Pattern of cortical reorganization in amyotrophic lateral sclerosis: a functional magnetic resonance imaging study

Depending on individual lesion location and extent, reorganization of the human motor system has been observed with a high interindividual variability. In addition, variability of forces exerted, of motor effort, and of movement strategies complicates the interpretation of functional imaging studies. We hypothesize that a general pattern of reorganization can be identified if a homogeneous patient population is chosen and experimental conditions are controlled. Patients with amyotrophic lateral sclerosis (ALS) and healthy volunteers were trained to perform a simple finger flexion task with 10% of each individual’s maximum grip force with constant movement amplitude and frequency. The activation pattern in ALS patients was distinctly different to that in healthy controls: In ALS patients, motor cortex activation was located more anteriorly, encompassing the premotor gyrus. The cluster volume within the supplementary motor area (SMA) was higher and shifted toward the pre-SMA. Contralateral inferior area 6 and bilateral parietal area 40 revealed higher cluster volumes. Our results demonstrate a general pattern of functional changes after motor neuron degeneration. They support the concept of a structurally parallel and functionally specialized organization of voluntary motor control. Degeneration of the first and second motor neurons leads to enhanced recruitment of motor areas usually involved in initiation and planning of movement. Partial compensation between functionally related motor areas seems to be a strategy to optimize performance if the most efficient pathway is unavailable.

[1]  M. Hepp-Reymond,et al.  Force-related neuronal activity in two regions of the primate ventral premotor cortex. , 1994, Canadian journal of physiology and pharmacology.

[2]  J Valls-Solé,et al.  Rapid modulation of human cortical motor outputs following ischaemic nerve block. , 1993, Brain : a journal of neurology.

[3]  J. Tanji,et al.  Both supplementary and presupplementary motor areas are crucial for the temporal organization of multiple movements. , 1998, Journal of neurophysiology.

[4]  Jerre Levy,et al.  A review, analysis, and some new data on hand-posture distributions in left-handers , 1984, Brain and Cognition.

[5]  A. Hudson,et al.  Changes in sizes of cortical and lower motor neurons in amyotrophic lateral sclerosis. , 1991, Brain : a journal of neurology.

[6]  R. C. Oldfield The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[7]  S. P. Evseev,et al.  The Control of Movement , 1996 .

[8]  L. J. Chapman,et al.  The measurement of handedness , 1987, Brain and Cognition.

[9]  J. Kaas,et al.  Reorganization in Primary Motor Cortex of Primates with Long-Standing Therapeutic Amputations , 1999, The Journal of Neuroscience.

[10]  RP Dum,et al.  Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[11]  Richard S. J. Frackowiak,et al.  The functional anatomy of motor recovery after stroke in humans: A study with positron emission tomography , 1991, Annals of neurology.

[12]  Jun Tanji,et al.  New concepts of the supplementary motor area , 1996, Current Opinion in Neurobiology.

[13]  RP Dum,et al.  The origin of corticospinal projections from the premotor areas in the frontal lobe , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[14]  S Takahashi,et al.  Functional MR imaging of cortical activation of the cerebral hemispheres during motor tasks. , 1998, AJNR. American journal of neuroradiology.

[15]  T. Lawyer,et al.  Amyotrophic lateral sclerosis. , 1953, A.M.A. archives of neurology and psychiatry.

[16]  Paul B. Johnson,et al.  Premotor and parietal cortex: corticocortical connectivity and combinatorial computations. , 1997, Annual review of neuroscience.

[17]  B. Brooks,et al.  El escorial World Federation of Neurology criteria for the diagnosis of amyotrophic lateral sclerosis , 1994, Journal of the Neurological Sciences.

[18]  Yue Cao,et al.  Pilot study of functional MRI to assess cerebral activation of motor function after poststroke hemiparesis. , 1998, Stroke.

[19]  K. Zilles,et al.  Polymodal Motion Processing in Posterior Parietal and Premotor Cortex A Human fMRI Study Strongly Implies Equivalencies between Humans and Monkeys , 2001, Neuron.

[20]  A. Murata,et al.  Largely segregated parietofrontal connections linking rostral intraparietal cortex (areas AIP and VIP) and the ventral premotor cortex (areas F5 and F4) , 1999, Experimental Brain Research.

[21]  B. Weber,et al.  Context-dependent force coding in motor and premotor cortical areas , 1999, Experimental Brain Research.

[22]  D. McCloskey,et al.  Sensations of heaviness. , 1977, Brain : a journal of neurology.

[23]  A. Scheibel,et al.  Degeneration of the human Betz cell due to amyotrophic lateral sclerosis , 1979, Experimental Neurology.

[24]  G. Rizzolatti,et al.  The organization of the cortical motor system: new concepts. , 1998, Electroencephalography and clinical neurophysiology.

[25]  W. Brown,et al.  Clinicopathological features of primary lateral sclerosis are different from amyotrophic lateral sclerosis , 1993, Brain Research Bulletin.

[26]  I. Darian‐Smith,et al.  Multiple corticospinal neuron populations in the macaque monkey are specified by their unique cortical origins, spinal terminations, and connections. , 1994, Cerebral cortex.

[27]  H. Braak,et al.  A primitive gigantopyramidal field buried in the depth of the cingulate sulcus of the human brain , 1976, Brain Research.

[28]  V. Hömberg,et al.  Reorganization of motor output in the non-affected hemisphere after stroke. , 1997, Brain : a journal of neurology.

[29]  J. Kalaska,et al.  Prior information in motor and premotor cortex: activity during the delay period and effect on pre-movement activity. , 2000, Journal of neurophysiology.

[30]  D. Arnold,et al.  Detection of cortical neuron loss in motor neuron disease by proton magnetic resonance spectroscopic imaging in vivo , 1994, Neurology.

[31]  K. Zilles,et al.  Functional neuroanatomy of the primate isocortical motor system , 2000, Anatomy and Embryology.

[32]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[33]  R W Cox,et al.  Software tools for analysis and visualization of fMRI data , 1997, NMR in biomedicine.

[34]  Mauro Silvestrini,et al.  Ipsilateral activation of the unaffected motor cortex in patients with hemiparetic stroke , 2000, Clinical Neurophysiology.

[35]  A Curt,et al.  How does the human brain deal with a spinal cord injury? , 1998, The European journal of neuroscience.

[36]  L. Cohen,et al.  Modulation of Plasticity in Human Motor Cortex after Forearm Ischemic Nerve Block , 1998, The Journal of Neuroscience.

[37]  Gary W Thickbroom,et al.  Long-term changes in motor cortical organisation after recovery from subcortical stroke 1 1 Published on the World Wide Web on 1 December 2000. , 2001, Brain Research.

[38]  R. J. Seitz,et al.  Precentral glioma location determines the displacement of cortical hand representation. , 1998, Neurosurgery.

[39]  Richard B. Stein Control of Movement , 1980 .

[40]  J Tanji,et al.  Comparison of movement-related activity in two cortical motor areas of primates. , 1982, Journal of neurophysiology.

[41]  P N Leigh,et al.  Cortical function in amyotrophic lateral sclerosis. A positron emission tomography study. , 1993, Brain : a journal of neurology.

[42]  M. Hallett,et al.  Mesial motor areas in self-initiated versus externally triggered movements examined with fMRI: effect of movement type and rate. , 1999, Journal of neurophysiology.

[43]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[44]  K. Zilles,et al.  Functions and structures of the motor cortices in humans , 1996, Current Opinion in Neurobiology.

[45]  H J Freund Functional organization of the human supplementary motor area and dorsolateral premotor cortex. , 1996, Advances in neurology.

[46]  G. Rizzolatti,et al.  Parietal cortex: from sight to action , 1997, Current Opinion in Neurobiology.

[47]  Richard S. J. Frackowiak,et al.  Cortical function in progressive lower motor neuron disorders and amyotrophic lateral sclerosis , 1994, Neurology.

[48]  G Rizzolatti,et al.  Parcellation of human mesial area 6: cytoarchitectonic evidence for three separate areas , 1998, The European journal of neuroscience.

[49]  A. P. Georgopoulos,et al.  Functional magnetic resonance imaging of motor cortex: hemispheric asymmetry and handedness. , 1993, Science.

[50]  Karl J. Friston,et al.  Individual patterns of functional reorganization in the human cerebral cortex after capsular infraction , 1993, Annals of neurology.

[51]  J. Kril,et al.  Motor neuron disease: A primary disorder of corticomotoneurons? , 1995, Muscle & nerve.

[52]  R. Müller,et al.  Brain Organization of Motor and Language Functions Following Hemispherectomy: A [15O]-Water Positron Emission Tomography Study , 1998, Journal of child neurology.

[53]  J. Liepert,et al.  Motor cortex disinhibition of the unaffected hemisphere after acute stroke , 2000, Muscle & nerve.

[54]  Karl J. Friston,et al.  Functional reorganization of the brain in recovery from striatocapsular infarction in man , 1992, Annals of neurology.