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First published November/December 2007

Cortical Plasticity in Amyotrophic Lateral Sclerosis: Motor Imagery and Function

Abstract

Background. Cortical networks underlying motor imagery are functionally close to motor performance networks and can be activated by patients with severe motor disabilities. Objective. The aim of the study was to examine the longitudinal effect of progressive motoneuron degeneration on cortical representation of motor imagery and function in amyotrophic lateral sclerosis. Methods. The authors studied 14 amyotrophic lateral sclerosis patients and 15 healthy controls and a subgroup of 11 patients and 14 controls after 6 months with a grip force paradigm comprising imagery and execution tasks using functional magnetic resonance imaging. Results. Motor imagery activated similar neural networks as motor execution in amyotrophic lateral sclerosis patients and healthy subjects in the primary motor (BA 4), premotor, and supplementary motor (BA 6) cortex. Amyotrophic lateral sclerosis patients presented a stronger response within premotor and primary motor areas for imagery and execution compared to controls. After 6 months, these differences persisted with additional activity in the precentral gyrus in patients as well as in a frontoparietal network for motor imagery, in which activity increased with impairment. Conclusion. The findings suggest an ongoing compensatory process within the higher order motor-processing system of amyotrophic lateral sclerosis patients, probably to overcome loss of function in primary motor and motor imagery-specific networks. The increased activity in precentral and frontoparietal networks in motor imagery might be used to control brain-computer interfaces to drive communication and limb prosthetic devices in patients with loss of motor control such as severely disabled amyotrophic lateral sclerosis patients in a locked-in-like state.

References

Elbert T., Rockstroh B. Reorganization of human cerebral cortex: the range of changes following use and injury. Neuroscientist. 2004;10:129-141.
Brooks BR, Bushara K., Khan A., et al. Functional magnetic resonance imaging (fMRI) clinical studies in ALS: paradigms, problems and promises. Amyotroph Lateral Scler Other Motor Neuron Disord. 2000;1:23-32.
Kew Jjm, Leigh PN, Playford ED, et al. Cortical function in amyotrophic lateral sclerosis: a positron emission tomography study. Brain. 1993;116:655-680.
Kew Jjm, Brooks DJ, Passingham RE, et al. Cortical function in progressive lower motor neuron disorders and amyotrophic lateral sclerosis: a comparative PET study. Neurology. 1994;44:1101-1110.
Konrad C., Henningsen H., Bremer J., et al. Pattern of cortical reorganization in amyotrophic lateral sclerosis: a functional magnetic resonance imaging study. Exp Brain Res. 2002;143:51-56.
Schoenfeld MA, Tempelmann C., Gaul C., et al. Functional motor compensation in amyotrophic lateral sclerosis. J Neurol. 2005; 252:944-952.
Konrad C., Jansen A., Henningsen H., et al. Subcortical reorganization in amyotrophic lateral sclerosis . Exp Brain Res. 2006; 172:361-369.
Tessitore A., Esposito F., Monsurro MR, et al. Subcortical motor plasticity in patients with sporadic ALS: an fMRI study. Brain Res Bull. 2006;69:489-494.
Gerardin E., Sirigu A., Lehericy S., et al. Partially overlapping neural networks for real and imagined hand movements. Cereb Cortex. 2000;10:1093-1104.
Lotze M., Montoya P., Erb M., et al. Activation of cortical and cerebellar motor areas during executed and imagined hand movements: an fMRI study. J Cogn Neurosc . 1999;11:491-501.
Lotze M., Halsband U. Motor imagery. J Physiol Paris. 2006;99: 386-395.
Porro CA, Francescato MP, Cettolo V., et al. Primary motor and sensory cortex activation during motor performance and motor imagery: a functional magnetic resonance imaging study. J Neurosci. 1996;16:7688-7698.
Stephan KM, Fink GR, Passingham RE, et al. Functional anatomy of the mental representation of upper extremity movements in healthy subjects. J Neurophysiol. 1995;73:373-386.
Alkadhi H., Brugger P., Boendermaker SH, et al. What disconnection tells about motor imagery: evidence from paraplegic patients. Cereb Cortex. 2005;15:31-140.
Cunnington R., Egan GF, O'Sullivan JD, et al. Motor imagery in Parkinson's disease: a PET study. Mov Disord. 2001;16: 849-857.
Samuel M., Ceballos-Baumann AO, Boecker H., et al. Motor imagery in normal subjects and Parkinson's disease patients: an H215O PET study. Neuroreport. 2001;12:821-828.
Kübler A., Nijboer F., Mellinger J., et al. Patients with ALS can use sensorimotor rhythms to operate a brain-computer interface. Neurology. 2005;64:1775-1777.
Brooks BR Revised criteria for the diagnosis of amyotrophic lateral sclerosis. Subcommittee on Motor Neuron Diseases of World Federation of Neurology Research Group on Neuromuscular Diseases, El Escorial “Clinical Limits of ALS” Workshop Contributors (1994). El Escorial World Federation of Neurology criteria for the diagnosis of amyotrophic lateral sclerosis. J Neur Sci. 1998;124:96-107.
Lulé D., Kurt A., Jürgens R., et al. Emotional responding in amyotrophic lateral sclerosis. J Neurol. 2005;252:1517-1524.
Oldfield RC The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9:97-113.
Friston KJ, Holmes AP, Worsley KJ, et al. Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Map. 1995;2:189-210. Developer version January 2005. Available at: http://www.fil.ion.ucl.ac.uk/spm. Accessed January 3, 2005.
Talaraich J., Tournoux P. Co-Planar Stereotaxic Atlas of the Human Brain. New York : Thieme Medical Publishers; 1988 .
Friston KJ, Glaser DE, Henson Rna, et al. Classical and Bayesian inference in neuroimaging: applications . Neuroimage. 2002;16: 484-512.
Friston KJ, Penny W., Phillips C., et al. Classical and Bayesian inference in neuroimaging: theory. Neuroimage. 2002;16:465-483.
Dempster AP, Rubin DB, Tsutakawa RK Estimation in covariance component models. J Am Stat Assoc. 1981;76:341-353.
Tzourio-Mazoyer N., Landeau B., Papathanassiou D., et al. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single subject brain. Neuroimage. 2002;15:273-289.
Maldjian JA, Laurienti PJ, Kraft RA, et al. An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets. Neuroimage. 2003;19:1233-1239.
Eickhoff S., Stephan KE, Mohlberg H., et al. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage . 2005;25:1325-1335.
Pakhomov S. MNI Space Utility (MSU). October 2001. Available at: http://www.ihb.spb.ru/~pet_lab/MSU/MSUMain.html. Accessed May 10, 2005.
Debaere F., Wenderoth N., Sunaert S., et al. Cerebellar and premotor function in bimanual coordination: parametric neural responses to spatiotemporal complexity and cycling frequency. Neuroimage. 2004;21:1416-1427.
Pioro EP, Antel JP, Cashman NR, et al. Detection of cortical neuron loss in motor neuron disease by proton magnetic resonance spectroscopic imaging in vivo. Neurology. 1994;44:1933-1938.
Pamphlett R., Kril J., Hng TM Motor neuron disease: a primary disorder of corticomotoneurons? Muscle Nerve. 1995;18:314-318.
Boecker H., Ceballos-Baumann AO, Bartenstein P., et al. An H(2)(15) O positron emission tomography study on mental imagery of movement sequences: the effect of modulating sequence length and direction . Neuroimage. 2002;17:999-1009.
Rubia K., Russell T., Overmeyer S., et al. Mapping motor inhibition: conjunctive brain activations across different versions of go/no-go and stop tasks. Neuroimage . 2001;13:250-261.
Picard N., Strick PL Imaging the premotor areas. Curr Opin Neurobiol. 2001;11:663-672.
Rizzolatti G., Fadiga L., Fogassi L., et al. The space around us. Science. 1997;277:190-191.
Griffiths TD, Green GG, Rees A., et al. Human brain areas involved in the analysis of auditory movement. Hum Brain Mapp. 2000;9:72-80.
Cramer SC, Nelles G., Benson RR, et al. A functional MRI study of subjects recovered from hemiparetic stroke. Stroke. 1997;28: 2518-2527.
Ludolph AC, Langen KJ, Regard M., et al. Frontal lobe function in amyotrophic lateral sclerosis: a neuropsychologic and positron emission tomography study. Acta Neurol Scand. 1992;85:81-89.

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Article first published: November/December 2007
Issue published: November/December 2007

Keywords

  1. Amyotrophic lateral sclerosis (ALS)
  2. Cortical plasticity
  3. Motor imagery
  4. fMRI
  5. Brain-computer interfaces

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PubMed: 17476000

Authors

Affiliations

Dorothée Lulé, PhD
Section of Neurophysiology, Univeristy of Ulm, Ulm, Germany, Eberhard-Karls-University of Tübingen, Institute of Medical Psychology and Behavioral Neurobiology, Germany, [email protected]
Volker Diekmann, PhD
Section of Neurophysiology, Univeristy of Ulm, Ulm, Germany
Jan Kassubek, MD
Department of Neurology University of Ulm, Ulm, Germany
Anja Kurt, MD
Department of Neurology University of Ulm, Ulm, Germany
Niels Birbaumer, PhD
Eberhard-Karls-University of Tübingen, Institute of Medical Psychology and Behavioral Neurobiology, Germany, National Institutes of Health, NINDS, Human Cortical Physiology, Bethesda, Maryland
Albert C. Ludolph, MD
Department of Neurology University of Ulm, Ulm, Germany
Eduard Kraft, MD
Department of Neurology University of Ulm, Ulm, Germany

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