Suppression of the non-dominant motor cortex during bimanual symmetric finger movement: A functional magnetic resonance imaging study

Patterns of bimanual coordination in which homologous muscles are simultaneously active are more stable than those in which homologous muscles are engaged in an alternating fashion. This may be attributable to the stronger involvement of the dominant motor cortex in ipsilateral hand movements via interaction with the non-dominant motor system, known as neural crosstalk. We used functional magnetic resonance imaging to investigate the neural representation of the interhemispheric interaction during bimanual mirror movements. Thirteen right-handed subjects completed four conditions: sequential finger tapping using the right and left index and middle fingers, bimanual mirror and parallel finger tapping. Auditory cues (3 Hz) were used to keep the tapping frequency constant. Task-related activation in the right primary motor cortex was significantly less prominent during mirror than unimanual left-handed movements. This was mirror- and non-dominant side-specific; parallel movements did not cause such a reduction, and the left primary motor cortex showed no such differential activation across the unimanual right, bimanual mirror, and bimanual parallel conditions. Reducing the contralateral innervation of the left hand may increase the fraction of the force command to the left hand coming from the left primary motor cortex, enhancing the neural crosstalk.

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

[2]  Karl J. Friston,et al.  How Many Subjects Constitute a Study? , 1999, NeuroImage.

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

[4]  R. C. Oldfield THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

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

[6]  M. Hallett,et al.  The relative metabolic demand of inhibition and excitation , 2000, Nature.

[7]  Ichiro Kanazawa,et al.  Interhemispheric facilitation of the hand area of the human motor cortex , 1993, Neuroscience Letters.

[8]  K. Zilles,et al.  The role of ventral medial wall motor areas in bimanual co-ordination. A combined lesion and activation study. , 1999, Brain : a journal of neurology.

[9]  R. Ivry,et al.  When two hands are better than one: reduced timing variability during bimanual movements. , 1996, Journal of experimental psychology. Human perception and performance.

[10]  P. Strick,et al.  Cerebellar Loops with Motor Cortex and Prefrontal Cortex of a Nonhuman Primate , 2003, The Journal of Neuroscience.

[11]  F Debaere,et al.  Cerebellar and premotor function in bimanual coordination: parametric neural responses to spatiotemporal complexity and cycling frequency , 2004, NeuroImage.

[12]  G. Bruce Pike,et al.  Hemodynamic and metabolic responses to neuronal inhibition , 2004, NeuroImage.

[13]  Lutz Jäncke,et al.  Bimanual versus unimanual coordination: what makes the difference? , 2004, NeuroImage.

[14]  U. Ziemann,et al.  Hemispheric asymmetry of transcallosal inhibition in man. , 1995, Experimental brain research.

[15]  K. Stephan,et al.  Cerebral midline structures in bimanual coordination , 1999, Experimental Brain Research.

[16]  Daniel Cattaert,et al.  Simulating a neural cross-talk model for between-hand interference during bimanual circle drawing , 1999, Biological Cybernetics.

[17]  D. Harrington,et al.  Limb-Sequencing Deficits After Left but not Right Hemisphere Damage , 1994, Brain and Cognition.

[18]  J C Rothwell,et al.  Comparison of descending volleys evoked by transcranial magnetic and electric stimulation in conscious humans. , 1998, Electroencephalography and clinical neurophysiology.

[19]  Deborah L. Harrington,et al.  The effects of task complexity on motor performance in left and right CVA patients , 1987, Neuropsychologia.

[20]  R. Ivry,et al.  Callosotomy patients exhibit temporal uncoupling during continuous bimanual movements , 2002, Nature Neuroscience.

[21]  S. Swinnen Intermanual coordination: From behavioural principles to neural-network interactions , 2002, Nature Reviews Neuroscience.

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

[23]  Alan Sunderland,et al.  fMRI signal decreases in ipsilateral primary motor cortex during unilateral hand movements are related to duration and side of movement , 2005, NeuroImage.

[24]  Karl J. Friston,et al.  Detecting Activations in PET and fMRI: Levels of Inference and Power , 1996, NeuroImage.

[25]  Natalia Dounskaia,et al.  Egocentric and Allocentric Constraints in the Expression of Patterns of Interlimb Coordination , 1997, Journal of Cognitive Neuroscience.

[26]  Richard B Ivry,et al.  Temporal Control and Coordination: The Multiple Timer Model , 2002, Brain and Cognition.

[27]  P. Matthews,et al.  Functional MRI cerebral activation and deactivation during finger movement , 2000, Neurology.

[28]  J. Kelso Phase transitions and critical behavior in human bimanual coordination. , 1984, The American journal of physiology.

[29]  H. Forssberg,et al.  Neural networks for the coordination of the hands in time. , 2003, Journal of neurophysiology.

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

[31]  N. Sadato,et al.  Role of the Supplementary Motor Area and the Right Premotor Cortex in the Coordination of Bimanual Finger Movements , 1997, The Journal of Neuroscience.

[32]  M. Honda,et al.  Neural correlates of the spontaneous phase transition during bimanual coordination. , 2006, Cerebral cortex.

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

[34]  U. Ziemann,et al.  Hemispheric asymmetry of transcallosalinhibition in man , 2004, Experimental Brain Research.

[35]  M. Wyke,et al.  The effects of brain lesions on the performance of bilateral arm movements. , 1971, Neuropsychologia.

[36]  D. Kimura,et al.  Acquisition of a motor skill after left-hemisphere damage. , 1977, Brain : a journal of neurology.

[37]  W. Prinz,et al.  Perceptual basis of bimanual coordination , 2001, Nature.

[38]  Farsin Hamzei,et al.  Reduction of Excitability (“Inhibition”) in the Ipsilateral Primary Motor Cortex Is Mirrored by fMRI Signal Decreases , 2002, NeuroImage.

[39]  K. Meador,et al.  Functional MRI cerebral activation and deactivation during finger movement , 2000, Neurology.