Acting alters visual processing: flexible recruitment of visual areas by one's own actions.

Using functional magnetic resonance imaging, we investigated the effect of motor preparation/execution on the activation of visual cortical areas by action observation. We presented videos of human actors performing several fine manipulative actions (e.g., grasping) with the hand or foot, together with appropriate control stimuli. Subjects either responded in a central fixation task with the hand (A) or foot (B) or viewed the stimuli passively (C). Experimental conditions were arranged according to a 2 × 2 × 3 factorial design with action, effector, and response as factors. Bilateral posterior parietal cortex was more strongly activated for action videos compared with controls during active runs (A or B) contrasted with passive runs (C). Two neighboring regions in the right fusiform gyrus (FG) were activated when the effector employed to respond in the task matched that displayed in the videos (A or B), independently of whether the stimulus was an action or a control. Neighboring regions in the right posterior middle temporal gyrus (MTG) were also activated when the effector observed and that used to respond matched (A or B), but only for action videos, not controls. Our results indicate flexible modulation of visual areas during concurrent action observation and action execution/preparation, which was effector specific in the FG and MTG.

[1]  P. Fox,et al.  Intersubject variability of functional areas in the human visual cortex , 1998, Human brain mapping.

[2]  Jody C Culham,et al.  Behavioral / Systems / Cognitive Functional Magnetic Resonance Imaging Reveals the Neural Substrates of Arm Transport and Grip Formation in Reach-to-Grasp Actions in Humans , 2010 .

[3]  C. Galletti,et al.  Wide-Field Retinotopy Defines Human Cortical Visual Area V6 , 2006, The Journal of Neuroscience.

[4]  H. Sakata,et al.  Neural mechanisms of visual guidance of hand action in the parietal cortex of the monkey. , 1995, Cerebral cortex.

[5]  James Stanley,et al.  Functional activation in parieto-premotor and visual areas dependent on congruency between hand movement and visual stimuli during motor-visual priming , 2007, NeuroImage.

[6]  G. Aschersleben,et al.  The Theory of Event Coding (TEC): a framework for perception and action planning. , 2001, The Behavioral and brain sciences.

[7]  G. Luppino,et al.  Cortical connections of the inferior parietal cortical convexity of the macaque monkey. , 2006, Cerebral cortex.

[8]  Penny A. MacDonald,et al.  The role of parietal cortex in awareness of self-generated movements: a transcranial magnetic stimulation study. , 2003, Cerebral cortex.

[9]  F. Plum Handbook of Physiology. , 1960 .

[10]  T. Allison,et al.  Functional anatomy of biological motion perception in posterior temporal cortex: an FMRI study of eye, mouth and hand movements. , 2005, Cerebral cortex.

[11]  G. Rizzolatti,et al.  Action observation activates premotor and parietal areas in a somatotopic manner: an fMRI study , 2001, The European journal of neuroscience.

[12]  G. Orban,et al.  The Retinotopic Organization of the Human Middle Temporal Area MT/V5 and Its Cortical Neighbors , 2010, The Journal of Neuroscience.

[13]  C. Cavina-Pratesi,et al.  Dissociable neural responses to hands and non-hand body parts in human left extrastriate visual cortex. , 2010, Journal of neurophysiology.

[14]  R. Andersen,et al.  Coding of intention in the posterior parietal cortex , 1997, Nature.

[15]  B. Bergum,et al.  Attention and performance IX , 1982 .

[16]  Patrizia Fattori,et al.  The Dorsomedial Pathway Is Not Just for Reaching: Grasping Neurons in the Medial Parieto-Occipital Cortex of the Macaque Monkey , 2010, The Journal of Neuroscience.

[17]  Michael A. Arbib,et al.  Perceptual Structures and Distributed Motor Control , 1981 .

[18]  Paul E. Downing,et al.  Is the extrastriate body area involved in motor actions? , 2005, Nature Neuroscience.

[19]  B. Hommel,et al.  Intentional control of attention: action planning primes action-related stimulus dimensions , 2007, Psychological research.

[20]  G. Rizzolatti,et al.  Two different streams form the dorsal visual system: anatomy and functions , 2003, Experimental Brain Research.

[21]  Johan Wagemans,et al.  Distributed subordinate specificity for bodies, faces, and buildings in human ventral visual cortex , 2010, NeuroImage.

[22]  G. Rizzolatti,et al.  Action for perception: a motor-visual attentional effect. , 1999, Journal of experimental psychology. Human perception and performance.

[23]  Aina Puce,et al.  Common and distinct brain activation to viewing dynamic sequences of face and hand movements , 2007, NeuroImage.

[24]  Uta Frith,et al.  Your Own Action Influences How You Perceive Another Person's Action , 2004, Current Biology.

[25]  Karl J. Friston,et al.  Generalisability, Random Effects & Population Inference , 1998, NeuroImage.

[26]  Alan C. Evans,et al.  A new anatomical landmark for reliable identification of human area V5/MT: a quantitative analysis of sulcal patterning. , 2000, Cerebral cortex.

[27]  Margaret Wilson,et al.  The mirror reflects both ways: Action influences perception of others , 2010, Brain and Cognition.

[28]  R. Andersen,et al.  Functional analysis of human MT and related visual cortical areas using magnetic resonance imaging , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  A. Murata,et al.  Cortical connections of the macaque anterior intraparietal (AIP) area. , 2008, Cerebral cortex.

[30]  Rebecca F. Schwarzlose,et al.  Separate face and body selectivity on the fusiform gyrus. , 2010, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  C. Galletti,et al.  Role of the medial parieto-occipital cortex in the control of reaching and grasping movements , 2003, Experimental Brain Research.

[32]  J C Mazziotta,et al.  Reafferent copies of imitated actions in the right superior temporal cortex , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[33]  N. Kanwisher,et al.  The Fusiform Face Area: A Module in Human Extrastriate Cortex Specialized for Face Perception , 1997, The Journal of Neuroscience.

[34]  G. Orban,et al.  Extracting 3D from Motion: Differences in Human and Monkey Intraparietal Cortex , 2002, Science.

[35]  P. Downing,et al.  Selectivity for the human body in the fusiform gyrus. , 2005, Journal of neurophysiology.

[36]  C. Galletti,et al.  Occipital (V6) and parietal (V6A) areas in the anterior wall of the parieto‐occipital sulcus of the macaque: a cytoarchitectonic study , 2005, The European journal of neuroscience.

[37]  Michael Erb,et al.  The neural correlates of perceiving one's own movements , 2003, NeuroImage.

[38]  A. Meltzoff,et al.  An fMRI study of imitation: action representation and body schema , 2005, Neuropsychologia.

[39]  G. Orban,et al.  Coding observed motor acts: different organizational principles in the parietal and premotor cortex of humans. , 2010, Journal of neurophysiology.

[40]  D. V. van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex. , 2005, NeuroImage.

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

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

[43]  J. Marshall,et al.  The neural consequences of conflict between intention and the senses. , 1999, Brain : a journal of neurology.

[44]  M. Tarr,et al.  The Fusiform Face Area is Part of a Network that Processes Faces at the Individual Level , 2000, Journal of Cognitive Neuroscience.

[45]  G. Orban,et al.  Human Functional Magnetic Resonance Imaging Reveals Separation and Integration of Shape and Motion Cues in Biological Motion Processing , 2009, The Journal of Neuroscience.

[46]  R.N.Dej.,et al.  The Cerebral Cortex of Man , 1951, Neurology.

[47]  M. Jeannerod Intersegmental coordination during reaching at natural visual objects , 1981 .

[48]  A. Georgopoulos,et al.  Parietal cortex neurons of the monkey related to the visual guidance of hand movement , 1990, Experimental Brain Research.

[49]  Aina Puce,et al.  Viewing the motion of human body parts activates different regions of premotor, temporal, and parietal cortex , 2004, NeuroImage.

[50]  E. Zohary,et al.  Topographic Representation of the Human Body in the Occipitotemporal Cortex , 2010, Neuron.

[51]  Alison J. Wiggett,et al.  Dissociation of extrastriate body and biological-motion selective areas by manipulation of visual-motor congruency , 2009, Neuropsychologia.

[52]  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.

[53]  Maurizio Corbetta,et al.  Is the extrastriate body area involved in motor actions? , 2005, Nature Neuroscience.

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

[55]  Guy A. Orban,et al.  Integration of shape and motion cues in biological motion processing in the monkey STS , 2012, NeuroImage.

[56]  David C. Van Essen,et al.  A Population-Average, Landmark- and Surface-based (PALS) atlas of human cerebral cortex , 2005, NeuroImage.

[57]  Thomas E. Nichols,et al.  Everything You Never Wanted to Know about Circular Analysis, but Were Afraid to Ask , 2010, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[58]  Justin L. Gardner,et al.  Executed and Observed Movements Have Different Distributed Representations in Human aIPS , 2008, The Journal of Neuroscience.

[59]  R. Miall,et al.  Performing hand actions assists the visual discrimination of similar hand postures , 2006, Neuropsychologia.