. J., Morales, R., Garcia-Aracil, N., Sabater, J. M., Casals, A., and Zollo, L. (2013). Auto-adaptive robot-aided therapy using machine learning techniques. Comput. Methods Programs Biomed. 116, 123-130. doi: 10.1016/j.cmpb.2013.09.011
3. Bland, J. M., and Altman, D. G. (1996). Statistics notes: measurement error. BMJ 312:1654. doi: 10.1136/bmj.312.7047.1654
4. Brett, M., Anton, J.-L., Valabregue, R., and Poline, J.-B. (2002). “Region of interest analysis using an SPM toolbox,“ in 8th International Conference on Functional MappingoftheHuman Brain (Sendai).
5. Christensen, L. O., Johannsen, P., Sinkjaer, T., Petersen, N., Pyndt, H. S., and Nielsen, J. B. (2000). Cerebral activation during bicycle movements in man. Exp. Brain Res. 135, 66-72. doi: 10.1007/s002210000493
6. Ciccarelli, O., Toosy, A., Marsden, J., Wheeler-Kingshott, C., Sahyoun, C., Matthews, P., et al. (2005). Identifying brain regions for integrative sensorimotor processing with ankle movements. Exp. Brain Res. 166, 31-42. doi: 10.1007/s00221-005-2335-5
7. Coffman, K. A., Dum, R. P., and Strick, P. L. (2011). Cerebellar vermis is a target of projections from the motor areas in the cerebral cortex. Proc. Natl. Acad. Sci. U.S.A. 108, 16068-16073. doi: 10.1073/pnas.1107904108
8. Debaere, F., Swinnen, S. P., Béatse, E., Sunaert, S., Van Hecke, P., and Duysens, J. (2001). Brain areas involved in interlimb coordination: a distributed network. Neuroimage 14, 947-958. doi: 10.1006/nimg.2001.0892
9. Dietz, V. (2003). Spinal cord pattern generators for locomotion. Clin. Neurophysiol. 114, 1379-1389. doi: 10.1016/S1388-2457(03)00120-2
10. Dobkin, B. H., Firestine, A., West, M., Saremi, K., and Woods, R. (2004). Ankle dorsiflexion as an fMRI paradigm to assay motor control for walking during rehabilitation. Neuroimage 23, 370-381. doi: 10.1016/j.neuroimage.2004.06.008
11. Dresel, C., Castrop, F., Haslinger, B., Wohlschlaeger, A. M., Hennenlotter, A., and Ceballos-Baumann, A. O. (2005). The functional neuroanatomy of coordinated orofacial movements: sparse sampling fMRI of whistling. Neuroimage 28, 588-597. doi: 10.1016/j.neuroimage.2005.06.021
12. Duschau-Wicke, A., Caprez, A., and Riener, R. (2010). Patient-cooperative control increases active participation of individuals with SCI during robot-aided gait training. J. Neuroeng. Rehabil. 7:43. doi: 10.1186/1743-0003-7-43
13. Duysens, J., and Van De Crommert, H. W. (1998). Neural control of locomotion; Part 1: the central pattern generator from cats to humans. Gait Posture 7, 131-141. doi: 10.1016/S0966-6362(97)00042-8
14. Ehrsson, H. H., Fagergren, A., and Forssberg, H. (2001). Differential fronto-parietal activation depending on force used in a precision grip task: an fMRI study. J. Neurophysiol. 85, 2613-2623.
15. Eickhoff, S. B., Stephan, K. E., Mohlberg, H., Grefkes, C., Fink, G. R., Amunts, K., et al. (2005). A new SPM toolbox for combining probabilistic cytoarchi- tectonic maps and functional imaging data. Neuroimage 25, 1325-1335. doi: 10.1016/j.neuroimage.2004.12.034
16. Elias, L. J., Bryden, M. P., and Bulman-Fleming, M. B. (1998). Footedness is a better predictor than is handedness of emotional lateralization. Neuropsychologia 36, 37-43. doi: 10.1016/S0028-3932(97)00107-3
17. Field, A. S., Yen, Y.-F., Burdette, J. H., and Elster, A. D. (2000). False cerebral activation on BOLD functional MR images: study of low-amplitude motion weakly correlated to stimulus. ANJR Am. J. Neuroradiol. 21, 1388-1396.
18. Fitzsimmons, N. A., Lebedev, M. A., Peikon, I. D., and Nicolelis, M. A. (2009). Extracting kinematic parameters for monkey bipedal walking from cortical neuronal ensemble activity. Front. Integr. Neurosci. 3:3. doi: 10.3389/neuro.07.003.2009
19. Forman, S. D., Cohen, J. D., Fitzgerald, M., Eddy, W. F., Mintun, M. A., and Noll, D. C. (1995). Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn. Reson. Med. 33, 636-647. doi: 10.1002/mrm.1910330508
20. Francis, S., Lin, X., Aboushoushah, S., White, T. P., Phillips, M., Bowtell, R., et al. (2009). fMRI analysis of active, passive and electrically stimulated ankle dorsiflexion. Neuroimage 44, 469-479. doi: 10.1016/j.neuroimage.2008.09.017
21. Friston, K. J., Holmes, A. P., Worsley, K. J., Poline, J. P., Frith, C. D., and Frackowiak, R. S. J. (1994). Statistical parametric maps in functional imaging: a general linear approach. Hum. Brain Mapp. 2, 189-210. doi: 10.1002/hbm.460020402
22. Friston, K. J., Williams, S., Howard, R., Frackowiak, R. S., and Turner, R. (1996). Movement-related effects in fMRI time-series. Magn. Reson. Med. 35, 346-355. doi: 10.1002/mrm.1910350312
23. Fukuyama, H., Ouchi, Y., Matsuzaki, S., Nagahama, Y., Yamauchi, H., Ogawa, M., et al. (1997). Brain functional activity during gait in normal subjects: a SPECT study. Neurosci. Lett. 228, 183-186. doi: 10.1016/S0304-3940(97)00381-9
24. 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
25. Hall, D. A., Haggard, M. P., Akeroyd, M. A., Palmer, A. R., Summerfield, A. Q., Elliott, M. R., et al. (1999). “Sparse” temporal samplingin auditoryfMRI. Hum. Brain Mapp. 7, 213-223.
26. Harwin, W. S., Patton, J. L., and Edgerton, V. R. (2006). Challenges and opportunities for robot-mediated neurorehabilitation. Proc. IEEE 94, 1717-1726. doi: 10.1109/JPROC.2006.880671
27. Heuninckx, S., Wenderoth, N., and Swinnen, S. P. (2008). Systems neuroplasticity in the aging brain: recruiting additional neural resources for successful motor performance in elderly persons. J. Neurosci. 28, 91-99. doi: 10.1523/JNEUROSCI.3300-07.2008
28. Hollnagel, C., Brugger, M., Vallery, H., Wolf, P., Dietz, V., Kollias, S., et al. (2011). Brain activity during stepping: a novel MRI-compatible device. J. Neurosci. Methods 201, 124-130. doi: 10.1016/j.jneumeth.2011.07.022
29. Hollnagel, C., Vallery, H., Schadler, R., López, I.-L., Jaeger, L., Wolf, P., et al. (2013). Non-linear adaptive controllers for an over-actuated pneumatic MR-compatible stepper. Med. Biol. Eng. Comput. 51, 799-809. doi: 10.1007/s11517-013-1050-9
30. Iseki, K., Hanakawa, T., Shinozaki, J., Nankaku, M., and Fukuyama, H. (2008). Neural mechanisms involved in mental imagery and observation of gait. Neuroimage 41, 1021-1031. doi: 10.1016/j.neuroimage.2008.03.010
31. Jahn, K., Deutschlander, A., Stephan, T., Kalla, R., Wiesmann, M., Strupp, M., et al. (2008). Imaging human supraspinal locomotor centers in brainstem and cerebellum. Neuroimage 39, 786-792. doi: 10.1016/j.neuroimage.2007.09.047
32. Jahn, K., Deutschlander, A., Stephan, T., Strupp, M., Wiesmann, M., and Brandt, T. (2004). Brain activation patterns during imagined stance and locomotion in functional magnetic resonance imaging. Neuroimage 22, 1722-1731. doi: 10.1016/j.neuroimage.2004.05.017
33. Kapreli, E., Athanasopoulos, S., Papathanasiou, M., Van Hecke, P., Strimpakos, N., Gouliamos, A., et al. (2006). Lateralization of brain activity during lower limb joints movement. An fMRI study. Neuroimage 32, 1709-1721. doi: 10.1016/j.neuroimage.2006.05.043
34. Keisker, B., Hepp-Reymond, M. C., Blickenstorfer, A., Meyer, M., and Kollias, S. S. (2009). Differential force scaling of fine-graded power grip force in the sensorimotor network. Hum. Brain Mapp. 30, 2453-2465. doi: 10.1002/hbm.20676
35. Kriegeskorte, N., Simmons, W. K., Bellgowan, P. S., and Baker, C. I. (2009). Circular analysis in systems neuroscience: the dangers of double dipping. Nat. Neurosci. 12, 535-540. doi: 10.1038/nn.2303
36. La Fougere, C., Zwergal, A., Rominger, A., Forster, S., Fesl, G., Dieterich, M., et al. (2010). Real versus imagined locomotion: a [18F]-FDG PET-fMRI comparison. Neuroimage 50, 1589-1598. doi: 10.1016/j.neuroimage.2009.12.060
37. Lemmin, T., Ganesh, G., Gassert, R., Burdet, E., Kawato, M., and Haruno, M. (2010). Model-based attenuation of movement artifacts in fMRI. J. Neurosci. Methods 192, 58-69. doi: 10.1016/j.jneumeth.2010.07.013
38. Liddle, P. F., Kiehl, K. A., and Smith, A. M. (2001). Event-related fMRI study of response inhibition. Hum. Brain Mapp. 12, 100-109. doi: 10.1002/1097-0193(200102)12:2 <100::AID-HBM1007>3.0.C0;2-6
39. Liem, F., Lutz, K., Luechinger, R., Jancke, L., and Meyer, M. (2012). Reducing the interval between volume acquisitions improves “Sparse” scanning protocols in event-related auditory fMRI. Brain Topogr. 25, 182-193. doi: 10.1007/s10548-011-0206-x
40. Malouin, F., Richards, C. L., Jackson, P. L., Dumas, F., and Doyon, J. (2003). Brain activations duringmotorimageryoflocomotor-relatedtasks: aPETstudy. Hum. Brain Mapp. 19, 47-62. doi: 10.1002/hbm.10103
41. Marchal-Crespo, L., Schneider, J., Jaeger, L., and Riener, R. (2014). Learning a locomotor task: with or without errors? J. Neuroeng. Rehabil. 11:25. doi: 10.1186/1743-0003-11-25
42. Margulies, D. S., Kelly, A. M. C., Uddin, L. Q., Biswal, B. B., Castellanos, F. X., and Milham, M. P. (2007). Mapping the functional connectivity of anterior cingulate cortex. Neuroimage 37, 579-588. doi: 10.1016/j.neuroimage.2007.05.019
43. Martinez, M., Villagra, F., Loayza, F., Vidorreta, M., Arrondo, G., Luis, E., et al. (2014). MRI-compatible device for examining brain activation related to stepping. IEEE Trans. Med. Imaging 33, 1044-1053. doi: 10.1109/TMI.2014.2301493
44. Mehta, J. P., Verber, M. D., Wieser, J. A., Schmit, B. D., and Schindler-Ivens, S. M. (2009). A novel technique for examining human brain activity associated with pedaling using fMRI. J. Neurosci. Methods 179, 230-239. doi: 10.1016/j.jneumeth.2009.01.029
45. Mehta, J. P., Verber, M. D., Wieser, J. A., Schmit, B. D., and Schindler- Ivens, S. M. (2012). The effect of movement rate and complexity on functional magnetic resonance signal change during pedaling. Motor Control 16, 158-175.
46. Miall, R. C., and Wolpert, D. M. (1996). Forward models for physiological motor control. Neural Netw. 9, 1265-1279. doi: 10.1016/S0893-6080(96) 00035-4
47. Miyai, I., Suzuki, M., Hatakenaka, M., and Kubota, K. (2006). Effect ofbodyweight support on cortical activation during gait in patients with stroke. Exp. Brain Res. 169, 85-91. doi: 10.1007/s00221-005-0123-x
48. Miyai, I., Tanabe, H. C., Sase, I., Eda, H., Oda, I., Konishi, I., et al. (2001). Cortical mapping of gait in humans: a near-infrared spectroscopic topography study. Neuroimage 14, 1186-1192. doi: 10.1006/nimg.2001.0905
49. Morton, S. M., and Bastian, A. J. (2006). Cerebellar contributions to locomotor adaptations during splitbelt treadmill walking. J. Neurosci. 26, 9107-9116. doi: 10.1523/JNEUROSCI.2622-06.2006
50. Morton, S. M., and Bastian, A. J. (2007). Mechanisms of cerebellar gait ataxia. Cerebellum 6, 79-86. doi: 10.1080/14734220601187741
51. Nichols, T., Brett, M., Andersson, J., Wager, T., and Poline, J. B. (2005). Valid conjunction inference with the minimum statistic. Neurimage 25, 653-660. doi: 10.1016/j.neuroimage.2004.12.005
52. Obhi, S. S., Haggard, P., Taylor, J., and Pascual-Leone, A. (2002). rTMS to the supplementary motor area disrupts bimanual coordination. Motor Control 6, 319-332.
53. Perrachione, T. K., and Ghosh, S. S. (2013). Optimized design and analysis of sparse-sampling fMRI experiments. Front. Neurosci. 7:55. doi: 10.3389/fnins.2013.00055
54. Presacco, A., Forrester, L. W., and Contreras-Vidal, J. L. (2012). Decoding intralimb and inter-limb kinematics during treadmill walking from scalp elec- troencephalographic (EEG) signals. IEEE Trans. Neural Syst. Rehabil. Eng. 20, 212-219. doi: 10.1109/TNSRE.2012.2188304
55. Presacco, A., Goodman, R., Forrester, L., and Contreras-Vidal, J. L. (2011). Neural decoding of treadmill walking from noninvasive electroencephalographic signals. J. Neurophysiol. 106, 1875-1887. doi: 10.1152/jn.00104.201
56. Pruessmann, K. P., Weiger, M., Scheidegger, M. B., and Boesiger, P. (1999). SENSE: sensitivity encoding for fast MRI. Magn. Reson. Med. 42, 952-962.
57. Rubia, K., Russell, T., Overmeyer, S., Brammer, M. J., Bullmore, E. T., Sharma, T., et al. (2001). Mapping motor inhibition: conjunctive brain activations across different versions of go/no-go and stop tasks. Neuroimage 13, 250-261. doi: 10.1006/nimg.2000.0685
58. Sahyoun, C., Floyer-Lea, A., Johansen-Berg, H., and Matthews, P. M. (2004). Towards an understanding of gait control: brain activation during the anticipation, preparation and execution of foot movements. Neuroimage 21, 568-575. doi: 10.1016/j.neuroimage.2003.09.065
59. Schuck, A., Labruyere, R., Vallery, H., Riener, R., and Duschau-Wicke, A. (2012). Feasibility and effects of patient-cooperative robot-aided gait training applied in a 4-week pilot trial. J. Neuroeng. Rehabil. 9:31. doi: 10.1186/17430003-9-31
60. Serrien, D. J., Strens, L. H. A., Oliviero, A., and Brown, P. (2002). Repetitive transcranial magnetic stimulation of the supplementary motor area (SMA) degrades bimanual movement control in humans. Neurosci. Lett. 328, 89-92. doi: 10.1016/S0304-3940(02)00499-8
61. Seto, E., Sela, G., McIroy, W. E., Black, S. E., Staines, W. R., Bronskill, M. J., et al. (2001). Quantifying head motion associated with motor tasks used in fMRI. Neuroimage 14, 284-297. doi: 10.1006/nimg.2001.0829
62. Slotnick, S. D., Moo, L. R., Segal, J. B., and Hart, J. Jr. (2003). Distinct prefrontal cortex activity associated with item memory and source memory for visual shapes. BrainRes. Cogn.BrainRes. 17,75-82. doi: 10.1016/S0926-6410(03)00082-X
63. Sulzer, J., Duenas, J., Stampili, P., Hepp-Reymond, M. C., Kollias, S., Seifritz, E., et al. (2013). “Delineating the whole brain BOLD response to passive movement kinematics,” in IEEE... International Conference on Rehabilitation Robotics: [proceedings] 2013 (Seattle, WA), 1-5.
64. Swinnen, S. P. (2002). Intermanual coordination: from behavioural principles to neural-network interactions. Nat. Rev. Neurosci. 3, 348-359. doi: 10.1038/nrn807
65. Toyomura, A., Shibata, M., and Kuriki, S. (2012). Self-paced and externally triggered rhythmical lower limb movements: a functional MRI study. Neurosci. Lett. 516, 39-44. doi: 10.1016/j.neulet.2012.03.049
66. Weiller, C., Juptner, M., Fellows, S., Rijntjes, M., Leonhardt, G., Kiebel, S., et al. (1996). Brain representation of active and passive movements. Neuroimage 4, 105-110. doi: 10.1006/nimg.1996.0034
67. Williamson, J. W., Nobrega, A. C. L., Mccoll, R., Mathews, D., Winchester, P., Friberg, L., et al. (1997). Activation of the insular cortex during dynamic exercise in humans. J. Physiol. 503, 277-283. doi: 10.1111/j.1469-7793.1997.277bh.x
68. Winter, D. A. (1984). Kinematic and kinetic patterns in human gait: variability and compensating effects. Hum. Mov. Sci. 3, 51-76. doi: 10.1016/0167-9457(84)90005-8
69. Wolbrecht, E. T., Chan, V., Reinkensmeyer, D. J., and Bobrow, J. E. (2008). Optimizing Compliant, Model-Based Robotic Assistance to Promote Neurorehabilitation. IEEE Trans. Neural Syst. Rehabil. Eng. 16, 286-297. doi: 10.1109/TNSRE.2008.918389
70. Zaehle, T., Schmidt, C. F., Meyer, M., Baumann, S., Baltes, C., Boesiger, P., et al. (2007). Comparison of “silent" clustered and sparse temporal fMRI acquisitions in tonal and speech perception tasks. Neuroimage 37, 1195-1204. doi: 10.1016/j.neuroimage.2007.04.073