The Extrastriate Body Area Computes Desired Goal States during Action Planning123

Abstract How do object perception and action interact at a neural level? Here we test the hypothesis that perceptual features, processed by the ventral visuoperceptual stream, are used as priors by the dorsal visuomotor stream to specify goal-directed grasping actions. We present three main findings, which were obtained by combining time-resolved transcranial magnetic stimulation and kinematic tracking of grasp-and-rotate object manipulations, in a group of healthy human participants (N = 22). First, the extrastriate body area (EBA), in the ventral stream, provides an initial structure to motor plans, based on current and desired states of a grasped object and of the grasping hand. Second, the contributions of EBA are earlier in time than those of a caudal intraparietal region known to specify the action plan. Third, the contributions of EBA are particularly important when desired and current object configurations differ, and multiple courses of actions are possible. These findings specify the temporal and functional characteristics for a mechanism that integrates perceptual processing with motor planning.

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

[2]  F. D. de Lange,et al.  Motor planning is facilitated by adopting an action's goal posture: an fMRI study. , 2012, Cerebral cortex.

[3]  M. Candidi,et al.  Representation of body identity and body actions in extrastriate body area and ventral premotor cortex , 2007, Nature Neuroscience.

[4]  Loukia D. Loukopoulos,et al.  Planning reaches by evaluating stored postures. , 1995, Psychological review.

[5]  David A Rosenbaum,et al.  Grasping movement plans , 2006, Psychonomic bulletin & review.

[6]  Dwight J. Kravitz,et al.  The ventral visual pathway: an expanded neural framework for the processing of object quality , 2013, Trends in Cognitive Sciences.

[7]  P. Downing,et al.  The role of occipitotemporal body-selective regions in person perception , 2011, Cognitive neuroscience.

[8]  Joris Vangeneugden,et al.  Distinct Neural Mechanisms for Body Form and Body Motion Discriminations , 2014, The Journal of Neuroscience.

[9]  I. Toni,et al.  Compensatory Activity in the Extrastriate Body Area of Parkinson's Disease Patients , 2012, The Journal of Neuroscience.

[10]  A. Milner,et al.  Delayed reaching and grasping in patients with optic ataxia. , 2003, Progress in brain research.

[11]  M. Corbetta,et al.  Extrastriate body area in human occipital cortex responds to the performance of motor actions , 2004, Nature Neuroscience.

[12]  D. Rosenbaum,et al.  Posture-based motion planning: applications to grasping. , 2001, Psychological review.

[13]  M. Goodale,et al.  Two visual systems re-viewed , 2008, Neuropsychologia.

[14]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.

[15]  Brian N. Pasley,et al.  Transcranial Magnetic Stimulation Elicits Coupled Neural and Hemodynamic Consequences , 2007, Science.

[16]  A. Milner,et al.  Grasping the past delay can improve visuomotor performance , 2001, Current Biology.

[17]  M Desmurget,et al.  Role of the medial part of the intraparietal sulcus in implementing movement direction. , 2012, Cerebral cortex.

[18]  M Jeannerod,et al.  Visual pathways for object-oriented action and object recognition: functional anatomy with PET. , 1997, Cerebral cortex.

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

[20]  Eli Brenner,et al.  Robust movement segmentation by combining multiple sources of information , 2010, Journal of Neuroscience Methods.

[21]  J. Danckert Common Mechanisms in Perception and Action: Attention and Performance XIX Wolfgang Prinz, Bernhard Hommel (Eds.), Oxford University Press, 2002, Price: £ 65.00, ISBN: 0-19-851069 , 2003, Neuropsychologia.

[22]  Rainer Goebel,et al.  Optimizing Functional Accuracy of TMS in Cognitive Studies: A Comparison of Methods , 2009, Journal of Cognitive Neuroscience.

[23]  J. Krakauer,et al.  A computational neuroanatomy for motor control , 2008, Experimental Brain Research.

[24]  D. Wolpert,et al.  Maintaining internal representations: the role of the human superior parietal lobe , 1998, Nature Neuroscience.

[25]  Ivan Toni,et al.  Cortical Dynamics of Sensorimotor Integration during Grasp Planning , 2012, The Journal of Neuroscience.

[26]  T. C. W. Nijboer,et al.  Choosing between alternative wrist postures: Action planning needs perception , 2009, Neuropsychologia.

[27]  J. Ashburner,et al.  Nonlinear spatial normalization using basis functions , 1999, Human brain mapping.

[28]  Bernhard Hommel,et al.  The Functional and Neural Mechanism of Action Preparation: Roles of EBA and FFA in Voluntary Action Control , 2011, Journal of Cognitive Neuroscience.

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

[30]  P. Downing,et al.  The lateral occipitotemporal cortex in action , 2015, Trends in Cognitive Sciences.

[31]  J. Culham,et al.  Neural coding within human brain areas involved in actions , 2015, Current Opinion in Neurobiology.

[32]  Tracy R. Henderson,et al.  Simple metric for scaling motor threshold based on scalp-cortex distance: application to studies using transcranial magnetic stimulation. , 2005, Journal of neurophysiology.

[33]  N. Kanwisher,et al.  The Human Body , 2001 .

[34]  Jody C. Culham,et al.  Ventral and dorsal stream contributions to the online control of immediate and delayed grasping: A TMS approach , 2009, Neuropsychologia.

[35]  A. Caramazza,et al.  Left occipitotemporal cortex contributes to the discrimination of tool-associated hand actions: fMRI and TMS evidence , 2014, Front. Hum. Neurosci..

[36]  D. Rosenbaum,et al.  Cognition, action, and object manipulation. , 2012, Psychological bulletin.

[37]  D. Norris,et al.  BOLD contrast sensitivity enhancement and artifact reduction with multiecho EPI: Parallel‐acquired inhomogeneity‐desensitized fMRI , 2006, Magnetic resonance in medicine.

[38]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[39]  A. Caramazza,et al.  Closely overlapping responses to tools and hands in left lateral occipitotemporal cortex. , 2012, Journal of neurophysiology.

[40]  A. Sack,et al.  Pre-Stimulus Sham TMS Facilitates Target Detection , 2013, PloS one.