Abstract
Although several features of brain motor function appear to be preserved even in chronic complete SCI, previous functional MRI (fMRI) studies have also identified significant derangements such as a strongly reduced volume of activation, a poor modulation of function and abnormal activation patterns. It might be speculated that extensive motor imagery training may serve to prevent such abnormalities. We here report on a unique patient with a complete traumatic SCI below C5 who learned to elicit electroencephalographic signals β-bursts in the midline region upon imagination of foot movements. This enabled him to use a neuroprosthesis and to “walk from thought” in a virtual environment via a brain–computer interface (BCI). We here used fMRI at 3T during imagined hand and foot movements to investigate the effects of motor imagery via persistent BCI training over 8 years on brain motor function and compared these findings to a group of five untrained healthy age-matched volunteers during executed and imagined movements. We observed robust primary sensorimotor cortex (SMC) activity in expected somatotopy in the tetraplegic patient upon movement imagination while such activation was absent in healthy untrained controls. Sensorimotor network activation with motor imagery in the patient (including SMC contralateral to and the cerebellum ipsilateral to the imagined side of movement as well as supplementary motor areas) was very similar to the pattern observed with actual movement in the controls. We interpret our findings as evidence that BCI training as a conduit of motor imagery training may assist in maintaining access to SMC in largely preserved somatopy despite complete deafferentation.
Similar content being viewed by others
References
Alkadhi H, Brugger P, Boendermaker SH, Crelier G, Curt A, Hepp-Reymond M-C, Kollias SS (2005) What disconnection tells about motor imagery: evidence from paraplegic patients. Cereb Cortex 15:131–140
Beckmann CF, Smith SM (2004) Probabilistic independent component analysis for functional magnetic resonance imaging. IEEE Trans Med Imaging 23:137–152
Beckmann CF, Jenkinson M, Smith SM (2003) General multilevel linear modeling for group analysis in FMRI. Neuroimage 20:1052
Binkofski F, Seitz RJ (2004) Modulation of the BOLD-response in early recovery from sensorimotor stroke. Neurology 63:1223–1229
Birbaumer N, Cohen LG (2007) Brain-computer interfaces: communication and restoration of movement in paralysis. J Physiol 579:621–636
Cramer SC, Lastra L, Lacourse MG, Cohen MJ (2005) Brain motor system function after chronic, complete spinal cord injury. Brain 128:2941–2950
Cramer SC, Orr EL, Cohen MJ, Lacourse MG (2007) Effects of motor imagery training after chronic, complete spinal cord injury. Exp Brain Res 177:233–242
de Vries S, Mulder T (2007) Motor imagery and stroke rehabilitation: a critical discussion. J Rehabil Med 39:5–13
Ehrsson HH, Geyer S, Naito E (2003) Imagery of voluntary movement of fingers, toes, and tongue activates corresponding body-part-specific motor representations. J Neurophysiol 90:3304–3316
Floyer-Lea A, Matthews PM (2005) Distinguishable brain activation networks for short- and long-term motor skill learning. J Neurophysiol 94:512–518
Friehs GM, Zerris VA, Ojakangas CL, Fellows MR, Donoghue JP (2004) Brain-machine and brain-computer interfaces. Stroke 35:2702–2705
Gerardin E, Sirigu A, Lehericy S, Poline JB, Gaymard B, Marsault C, Agid Y, Le Bihan D (2000) Partially overlapping neural networks for real and imagined hand movements. Cereb Cortex 10:1093–1104
Hanakawa T, Immisch I, Toma K, Dimyan MA, Van Gelderen P, Hallett M (2003) Functional properties of brain areas associated with motor execution and imagery. J Neurophysiol 89:989–1002
Hotz-Boendermaker S, Funk M, Summers P, Brugger P, Hepp-Reymond M-C, Curt A, Kollias SS (2008) Preservation of motor programs in paraplegics as demonstrated by attempted and imagined foot movements. Neuroimage 39:383–394
Jackson PL, Lafleur MF, Malouin F, Richards CL, Doyon J (2003) Functional cerebral reorganization following motor sequence learning through mental practice with motor imagery. Neuroimage 20:1171–1180
Johnson-Frey SH (2004) Stimulation through simulation? Motor imagery and functional reorganization in hemiplegic stroke patients. Brain Cogn 55:328–331
Kalb RG (2003) Getting the spinal cord to think for itself. Arch Neurol 60:805–808
Kasess CH, Windischberger C, Cunnington R, Lanzenberger R, Pezawas L, Moser E (2008) The suppressive influence of SMA on M1 in motor imagery revealed by fMRI and dynamic causal modeling. Neuroimage 40:828–837
Kirshblum SC, Priebe MM, Ho CH, Scelza WM, Chiodo AE, Wuermser LA (2007) Spinal cord injury medicine. 3. Rehabilitation phase after acute spinal cord injury. Arch Phys Med Rehabil 88:S62–S70
Lacourse MG, Orr ELR, Cramer SC, Cohen MJ (2005) Brain activation during execution and motor imagery of novel and skilled sequential hand movements. Neuroimage 27:505
Lauer RT, Peckham PH, Kilgore KL (1999) EEG-based control of a hand grasp neuroprosthesis. Neuroreport 10:1767–1771
Leeb R, Friedman D, Müller-Putz G, Scherer R, Slater M, Pfurtscheller G (2007) Self-paced (asynchronous) BCI control of a wheelchair in Virtual Environments: a case study with a tetraplegic. Comput Intell Neurosci:1–8
Muller-Putz GR, Zimmermann D, Graimann B, Nestinger K, Korisek G, Pfurtscheller G (2007) Event-related beta EEG-changes during passive and attempted foot movements in paraplegic patients. Brain Res 1137:84–91
Neuper C, Muller-Putz GR, Scherer R, Pfurtscheller G (2006) Motor imagery and EEG-based control of spelling devices and neuroprostheses. Prog Brain Res 159:393–409
Pfurtscheller G, Guger C, Muller G, Krausz G, Neuper C (2000) Brain oscillations control hand orthosis in a tetraplegic. Neurosci Lett 13:211–214
Pfurtscheller G, Muller GR, Pfurtscheller J, Gerner HJ, Rupp R (2003) ‘Thought’—control of functional electrical stimulation to restore hand grasp in a patient with tetraplegia. Neurosci Lett 351:33–36
Pfurtscheller G, Müller-Putz G, Pfurtscheller J, Rupp R (2005) EEG-based asynchronous BCI controls functional electrical stimulation in a tetraplegic patient. EURASIP J Appl Signal Processing 19:3152–3155
Pfurtscheller G, Leeb R, Keinrath C, Friedman D, Neuper C, Guger C, Slater M (2006) Walking from thought. Brain Res 1071:145–152
Sabbah P, de SS, Leveque C, Gay S, Pfefer F, Nioche C, Sarrazin JL, Barouti H, Tadie M, Cordoliani YS (2002) Sensorimotor cortical activity in patients with complete spinal cord injury: a functional magnetic resonance imaging study. J Neurotrauma 19:53–60
Schmahmann JD, Doyon J, Toga AW, Petrides M, Evans AC (2000) MRI atlas of the human cerebellum. Academic, San Diego
Sharma N, Pomeroy VM, Baron J-C (2006) Motor imagery: a backdoor to the motor system after stroke? Stroke 37:1941–1952
Suga R, Tobimatsu S, Kira J, Kato M (1999) Motor and somatosensory evoked potential findings in HTLV-I associated myelopathy. J Neurol Sci 167:102–106
Tobimatsu S, Sun SJ, Fukui R, Kato M (1998) Effects of sex, height and age on motor evoked potentials with magnetic stimulation. J Neurol 245:256–261
Weiller C, Juptner M, Fellows S, Rijntjes M, Leonhardt G, Kiebel S, Muller S, Diener HC, Thilmann AF (1996) Brain representation of active and passive movements. Neuroimage 4:105
Wolpaw JR, Birbaumer N, McFarland DJ, Pfurtscheller G, Vaughan TM (2002) Brain-computer interfaces for communication and control. Clin Neurophysiol 113:767–791
Woolrich MW, Behrens TEJ, Beckmann CF, Jenkinson M, Smith SM (2004) Multilevel linear modelling for FMRI group analysis using Bayesian inference. Neuroimage 21:1732
Worsley KJ, Evans AC, Marrett S, Neelin P (1992) A three-dimensional statistical analysis for CBF activation studies in human brain. J Cereb Blood Flow Metab 12:900–918
Acknowledgments
This work has been supported by the FWF Austrian Science Fund (SR, grant number P15158), “Lorenz Böhler Gesellschaft” and “Allgemeine Unfallversicherung AUVA” (GP, G-M P). We thank the patient for his enthusiasm with the BCI training and this project and Karin Brodtrager for technical assistance.
Conflict of interest:
None declared.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Enzinger, C., Ropele, S., Fazekas, F. et al. Brain motor system function in a patient with complete spinal cord injury following extensive brain–computer interface training. Exp Brain Res 190, 215–223 (2008). https://doi.org/10.1007/s00221-008-1465-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-008-1465-y