Handedness, dexterity, and motor cortical representations.

Motor system organization varies with handedness. However, previous work has focused almost exclusively on direction of handedness (right or left) as opposed to degree of handedness (strength). In the present study, we determined whether measures of interhemispheric interactions and degree of handedness are related to contra- and ipsilateral motor cortical representations. Participants completed a battery of handedness assessments including both handedness preference measures and behavioral measures of intermanual differences in dexterity, a computerized version of the Poffenberger paradigm (PP) to estimate interhemispheric transfer time (IHTT), and they underwent transcranial magnetic stimulation (TMS) mapping of both motor cortices while we recorded muscle activity from the first dorsal interosseous muscle bilaterally. A greater number of ipsilateral motor evoked potentials (iMEPs) were elicited in less lateralized individuals with the number of iMEPs correlated with IHTT. There were no relationships between handedness or lateralization of dexterity and symmetry of contralateral motor representations, although this symmetry was related to IHTT. Finally, IHTT was positively correlated with multiple measures of laterality and handedness. These findings demonstrate that degree of laterality of dexterity is related to the propensity for exhibiting iMEPs and the speed of interhemispheric interactions. However, it is not clear whether iMEPs are directly mediated via ipsilateral corticospinal projections or are transcallosally transmitted.

[1]  T. Paus,et al.  Transcranial magnetic stimulation and the challenge of coil placement: A comparison of conventional and stereotaxic neuronavigational strategies , 2008, Human brain mapping.

[2]  J. Klein,et al.  Human Motor Corpus Callosum: Topography, Somatotopy, and Link between Microstructure and Function , 2007, The Journal of Neuroscience.

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

[4]  Nicolas Cherbuin,et al.  Hemispheric interactions are different in left-handed individuals. , 2006, Neuropsychology.

[5]  R. Nicoletti,et al.  Is interhemispheric transfer of visuomotor information asymmetric? Evidence from a meta-analysis , 1991, Neuropsychologia.

[6]  Tatsuya Asai,et al.  Hemispheric Asymmetry of Frequency-Dependent Suppression in the Ipsilateral Primary Motor Cortex During Finger Movement: A Functional Magnetic Resonance Imaging Study , 2008, Cerebral cortex.

[7]  Robert L. Sainburg,et al.  Handedness: Differential Specializations for Control of Trajectory and Position , 2005, Exercise and sport sciences reviews.

[8]  Julie Duque,et al.  Intermanual Differences in Movement-related Interhemispheric Inhibition , 2007, Journal of Cognitive Neuroscience.

[9]  L M Harrison,et al.  Evidence for bilateral innervation of certain homologous motoneurone pools in man. , 1994, The Journal of physiology.

[10]  Nicolas Cherbuin,et al.  Efficiency of callosal transfer and hemispheric interaction. , 2006, Neuropsychology.

[11]  R. Davidson,et al.  Visual evoked potential measures of interhemispheric transfer time in humans. , 1989, Behavioral neuroscience.

[12]  J. Régis,et al.  Effects of handedness and sex on the morphology of the corpus callosum: A study with brain magnetic resonance imaging , 1991, Brain and Cognition.

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

[14]  G. Thickbroom,et al.  Transcranial magnetic stimulation mapping of the motor cortex in normal subjects The representation of two intrinsic hand muscles , 1993, Journal of the Neurological Sciences.

[15]  L. Jäncke,et al.  Extensive training of elementary finger tapping movements changes the pattern of motor cortex excitability , 2006, Experimental Brain Research.

[16]  Aimee J Nelson,et al.  Bi-directional interhemispheric inhibition during unimanual sustained contractions , 2009, BMC Neuroscience.

[17]  P M Rossini,et al.  Interhemispheric differences of hand muscle representation in human motor cortex , 1997, Muscle & nerve.

[18]  D. Perani,et al.  Interhemispheric transmission of visuomotor information in humans: fMRI evidence. , 2002, Journal of neurophysiology.

[19]  S. Small,et al.  Lateralization of motor circuits and handedness during finger movements , 2001, European journal of neurology.

[20]  Didier Cros,et al.  Physiological motor asymmetry in human handedness: evidence from transcranial magnetic stimulation , 1994, Brain Research.

[21]  Virgil G Mathiowetz,et al.  The Purdue Pegboard , 1986 .

[22]  S. F. Witelson Hand and sex differences in the isthmus and genu of the human corpus callosum. A postmortem morphological study. , 1989, Brain : a journal of neurology.

[23]  T. Wüstenberg,et al.  Asymmetry of cortical activation during maximum and convenient tapping speed , 2004, Neuroscience Letters.

[24]  Samuel W. Fernberger,et al.  Reaction Time To Retinal Stimulation: With Special Reference To The Time Lost In Conduction Through Nerve Centers... , 2009 .

[25]  Hartwig R. Siebner,et al.  Long-Term Consequences of Switching Handedness: A Positron Emission Tomography Study on Handwriting in “Converted” Left-Handers , 2002, The Journal of Neuroscience.

[26]  C. Marzi The Poffenberger paradigm: a first, simple, behavioural tool to study interhemispheric transmission in humans , 1999, Brain Research Bulletin.

[27]  M. Annett Handedness and cerebral dominance: the right shift theory. , 1998, The Journal of neuropsychiatry and clinical neurosciences.

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

[29]  M. Hallett,et al.  Cortical motor representation of the ipsilateral hand and arm , 2004, Experimental Brain Research.

[30]  S. F. Witelson The brain connection: the corpus callosum is larger in left-handers. , 1985, Science.

[31]  Daniel J. Goble,et al.  Proprioceptive target matching asymmetries in left-handed individuals , 2009, Experimental Brain Research.

[32]  Dequan Wang,et al.  Ipsilateral responses of motor evoked potential correlated with the motor functional outcomes after cortical resection. , 2009, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[34]  S. Folstein,et al.  "Mini-mental state". A practical method for grading the cognitive state of patients for the clinician. , 1975, Journal of psychiatric research.

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

[36]  H. Kuypers,et al.  Cerebral control of contralateral and ipsilateral arm, hand and finger movements in the split-brain rhesus monkey. , 1973, Brain : a journal of neurology.

[37]  Paul M. Thompson,et al.  When more is less: Associations between corpus callosum size and handedness lateralization , 2010, NeuroImage.

[38]  B. Day,et al.  Interhemispheric inhibition of the human motor cortex. , 1992, The Journal of physiology.

[39]  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.

[40]  S. Swinnen,et al.  Dynamics of hemispheric specialization and integration in the context of motor control , 2006, Nature Reviews Neuroscience.

[41]  Robert L. Sainburg,et al.  Hemispheric specialization and functional impact of ipsilesional deficits in movement coordination and accuracy , 2009, Neuropsychologia.

[42]  M. Peters,et al.  The Parallel Brain: The Cognitive Neuroscience of the Corpus Callosum , 2004 .

[43]  W. Triggs,et al.  Hand preference and transcranial magnetic stimulation asymmetry of cortical motor representation , 1999, Brain Research.

[44]  M. Hallett,et al.  Noninvasive mapping of muscle representations in human motor cortex. , 1992, Electroencephalography and clinical neurophysiology.

[45]  R. Nicoletti,et al.  Left-right asymmetry of callosal transfer in normal human subjects , 1994, Behavioural Brain Research.

[46]  G. Hynd,et al.  The Role of the Corpus Callosum in Interhemispheric Transfer of Information: Excitation or Inhibition? , 2005, Neuropsychology Review.

[47]  J. Netz,et al.  Asymmetry in transcallosal inhibition. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[48]  Sam Silverman,et al.  THE RHESUS MONKEY , 1982 .

[49]  Julie Duque,et al.  Transcallosal inhibition in chronic subcortical stroke , 2005, NeuroImage.

[50]  U. Ziemann,et al.  Differences of the ipsilateral silent period in small hand muscles , 2006, Muscle & nerve.

[51]  D. Muller,et al.  Ontogeny of ipsilateral corticospinal projections: A developmental study with transcranial magnetic stimulation , 1997, Annals of neurology.

[52]  F. Fazio,et al.  Pathways of interhemispheric transfer in normals and in a split-brain subject A positron emission tomography study , 1999, Experimental Brain Research.

[53]  J. Tiffin,et al.  The Purdue pegboard; norms and studies of reliability and validity. , 1948, The Journal of applied psychology.

[54]  A Schnitzler,et al.  Handedness and asymmetry of hand representation in human motor cortex. , 1998, Journal of neurophysiology.

[55]  R. Carson Neural pathways mediating bilateral interactions between the upper limbs , 2005, Brain Research Reviews.

[56]  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.

[57]  P. Bawa,et al.  Bilateral responses of upper limb muscles to transcranial magnetic stimulation in human subjects , 2004, Experimental Brain Research.

[58]  M. A. Gresty,et al.  Influence of whole-body pitch tilt and kinesthetic cues on the perceived gravity-referenced eye level , 2004, Experimental Brain Research.

[59]  Rachael Seidler,et al.  Degree of handedness affects intermanual transfer of skill learning , 2008, Experimental Brain Research.

[60]  D. Goble,et al.  The biological and behavioral basis of upper limb asymmetries in sensorimotor performance , 2008, Neuroscience & Biobehavioral Reviews.

[61]  K. Heilman,et al.  Ipsilateral motor activation during unimanual and bimanual motor tasks , 2007, Clinical Neurophysiology.

[62]  René Westerhausen,et al.  Effects of handedness and gender on macro- and microstructure of the corpus callosum and its subregions: a combined high-resolution and diffusion-tensor MRI study. , 2004, Brain research. Cognitive brain research.

[63]  Aysenil Belger,et al.  Interhemispheric Interaction: How Do the Hemispheres Divide and Conquer a Task? , 1990, Cortex.

[64]  M. Hallett,et al.  Hemispheric asymmetry of ipsilateral motor cortex activation during unimanual motor tasks: further evidence for motor dominance , 2001, Clinical Neurophysiology.

[65]  E. Mulvey,et al.  Regression analyses of counts and rates: Poisson, overdispersed Poisson, and negative binomial models. , 1995, Psychological bulletin.

[66]  Robert L. Sainburg,et al.  Interlimb transfer of visuomotor rotations depends on handedness , 2006, Experimental Brain Research.

[67]  Vincenzo Romei,et al.  Handedness is mainly associated with an asymmetry of corticospinal excitability and not of transcallosal inhibition , 2004, Clinical Neurophysiology.

[68]  B. Meyer,et al.  Inhibitory and excitatory interhemispheric transfers between motor cortical areas in normal humans and patients with abnormalities of the corpus callosum. , 1995, Brain : a journal of neurology.

[69]  Robert L Sainburg,et al.  Ipsilesional motor deficits following stroke reflect hemispheric specializations for movement control. , 2007, Brain : a journal of neurology.