Motor Sequence Complexity and Performing Hand Produce Differential Patterns of Hemispheric Lateralization

Studies in brain damaged patients conclude that the left hemisphere is dominant for controlling heterogeneous sequences performed by either hand, presumably due to the cognitive resources involved in planning complex sequential movements. To determine if this lateralized effect is due to asymmetries in primary sensorimotor or association cortex, whole-brain functional magnetic resonance imaging was used to measure differences in volume of activation while healthy right-handed subjects performed repetitive (simple) or heterogeneous (complex) finger sequences using the right or left hand. Advanced planning, as evidenced by reaction time to the first key press, was greater for the complex than simple sequences and for the left than right hand. In addition to the expected greater contralateral activation in the sensorimotor cortex (SMC), greater left hemisphere activation was observed for left, relative to right, hand movements in the ipsilateral left superior parietal area and for complex, relative to simple, sequences in the left premotor and parietal cortex, left thalamus, and bilateral cerebellum. No such volumetric asymmetries were observed in the SMC. Whereas the overall MR signal intensity was greater in the left than right SMC, the extent of this asymmetry did not vary with hand or complexity level. In contrast, signal intensity in the parietal and premotor cortex was greater in the left than right hemisphere and for the complex than simple sequences. Signal intensity in the caudal anterior cerebellum was greater bilaterally for the complex than simple sequences. These findings suggest that activity in the SMC is associated with execution requirements shared by the simple and complex sequences independent of their differential cognitive requirements. In contrast, consistent with data in brain damaged patients, the left dorsal premotor and parietal areas are engaged when advanced planning is required to perform complex motor sequences that require selection of different effectors and abstract organization of the sequence, regardless of the performing hand.

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

[2]  Stephen J. DeArmond,et al.  Structure of the human brain : a photographic atlas , 1974 .

[3]  D. Kimura,et al.  Motor functions of the left hemisphere. , 1974, Brain : a journal of neurology.

[4]  A. Fugl-Meyer,et al.  The post-stroke hemiplegic patient. 1. a method for evaluation of physical performance. , 1975, Scandinavian journal of rehabilitation medicine.

[5]  E. M. Wilson,et al.  Regional cerebral blood flow comparison of right and left hand movement , 1979, Neurology.

[6]  J. Annett,et al.  The Control of Movement in the Preferred and Non-Preferred Hands* , 1979, The Quarterly journal of experimental psychology.

[7]  B. Milner,et al.  Performance of complex arm and facial movements after focal brain lesions , 1981, Neuropsychologia.

[8]  Dirk-Jan Povel,et al.  Theory of serial pattern production: Tree traversals. , 1982 .

[9]  D. Kimura,et al.  Left-hemisphere control of oral and brachial movements and their relation to communication. , 1982, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[10]  D J Povel,et al.  Structural factors in patterned finger tapping. , 1982, Acta psychologica.

[11]  K. Haaland,et al.  The different types of limb apraxia errors made by patients with left vs. right hemisphere damage , 1984, Brain and Cognition.

[12]  D. Pandya,et al.  Projections to the frontal cortex from the posterior parietal region in the rhesus monkey , 1984, The Journal of comparative neurology.

[13]  D. Harrington,et al.  Programming sequences of hand postures. , 1987, Journal of motor behavior.

[14]  Shmuel Peleg,et al.  Image sequence enhancement using sub-pixel displacements , 1988, Proceedings CVPR '88: The Computer Society Conference on Computer Vision and Pattern Recognition.

[15]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[16]  P. Goldman-Rakic,et al.  Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections , 1989, The Journal of comparative neurology.

[17]  M. P. Bryden,et al.  Different Dimensions of Hand Preference That Relate to Skilled and Unskilled Activities , 1989, Cortex.

[18]  Deborah L. Harrington,et al.  Hemispheric control of the initial and corrective components of aiming movements , 1989, Neuropsychologia.

[19]  D. Harrington,et al.  Hemispheric specialization for motor sequencing: Abnormalities in levels of programming , 1991, Neuropsychologia.

[20]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[21]  R. S. Hinks,et al.  Time course EPI of human brain function during task activation , 1992, Magnetic resonance in medicine.

[22]  D. Harrington,et al.  Motor sequencing with left hemisphere damage. Are some cognitive deficits specific to limb apraxia? , 1992, Brain : a journal of neurology.

[23]  J. Binder,et al.  Functional magnetic resonance imaging of complex human movements , 1993, Neurology.

[24]  M. Honda,et al.  Both primary motor cortex and supplementary motor area play an important role in complex finger movement. , 1993, Brain : a journal of neurology.

[25]  N. Miller,et al.  Technique to improve chronic motor deficit after stroke. , 1993, Archives of physical medicine and rehabilitation.

[26]  Richard G. Carson,et al.  Manual asymmetries: old problems and new directions , 1993 .

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

[28]  S. Kinomura,et al.  Regional cerebral blood flow changes of cortical motor areas and prefrontal areas in humans related to ipsilateral and contralateral hand movement , 1993, Brain Research.

[29]  U Sabatini,et al.  Journal of Cerebral Blood Flow and Metabolism Effect of Side and Rate of Stimulation on Cerebral Blood Flow Changes in Motor Areas during Finger Movements in Humans , 2022 .

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

[31]  Richard S. J. Frackowiak,et al.  The neural correlates of the verbal component of working memory , 1993, Nature.

[32]  A. P. Georgopoulos,et al.  Movement parameters and neural activity in motor cortex and area 5. , 1994, Cerebral cortex.

[33]  K. Kurata Information processing for motor control in primate premotor cortex , 1994, Behavioural Brain Research.

[34]  M Requardt,et al.  Functional cooperativity of human cortical motor areas during self-paced simple finger movements. A high-resolution MRI study. , 1994, Brain : a journal of neurology.

[35]  H. Sakata,et al.  Deficit of hand preshaping after muscimol injection in monkey parietal cortex , 1994, Neuroreport.

[36]  Leslie G. Ungerleider,et al.  Functional MRI evidence for adult motor cortex plasticity during motor skill learning , 1995, Nature.

[37]  A. G. Fisher,et al.  Differences between persons with right or left cerebral vascular accident on the Assessment of Motor and Process Skills. , 1995, Archives of physical medicine and rehabilitation.

[38]  A. Schleicher,et al.  Asymmetry in the Human Motor Cortex and Handedness , 1996, NeuroImage.

[39]  V M Haughton,et al.  Ipsilateral hemisphere activation during motor and sensory tasks. , 1996, AJNR. American journal of neuroradiology.

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

[41]  S P Wise,et al.  The premotor cortex and nonstandard sensorimotor mapping. , 1996, Canadian journal of physiology and pharmacology.

[42]  D. Harrington,et al.  Hemispheric asymmetry of movement , 1996, Current Opinion in Neurobiology.

[43]  R. Shadmehr,et al.  Neural correlates of motor memory consolidation. , 1997, Science.

[44]  S G Kim,et al.  Functional activation in motor cortex reflects the direction and the degree of handedness. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[45]  Richard S. J. Frackowiak,et al.  Anatomy of motor learning. I. Frontal cortex and attention to action. , 1997, Journal of neurophysiology.

[46]  P. Skudlarski,et al.  An fMRI study of the human cortical motor system response to increasing functional demands. , 1997, Magnetic resonance imaging.

[47]  H. Flor,et al.  The Arm Motor Ability Test: reliability, validity, and sensitivity to change of an instrument for assessing disabilities in activities of daily living. , 1997, Archives of physical medicine and rehabilitation.

[48]  M. Hallett,et al.  Involvement of the ipsilateral motor cortex in finger movements of different complexities , 1997, Annals of neurology.

[49]  Edward E. Smith,et al.  Temporal dynamics of brain activation during a working memory task , 1997, Nature.

[50]  J M Bower,et al.  Control of sensory data acquisition. , 1997, International review of neurobiology.

[51]  Alan C. Evans,et al.  Cerebellar Contributions to Motor Timing: A PET Study of Auditory and Visual Rhythm Reproduction , 1998, Journal of Cognitive Neuroscience.

[52]  J. Doyon,et al.  Role of the striatum, cerebellum and frontal lobes in the automatization of a repeated visuomotor sequence of movements , 1998, Neuropsychologia.

[53]  J. Callicott,et al.  Hemispheric control of motor function: a whole brain echo planar fMRI study , 1998, Psychiatry Research: Neuroimaging.

[54]  M. Hallett,et al.  The functional neuroanatomy of simple and complex sequential finger movements: a PET study. , 1998, Brain : a journal of neurology.

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

[56]  Seong-Gi Kim,et al.  Effects of movement predictability on cortical motor activation , 1998, Neuroscience Research.

[57]  A. Gordon,et al.  Functional magnetic resonance imaging of motor, sensory, and posterior parietal cortical areas during performance of sequential typing movements , 1998, Experimental Brain Research.

[58]  Karl J. Friston,et al.  Role of the human rostral supplementary motor area and the basal ganglia in motor sequence control: investigations with H2 15O PET. , 1998, Journal of neurophysiology.

[59]  M Hallett,et al.  Inhibitory influence of the ipsilateral motor cortex on responses to stimulation of the human cortex and pyramidal tract , 1998, The Journal of physiology.

[60]  R. Passingham,et al.  Temporary interference in human lateral premotor cortex suggests dominance for the selection of movements. A study using transcranial magnetic stimulation. , 1998, Brain : a journal of neurology.

[61]  D. Hoffman,et al.  Muscle and movement representations in the primary motor cortex. , 1999, Science.

[62]  Carlo Adolfo Porro,et al.  Bilateral representation of sequential finger movements in human cortical areas , 1999, Neuroscience Letters.

[63]  M Hallett,et al.  Dissociation of the pathways mediating ipsilateral and contralateral motor‐evoked potentials in human hand and arm muscles , 1999, The Journal of physiology.

[64]  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.

[65]  J. Jonides,et al.  Storage and executive processes in the frontal lobes. , 1999, Science.

[66]  R T Knight,et al.  Neural representations of skilled movement. , 2000, Brain : a journal of neurology.

[67]  E. Taub,et al.  Objective measurement of functional upper-extremity movement using accelerometer recordings transformed with a threshold filter. , 2000, Stroke.

[68]  K. Heilman,et al.  Neglect and Related Disorders , 1984, Seminars in neurology.

[69]  D. Elliott,et al.  Moving into the New Millennium: Some Perspectives on the Brain in Action , 2000, Brain and Cognition.

[70]  J. Moll,et al.  Functional MRI correlates of real and imagined tool-use pantomimes , 2000, Neurology.

[71]  Alan C. Evans,et al.  MRI Atlas of the Human Cerebellum , 2000 .

[72]  Mark S. Seidenberg,et al.  Neural Systems Underlying the Recognition of Familiar and Newly Learned Faces , 2000, The Journal of Neuroscience.

[73]  Stephen M. Rao,et al.  Specialized Neural Systems Underlying Representations of Sequential Movements , 2000, Journal of Cognitive Neuroscience.

[74]  R. Sainburg Evidence for a dynamic-dominance hypothesis of handedness , 2001, Experimental Brain Research.

[75]  Matthew F. S. Rushworth,et al.  Attention systems and the organization of the human parietal cortex , 2001, NeuroImage.

[76]  Richard G. Carson,et al.  Manual Asymmetries in the Preparation and Control of Goal-Directed Movements , 2001, Brain and Cognition.

[77]  R. E Passingham,et al.  Cerebral dominance for action in the human brain: the selection of actions , 2001, Neuropsychologia.

[78]  D. Boussaoud Attention versus Intention in the Primate Premotor Cortex , 2001, NeuroImage.

[79]  Scott T. Grafton,et al.  Motor sequence learning with the nondominant left hand , 2002, Experimental Brain Research.

[80]  M. Hallett,et al.  Early consolidation in human primary motor cortex , 2002, Nature.

[81]  H. Vet,et al.  Clinimetric Properties of the Motor Activity Log for the Assessment of Arm Use in Hemiparetic Patients , 2004, Stroke.

[82]  M. Goodale,et al.  The effects of unilateral brain damage on visually guided reaching: hemispheric differences in the nature of the deficit , 2004, Experimental Brain Research.

[83]  Donna S Hoffman,et al.  Deficits in movements of the wrist ipsilateral to a stroke in hemiparetic subjects. , 2004, Journal of neurophysiology.

[84]  C. J. Winstein,et al.  Effects of unilateral brain damage on the control of goal-directed hand movements , 2004, Experimental Brain Research.

[85]  R. Kettner,et al.  Control of remembered reaching sequences in monkey , 1996, Experimental Brain Research.

[86]  R. Kettner,et al.  Control of remembered reaching sequences in monkey , 1996, Experimental Brain Research.

[87]  Roland R. Lee,et al.  Hemispheric asymmetries for kinematic and positional aspects of reaching. , 2004, Brain : a journal of neurology.

[88]  Robert L Sainburg,et al.  Interlimb differences in control of movement extent. , 2004, Journal of neurophysiology.

[89]  J. Poole,et al.  Functional implications of ipsilesional motor deficits after unilateral stroke. , 2005, Archives of physical medicine and rehabilitation.

[90]  Jill Whitall,et al.  Hand dominance and side of stroke affect rehabilitation in chronic stroke , 2005, Clinical rehabilitation.

[91]  I. Derakhshan Anatomy of handedness and the laterality of seizure onset: surgical implications of new understandings in motor control , 2005, Neurological research.

[92]  Malcolm H Granat,et al.  Continuous monitoring of upper-limb activity in a free-living environment. , 2005, Archives of physical medicine and rehabilitation.

[93]  Donatella Spinelli,et al.  Effect of practice on brain activity: an investigation in top-level rifle shooters. , 2005, Medicine and science in sports and exercise.

[94]  Maurits W van der Molen,et al.  Preparation for speeded action as a psychophysiological concept. , 2005, Psychological bulletin.

[95]  E. Taub,et al.  Reliability and Validity of the Upper-Extremity Motor Activity Log-14 for Measuring Real-World Arm Use , 2005, Stroke.

[96]  S. Swinnen,et al.  The role of anterior cingulate cortex and precuneus in the coordination of motor behaviour , 2005, The European journal of neuroscience.

[97]  E. Taub,et al.  The EXCITE Trial: Attributes of the Wolf Motor Function Test in Patients with Subacute Stroke , 2005, Neurorehabilitation and neural repair.