Parietal rTMS Disrupts the Initiation but not the Execution of On-line Adjustments to a Perturbation of Object Size

Previous studies have implicated the human parietal lobes in the on-line guidance of action. However, no study to date has examined at what stage in the on-line adjustment process do the parietal lobes play their most critical role. Repetitive transcranial magnetic stimulation (rTMS) was applied over the left intraparietal sulcus as participants reached to grasp a small or large illuminated cylinder. On some trials, the illumination could suddenly switch from the small to large cylinder, or vice-versa. SmallLarge switches were associated with relatively early grip aperture adjustments, whereas LargeSmall switches were associated with relatively late grip aperture adjustments. When rTMS was applied early in the movement, it disrupted on-line adjustments to SmallLarge target switches, but not to LargeSmall switches. Conversely, when rTMS was applied late in the movement, it disrupted adjustments to LargeSmall target switches but not to SmallLarge switches. The timing of the disruption by rTMS appeared linked to the initiation of the adjustment. It was concluded that the left parietal lobe plays a critical role in initiating an on-line adjustment to a change in target size, but not in executing that adjustment. The implications of these results for current views of on-line control are discussed.

[1]  K. Zilles,et al.  Differential Involvement of Parietal and Precentral Regions in Movement Preparation and Motor Intention , 2002, The Journal of Neuroscience.

[2]  S. Glover,et al.  Separate visual representations in the planning and control of action , 2004, Behavioral and Brain Sciences.

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

[4]  U. Castiello.  The neuroscience of grasping , 2005, Nature Reviews Neuroscience.

[5]  R. E. Passingham,et al.  Parietal cortex and movement I. Movement selection and reaching , 1997, Experimental Brain Research.

[6]  G. Fink,et al.  REVIEW: The functional organization of the intraparietal sulcus in humans and monkeys , 2005, Journal of anatomy.

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

[8]  M. Jeannerod.  The timing of natural prehension movements. , 1984, Journal of motor behavior.

[9]  Scott T. Grafton,et al.  Role of the posterior parietal cortex in updating reaching movements to a visual target , 1999, Nature Neuroscience.

[10]  Kenneth F. Valyear,et al.  Human parietal cortex in action , 2006, Current Opinion in Neurobiology.

[11]  C. C. A. M. Gielen,et al.  Conditions determining early modification of motor programmes in response to changes in target location , 2004, Experimental Brain Research.

[12]  M. Desmurget,et al.  An ‘automatic pilot’ for the hand in human posterior parietal cortex: toward reinterpreting optic ataxia , 2000, Nature Neuroscience.

[13]  D. Collins,et al.  Automatic 3D Intersubject Registration of MR Volumetric Data in Standardized Talairach Space , 1994, Journal of computer assisted tomography.

[14]  C. Prablanc,et al.  Large adjustments in visually guided reaching do not depend on vision of the hand or perception of target displacement , 1986, Nature.

[15]  A. Wing,et al.  Grasp size and accuracy of approach in reaching. , 1986, Journal of motor behavior.

[16]  Scott T. Grafton,et al.  A lesion of the posterior parietal cortex disrupts on-line adjustments during aiming movements , 2002, Neuropsychologia.

[17]  Scott T. Grafton,et al.  Forward modeling allows feedback control for fast reaching movements , 2000, Trends in Cognitive Sciences.

[18]  U. Castiello,et al.  Reach to grasp: the natural response to perturbation of object size , 2004, Experimental Brain Research.

[19]  J. Kalaska,et al.  Deciding not to GO: neuronal correlates of response selection in a GO/NOGO task in primate premotor and parietal cortex. , 1995, Cerebral cortex.

[20]  D. Wolpert,et al.  Is the cerebellum a smith predictor? , 1993, Journal of motor behavior.

[21]  D. Pandya,et al.  Anatomical investigation of projections to the basis pontis from posterior parietal association cortices in rhesus monkey , 1989, The Journal of comparative neurology.

[22]  C Dohle,et al.  Human anterior intraparietal area subserves prehension , 1998, Neurology.

[23]  D. Meyer,et al.  Conditions for a Linear Speed-Accuracy Trade-Off in Aimed Movements , 1983, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[24]  B. P. McCloskey,et al.  Knowledge about hand shaping and knowledge about objects. , 1987, Journal of motor behavior.

[25]  M. Jeannerod,et al.  Selective perturbation of visual input during prehension movements , 2004, Experimental Brain Research.

[26]  M. Jeannerod,et al.  Measuring time to awareness , 1991, Neuroreport.

[27]  Scott T. Grafton,et al.  Functional Anatomy of Nonvisual Feedback Loops during Reaching: A Positron Emission Tomography Study , 2001, The Journal of Neuroscience.

[28]  Scott T. Grafton,et al.  Virtual lesions of the anterior intraparietal area disrupt goal-dependent on-line adjustments of grasp , 2005, Nature Neuroscience.

[29]  G. Rizzolatti,et al.  Localization of grasp representations in humans by PET: 1. Observation versus execution , 1996, Experimental Brain Research.

[30]  Scott Glover,et al.  Optic ataxia as a deficit specific to the on-line control of actions , 2003, Neuroscience & Biobehavioral Reviews.

[31]  R. Klatzky.  The role of motor representations in semantic sensibility judgments , 1989 .

[32]  E. R. Crossman,et al.  Feedback Control of Hand-Movement and Fitts' Law , 1983, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[34]  Zoubin Ghahramani,et al.  Computational principles of movement neuroscience , 2000, Nature Neuroscience.

[35]  A. Wing,et al.  The Contribution of the Thumb to Reaching Movements , 1983, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[36]  M. Jeannerod,et al.  Selective perturbation of visual input during prehension movements , 1991, Experimental Brain Research.

[37]  J. Seal,et al.  Activity of neurons in area 5 during a simple arm movement in monkeys before and after deafferentation of the trained limb , 1982, Brain Research.

[38]  Scott T. Grafton,et al.  Localization of grasp representations in humans by positron emission tomography , 1996, Experimental Brain Research.

[39]  Accepted April,et al.  Factors affecting higher-order movement planning: a kinematic analysis of human prehension , 1991 .

[40]  M. Jeannerod,et al.  Perception of self-generated movement following left parietal lesion. , 1999, Brain : a journal of neurology.

[41]  G. J. Savelsbergh,et al.  Grasping tau. , 1991, Journal of experimental psychology. Human perception and performance.

[42]  R A Abrams,et al.  Optimality in human motor performance: ideal control of rapid aimed movements. , 1988, Psychological review.

[43]  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 .

[44]  M. Brammer,et al.  Progressive increase of frontostriatal brain activation from childhood to adulthood during event‐related tasks of cognitive control , 2006, Human brain mapping.

[45]  Leonardo G Cohen,et al.  Noninvasive cortical stimulation in neurorehabilitation: a review. , 2006, Archives of Physical Medicine and Rehabilitation.

[46]  Robert Sessions Woodworth,et al.  THE ACCURACY OF VOLUNTARY MOVEMENT , 1899 .

[47]  Richard A. Andersen,et al.  FMRI evidence for a 'parietal reach region' in the human brain , 2003, Experimental Brain Research.

[48]  Michael I. Jordan,et al.  An internal model for sensorimotor integration. , 1995, Science.

[49]  Ravi S. Menon,et al.  A comparison of frontoparietal fMRI activation during anti-saccades and anti-pointing. , 2000, Journal of neurophysiology.

[50]  R C Miall,et al.  The cerebellum, predictive control and motor coordination. , 2007, Novartis Foundation symposium.

[51]  P. Dixon,et al.  Semantics affect the planning but not control of grasping , 2002, Experimental Brain Research.