The relationship between brain activity and peak grip force is modulated by corticospinal system integrity after subcortical stroke

In healthy human subjects, the relative contribution of cortical regions to motor performance varies with the task parameters. Additionally, after stroke, recruitment of cortical areas during a simple motor task varies with corticospinal system integrity. We investigated whether the pattern of motor system recruitment in a task involving increasingly forceful hand grips is influenced by the degree of corticospinal system damage. Nine chronic subcortical stroke patients and nine age‐matched controls underwent functional magnetic brain imaging whilst performing repetitive isometric hand grips. Target grip forces were varied between 15% and 45% of individual maximum grip force. Corticospinal system functional integrity was assessed with transcranial magnetic stimulation. Averaged across all forces, there was more task‐related activation compared with rest in the secondary motor areas of patients with greater corticospinal system damage, confirming previous reports. However, here we were primarily interested in regional brain activation, which covaried with the amount of force generated, implying a prominent executive role in force production. We found that in control subjects and patients with lesser corticospinal system damage, signal change increased linearly with increasing force output in contralateral primary motor cortex, supplementary motor area and ipsilateral cerebellum. In contrast, in patients with greater corticospinal system damage, force‐related signal changes were seen mainly in contralesional dorsolateral premotor cortex, bilateral ventrolateral premotor cortices and contralesional cerebellum, but not ipsilesional primary motor cortex. These findings suggest that the premotor cortices might play a new and functionally relevant role in controlling force production in patients with more severe corticospinal system disruption.

[1]  G. Thickbroom,et al.  Differences in functional magnetic resonance imaging of sensorimotor cortex during static and dynamic finger flexion , 1999, Experimental Brain Research.

[2]  E. Evarts,et al.  Motor Cortex control of finely graded forces. , 1983, Journal of neurophysiology.

[3]  R. Lemon,et al.  Facilitation from ventral premotor cortex of primary motor cortex outputs to macaque hand muscles. , 2003, Journal of neurophysiology.

[4]  S. Barbay,et al.  Reorganization of remote cortical regions after ischemic brain injury: a potential substrate for stroke recovery. , 2003, Journal of neurophysiology.

[5]  M. Hepp-Reymond,et al.  Contrasting properties of monkey somatosensory and motor cortex neurons activated during the control of force in precision grip. , 1991, Journal of neurophysiology.

[6]  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.

[7]  R. Johansson,et al.  Cortical activity in precision- versus power-grip tasks: an fMRI study. , 2000, Journal of neurophysiology.

[8]  W. Byblow,et al.  The Contribution of Cervical Propriospinal Premotoneurons in Recovering Hemiparetic Stroke Patients , 2004, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[9]  M. Hepp-Reymond,et al.  Neuronal coding of static force in the primate motor cortex. , 1978, Journal de physiologie.

[10]  E. Bizzi,et al.  Neuronal correlates of movement dynamics in the dorsal and ventral premotor area in the monkey , 2005, Experimental Brain Research.

[11]  B. Rosen,et al.  A functional MRI study of subjects recovered from hemiparetic stroke. , 1997, Stroke.

[12]  P. Strick,et al.  Frontal Lobe Inputs to the Digit Representations of the Motor Areas on the Lateral Surface of the Hemisphere , 2005, The Journal of Neuroscience.

[13]  Karl J. Friston,et al.  Characterizing Stimulus–Response Functions Using Nonlinear Regressors in Parametric fMRI Experiments , 1998, NeuroImage.

[14]  R. Passingham,et al.  Relation between cerebral activity and force in the motor areas of the human brain. , 1995, Journal of neurophysiology.

[15]  Richard S. J. Frackowiak,et al.  Age-related changes in the neural correlates of motor performance. , 2003, Brain : a journal of neurology.

[16]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[17]  C. Fromm,et al.  Static firing rates of premotor and primary motor cortical neurons associated with torque and joint position , 2004, Experimental Brain Research.

[18]  R. Porter,et al.  Corticospinal Function and Voluntary Movement , 1993 .

[19]  A. M. Smith,et al.  Relation of activity in precentral cortical neurons to force and rate of force change during isometric contractions of finger muscles , 1975, Experimental Brain Research.

[20]  A. Sunderland,et al.  A Pilot Study of Event-Related Functional Magnetic Resonance Imaging of Monitored Wrist Movements in Patients With Partial Recovery , 2002, Stroke.

[21]  P. Matthews,et al.  The role of ipsilateral premotor cortex in hand movement after stroke , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[22]  T J Ebner,et al.  Visuomotor processing as reflected in the directional discharge of premotor and primary motor cortex neurons. , 1999, Journal of neurophysiology.

[23]  Christian Gerloff,et al.  The Role of Multiple Contralesional Motor Areas for Complex Hand Movements after Internal Capsular Lesion , 2006, The Journal of Neuroscience.

[24]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited—Again , 1995, NeuroImage.

[25]  G E Alexander,et al.  Neural representations of the target (goal) of visually guided arm movements in three motor areas of the monkey. , 1990, Journal of neurophysiology.

[26]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[27]  R. Turner,et al.  Event-Related fMRI: Characterizing Differential Responses , 1998, NeuroImage.

[28]  T. Ebner,et al.  Temporal encoding of movement kinematics in the discharge of primate primary motor and premotor neurons. , 1995, Journal of neurophysiology.

[29]  Ann M. Stowe,et al.  Extensive Cortical Rewiring after Brain Injury , 2005, The Journal of Neuroscience.

[30]  E. Pierrot-Deseilligny,et al.  Non‐monosynaptic transmission of the cortical command for voluntary movement in man. , 1994, The Journal of physiology.

[31]  Alan C. Evans,et al.  Morphology, morphometry and probability mapping of the pars opercularis of the inferior frontal gyrus: an in vivo MRI analysis , 1999, The European journal of neuroscience.

[32]  M. Torrens.  Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

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

[34]  Richard S. J. Frackowiak,et al.  Neural correlates of outcome after stroke: a cross-sectional fMRI study. , 2003, Brain : a journal of neurology.

[35]  Pattern of descending excitation of presumed propriospinal neurones at the onset of voluntary movement in humans. , 1994, Acta physiologica Scandinavica.

[36]  Roger N. Lemon,et al.  Reorganization of the Executive Motor System after Stroke , 1997 .

[37]  Richard S. J. Frackowiak,et al.  Motor system activation after subcortical stroke depends on corticospinal system integrity. , 2006, Brain : a journal of neurology.

[38]  Sabine Meunier,et al.  Changes in propriospinally mediated excitation of upper limb motoneurons in stroke patients. , 2003, Brain : a journal of neurology.

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

[40]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[41]  M. Ridding,et al.  Stimulus/response curves as a method of measuring motor cortical excitability in man. , 1997, Electroencephalography and clinical neurophysiology.

[42]  L. Cohen,et al.  Reorganization of the human ipsilesional premotor cortex after stroke. , 2004, Brain : a journal of neurology.

[43]  M. Hallett,et al.  Multimodal imaging of brain reorganization in motor areas of the contralesional hemisphere of well recovered patients after capsular stroke. , 2006, Brain : a journal of neurology.

[44]  T. Ebner,et al.  Representation of accuracy in the dorsal premotor cortex , 2000, The European journal of neuroscience.

[45]  H. Forssberg,et al.  Differential fronto-parietal activation depending on force used in a precision grip task: an fMRI study. , 2001, Journal of neurophysiology.

[46]  D. Hoffman,et al.  Direction of action is represented in the ventral premotor cortex , 2001, Nature Neuroscience.

[47]  A. Riehle,et al.  Monkey primary motor and premotor cortex: single-cell activity related to prior information about direction and extent of an intended movement. , 1989, Journal of neurophysiology.

[48]  H. Freund,et al.  Reorganisation of descending motor pathways in patients after hemispherectomy and severe hemispheric lesions demonstrated by magnetic brain stimulation , 2004, Experimental Brain Research.

[49]  R. Lemon,et al.  Macaque ventral premotor cortex exerts powerful facilitation of motor cortex outputs to upper limb motoneurons. , 2004, The Journal of Neuroscience.

[50]  J. Schaechter,et al.  Quantitative assessment of mirror movements after stroke. , 1998, Stroke.

[51]  Heidi Johansen-Berg,et al.  Neuroimaging in Stroke Recovery: A Position Paper from the First International Workshop on Neuroimaging and Stroke Recovery , 2004, Cerebrovascular Diseases.

[52]  G. Rizzolatti,et al.  Motor and cognitive functions of the ventral premotor cortex , 2002, Current Opinion in Neurobiology.

[53]  P. Strick,et al.  Cerebellar output channels. , 1997, International review of neurobiology.

[54]  T. Ebner,et al.  Neuronal specification of direction and distance during reaching movements in the superior precentral premotor area and primary motor cortex of monkeys. , 1993, Journal of neurophysiology.

[55]  G E Alexander,et al.  Preferential representation of instructed target location versus limb trajectory in dorsal premotor area. , 1997, Journal of neurophysiology.

[56]  A. Georgopoulos,et al.  The motor cortex and the coding of force. , 1992, Science.

[57]  R. Lemon,et al.  Differences in the corticospinal projection from primary motor cortex and supplementary motor area to macaque upper limb motoneurons: an anatomical and electrophysiological study. , 2002, Cerebral cortex.

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

[59]  S. Wise,et al.  Visuospatial versus visuomotor activity in the premotor and prefrontal cortex of a primate , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[60]  L. Cohen,et al.  Mechanisms influencing stimulus-response properties of the human corticospinal system , 2001, Clinical Neurophysiology.

[61]  H. Freund,et al.  Role of the premotor cortex in recovery from middle cerebral artery infarction. , 1998, Archives of neurology.

[62]  Paul B. Johnson,et al.  Cortical networks for visual reaching: physiological and anatomical organization of frontal and parietal lobe arm regions. , 1996, Cerebral cortex.

[63]  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.

[64]  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.

[65]  E. Evarts,et al.  Relation of pyramidal tract activity to force exerted during voluntary movement. , 1968, Journal of neurophysiology.

[66]  A. Schleicher,et al.  Broca's region revisited: Cytoarchitecture and intersubject variability , 1999, The Journal of comparative neurology.

[67]  Karl J. Friston,et al.  Modelling Geometric Deformations in Epi Time Series , 2022 .

[68]  C. Capaday,et al.  Input-output properties and gain changes in the human corticospinal pathway , 1997, Experimental Brain Research.

[69]  S. Scott,et al.  Reaching movements with similar hand paths but different arm orientations. II. Activity of individual cells in dorsal premotor cortex and parietal area 5. , 1997, Journal of neurophysiology.