Hemispheric asymmetries in goal-directed hand movements are independent of hand preference

Asymmetries in the kinematics and neural substrates of voluntary right and left eye-hand coordinated movements have been accredited to differential hemispheric specialization. An alternative explanation for between-hand movement differences could result from hand preference related effects. To test both assumptions, an experiment was conducted with left- and right-handers performing goal-directed movements with either hand paced by a metronome. Spatiotemporal accuracy was comparable between hands, whereas hand peak velocity was reached earlier when moving with the left compared to the right hand. The underlying brain activation patterns showed that both left- and right-handers activated more areas involved in visuomotor attention and saccadic control when using their left compared to the right hand. Altogether, these results confirm a unique perceptuomotor processing specialization of the left brain/right hand system that is independent of hand preference.

[1]  Nicole Wenderoth,et al.  Hemispheric asymmetries of motor versus nonmotor processes during (visuo)motor control , 2011, Human brain mapping.

[2]  I. Toni,et al.  Integration of target and effector information in the human brain during reach planning. , 2007, Journal of neurophysiology.

[3]  R Kawashima,et al.  Functional asymmetry of cortical motor control in left‐handed subjects , 1997, Neuroreport.

[4]  Scott T. Grafton,et al.  Motor task difficulty and brain activity: investigation of goal-directed reciprocal aiming using positron emission tomography. , 1997, Journal of neurophysiology.

[5]  Tzvi Ganel,et al.  Hemispheric specialization for the visual control of action is independent of handedness. , 2006, Journal of neurophysiology.

[6]  L. Jäncke,et al.  The Effect of Finger-Movement Speed of the Dominant and the Subdominant Hand on Cerebellar Activation: A Functional Magnetic Resonance Imaging Study , 1999, NeuroImage.

[7]  A. Toga,et al.  Mapping brain asymmetry , 2003, Nature Reviews Neuroscience.

[8]  Ronald R. Peeters,et al.  Hemispheric asymmetries in eye–hand coordination , 2008, NeuroImage.

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

[10]  W. Helsen,et al.  Temporal and spatial coupling of point of gaze and hand movements in aiming. , 1998, Journal of motor behavior.

[11]  Romeo Chua,et al.  The Influence of Target Perturbation on Manual Aiming Asymmetries in Right-Handers , 1995, Cortex.

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

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

[14]  S. Lehéricy,et al.  Foot, hand, face and eye representation in the human striatum. , 2003, Cerebral cortex.

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

[16]  Digby Elliott,et al.  Manual Asymmetries and Saccadic Eye Movements in Right-Handers During Single and Reciprocal Aiming Movements , 1998, Cortex.

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

[18]  Scott T. Grafton,et al.  Human functional anatomy of visually guided finger movements. , 1992, Brain : a journal of neurology.

[19]  R. Ivry,et al.  Ipsilateral motor cortex activity during unimanual hand movements relates to task complexity. , 2005, Journal of neurophysiology.

[20]  W. Helsen,et al.  Coupling of Eye, Finger, Elbow, and Shoulder Movements During Manual Aiming , 2000, Journal of motor behavior.

[21]  W. Helsen,et al.  The Control of Sequential Aiming Movements: The Influence of Practice and Manual Asymmetries On the One-Target Advantage , 2003, Cortex.

[22]  Matthew Heath,et al.  The control of goal-directed limb movements: Correcting errors in the trajectory , 1999 .

[23]  M. Corballis,et al.  Influence of Task Complexity on Manual Asymmetries , 2004, Cortex.

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

[25]  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.

[26]  H. Kennedy,et al.  Two Cortical Systems for Reaching in Central and Peripheral Vision , 2005, Neuron.

[27]  K M Heilman,et al.  Hand preference and magnetic resonance imaging asymmetries of the central sulcus. , 1998, Neuropsychiatry, neuropsychology, and behavioral neurology.

[28]  V. Nougier,et al.  Manual Asymmetries in Reaching Movement Control. II: Study of Left-Handers , 2001, Cortex.

[29]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[31]  D Elliott,et al.  Eye—Hand Coordination Asymmetries in Manual Aiming , 2007, Journal of motor behavior.

[32]  J. Binder,et al.  Distributed Neural Systems Underlying the Timing of Movements , 1997, The Journal of Neuroscience.

[33]  K Ugurbil,et al.  Activation of visuomotor systems during visually guided movements: a functional MRI study. , 1998, Journal of magnetic resonance.

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

[35]  S. Swinnen,et al.  Neural correlates of motor dysfunction in children with traumatic brain injury: exploration of compensatory recruitment patterns. , 2009, Brain : a journal of neurology.

[36]  K. Amunts,et al.  Interhemispheric asymmetry of the human motor cortex related to handedness and gender , 2000, Neuropsychologia.

[37]  Philippe S. Archambault,et al.  The cortical network for eye–hand coordination and its relevance to understanding motor disorders of parietal patients , 2006, Neuropsychologia.

[38]  Örjan Blom,et al.  The dorsal auditory pathway is involved in performance of both visual and auditory rhythms , 2009, NeuroImage.

[39]  W. Helsen,et al.  The type of visual information mediates eye and hand movement bias when aiming to a Müller–Lyer illusion , 2006, Experimental Brain Research.

[40]  M. Corbetta,et al.  Functional Organization of Human Intraparietal and Frontal Cortex for Attending, Looking, and Pointing , 2003, The Journal of Neuroscience.

[41]  B. Knowlton,et al.  Learning and memory functions of the Basal Ganglia. , 2002, Annual review of neuroscience.

[42]  E. A. Roy,et al.  Kinematic Analyses of Manual Asymmetries in Visual Aiming Movements , 1994, Brain and Cognition.

[43]  R. Turner,et al.  Characterizing Dynamic Brain Responses with fMRI: A Multivariate Approach , 1995, NeuroImage.

[44]  Takashi Hanakawa,et al.  Functional coupling underlying motor and cognitive functions of the dorsal premotor cortex , 2009, Behavioural Brain Research.

[45]  Laure Zago,et al.  Functional asymmetries revealed in visually guided saccades: an FMRI study. , 2009, Journal of neurophysiology.

[46]  J. Culham,et al.  The role of parietal cortex in visuomotor control: What have we learned from neuroimaging? , 2006, Neuropsychologia.

[47]  Roel M. Willems,et al.  Hand preference influences neural correlates of action observation , 2009, Brain Research.

[48]  Ivan Toni,et al.  Information processing in human parieto-frontal circuits during goal-directed bimanual movements , 2006, NeuroImage.

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

[50]  W. Helsen,et al.  Eye-Hand Coordination in Goal-Directed Action: Normal and Pathological Functioning , 2010 .

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

[52]  Digby Elliott,et al.  Hand, Space and Attentional Asymmetries in Goal-Directed Manual Aiming * * Presented at the Canadian Society for Psychomotor Learning and Sport Psychology (SCAPPS), Vancouver, B.C., Canada. October 1995. , 1997, Cortex.

[53]  W. Helsen,et al.  Vision and Laterality: Does Occlusion Disclose a Feedback Processing Advantage for the Right Hand System? , 2000, Cortex.

[54]  S. Swinnen,et al.  Neural Basis of Aging: The Penetration of Cognition into Action Control , 2005, The Journal of Neuroscience.

[55]  V. Nougier,et al.  Manual Asymmetries in Reaching Movement Control. I: Study of Right-Handers , 2001, Cortex.

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

[57]  Digby Elliott,et al.  A ménage À trois: the eye, the hand and on-line processing , 2002, Journal of sports sciences.

[58]  D. Elliott,et al.  The Preparation of Aiming Movements , 1995, Brain and Cognition.