Contribution of the motor system to the perception of reachable space: an fMRI study

The present functional magnetic resonance imaging (fMRI) study investigates the neural correlates of reachability judgements. In a block design experiment, 14 healthy participants judged whether a visual target presented at different distances in a virtual environment display was reachable or not with the right hand. In two control tasks, they judged the colour or the relative position of the visual target according to flankers. Contrasting the activations registered in the reachability judgement task and in the control tasks, we found activations in the frontal structures, and in the bilateral inferior and superior parietal lobe, including the precuneus, and the bilateral cerebellum. This fronto‐parietal network including the cerebellum overlaps with the brain network usually activated during actual motor production and motor imagery. In a following event‐related design experiment, we contrasted brain activations when targets were rated as ‘reachable’ with those when they were rated as ‘unreachable’. We found activations in the left premotor cortex, the bilateral frontal structures, and the left middle temporal gyrus. At a lower threshold, we also found activations in the left motor cortex, and in the bilateral cerebellum. Given that reaction time increased with target distance in reachable space, we performed a subsequent parametric analysis that revealed a related increase of activity in the fronto‐parietal network including the cerebellum. Unreachable targets did not show similar activation, and particularly in regions associated to motor production and motor imagery. Taken together, these results suggest that dynamical motor representations used to determine what is reachable are also part of the perceptual process leading to the distinct representation of peripersonal and extrapersonal spaces.

[1]  Daniel P. Kennedy,et al.  Personal Space Regulation by the Human Amygdala , 2009, Nature Neuroscience.

[2]  Fausta Lui,et al.  Does It Look Painful or Disgusting? Ask Your Parietal and Cingulate Cortex , 2008, The Journal of Neuroscience.

[3]  F. Previc.  The neuropsychology of 3-D space. , 1998, Psychological bulletin.

[4]  Claus Lamm,et al.  Predicting the actions of others taps into one's own somatosensory representations—A functional MRI study , 2007, Neuropsychologia.

[5]  Marcello Costantini,et al.  Grasping affordances with the other's hand: a TMS study. , 2013, Social cognitive and affective neuroscience.

[6]  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.

[7]  Brett R Fajen,et al.  Perceiving Possibilities for Action: On the Necessity of Calibration and Perceptual Learning for the Visual Guidance of Action , 2005, Perception.

[8]  Carl Gabbard,et al.  Perceived Reachability in Single- and Multiple-Degree-of-Freedom Workspaces , 2006, Journal of motor behavior.

[9]  M. Diamond,et al.  Primary Motor and Sensory Cortex Activation during Motor Performance and Motor Imagery: A Functional Magnetic Resonance Imaging Study , 1996, The Journal of Neuroscience.

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

[11]  C. Kennard,et al.  Human Medial Frontal Cortex Mediates Unconscious Inhibition of Voluntary Action , 2007, Neuron.

[12]  Y. Rossetti,et al.  Optic ataxia and the function of the dorsal stream: Contributions to perception and action , 2009, Neuropsychologia.

[13]  Alan Cowey,et al.  Spatial neglect in near and far space investigated by repetitive transcranial magnetic stimulation. , 2002, Brain : a journal of neurology.

[14]  H. Alkadhi,et al.  Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. , 1997, Brain : a journal of neurology.

[15]  M. Jeannerod.  Neural Simulation of Action: A Unifying Mechanism for Motor Cognition , 2001, NeuroImage.

[16]  Eiichi Naito,et al.  Human limb‐specific and non‐limb‐specific brain representations during kinesthetic illusory movements of the upper and lower extremities , 2007, The European journal of neuroscience.

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

[18]  P. Roland,et al.  I Feel My Hand Moving A New Role of the Primary Motor Cortex in Somatic Perception of Limb Movement , 2002, Neuron.

[19]  S. Robinovitch,et al.  Perception of postural limits during reaching. , 1998, Journal of motor behavior.

[20]  Giuseppe Vallar,et al.  The Cognitive and Neural Bases of Spatial Neglect , 2002 .

[21]  Ravi S. Menon,et al.  Functional imaging of human motor cortex at high magnetic field. , 1993, Journal of neurophysiology.

[22]  D. Wolpert,et al.  The cerebellum is involved in predicting the sensory consequences of action , 1999, Neuroreport.

[23]  Daniel M. Corcos,et al.  Three-dimensional locations and boundaries of motor and premotor cortices as defined by functional brain imaging: A meta-analysis , 2006, NeuroImage.

[24]  G. Rizzolatti,et al.  Coding near and far space , 2002 .

[25]  Mirko Farina.  Perception, action, and consciousness: Sensorimotor Dynamics and Two Visual Systems , 2010 .

[26]  Thomas E. Nichols,et al.  Thresholding of Statistical Maps in Functional Neuroimaging Using the False Discovery Rate , 2002, NeuroImage.

[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]  V. Gallese.  Embodied simulation: From neurons to phenomenal experience , 2005 .

[29]  Yann Coello,et al.  Motor representations and the perception of space: perceptual judgments of the boundary of action space , 2010 .

[30]  D. Proffitt,et al.  Action-specific influences on distance perception: a role for motor simulation. , 2008, Journal of experimental psychology. Human perception and performance.

[31]  M. Hallett,et al.  Functional properties of brain areas associated with motor execution and imagery. , 2003, Journal of neurophysiology.

[32]  Reinoud J. Bootsma,et al.  The Effects of Anxiety on Perceiving the Reachability of Passing Objects , 1992 .

[33]  Ravi S. Menon,et al.  Visually guided grasping produces fMRI activation in dorsal but not ventral stream brain areas , 2003, Experimental Brain Research.

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

[35]  M. Goodale,et al.  FMRI Reveals a Dissociation between Grasping and Perceiving the Size of Real 3D Objects , 2007, PloS one.

[36]  A Farnè,et al.  Dynamic size‐change of hand peripersonal space following tool use , 2000, Neuroreport.

[37]  Jonathan D. Nelson,et al.  Human cortical representations for reaching: Mirror neurons for execution, observation, and imagery , 2007, NeuroImage.

[38]  A. Proverbio.  Tool perception suppresses 10–12Hz μ rhythm of EEG over the somatosensory area , 2012, Biological Psychology.

[39]  L. Parsons,et al.  Use of implicit motor imagery for visual shape discrimination as revealed by PET , 1995, Nature.

[40]  Nicholas P. Holmes,et al.  The body schema and multisensory representation(s) of peripersonal space , 2004, Cognitive Processing.

[41]  W Pieter Medendorp,et al.  Parietofrontal circuits in goal‐oriented behaviour , 2011, The European journal of neuroscience.

[42]  V. Gallese.  The "Conscious" Dorsal Stream: Embodied Simulation and its Role in Space and Action Conscious Awareness , 2007 .

[43]  M. Jeannerod,et al.  Possible involvement of primary motor cortex in mentally simulated movement: a functional magnetic resonance imaging study. , 1996, Neuroreport.

[44]  Yann Coello,et al.  The perception of peripersonal space in right and left brain damage hemiplegic patients , 2014, Front. Hum. Neurosci..

[45]  Jérémy Bourgeois,et al.  Costs and benefits of tool-use on the perception of reachable space. , 2014, Acta psychologica.

[46]  Jody C. Culham,et al.  fMRI reveals a preference for near viewing in the human parieto-occipital cortex , 2007, NeuroImage.

[47]  M. Perenin,et al.  Cortical control of visually guided reaching: evidence from patients with optic ataxia. , 2005, Cerebral cortex.

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

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

[50]  M. Turvey,et al.  Visually perceiving what is reachable. , 1989 .

[51]  R. R. Blake,et al.  Aspiration and Performance in a Simulated Group Atmosphere , 1955 .

[52]  M. Erb,et al.  Activation of Cortical and Cerebellar Motor Areas during Executed and Imagined Hand Movements: An fMRI Study , 1999, Journal of Cognitive Neuroscience.

[53]  K. Heilman,et al.  Neglect of near peripersonal space. Evidence for multidirectional attentional systems in humans. , 1992, Brain : a journal of neurology.

[54]  Mark Hallett,et al.  A functional magnetic resonance imaging study of cortical regions associated with motor task execution and motor ideation in humans , 1995 .

[55]  M. Goldberg,et al.  Space and attention in parietal cortex. , 1999, Annual review of neuroscience.

[56]  Yann Coello,et al.  Space Boundaries in Schizophrenia Voluntary Action for Improved Judgments of Social Distances , 2011 .

[57]  W. Epstein,et al.  Perceiving Distance: A Role of Effort and Intent , 2004, Perception.

[58]  Patrizia Baraldi,et al.  Humor Comprehension and Appreciation: An fMRI Study , 2006, Journal of Cognitive Neuroscience.

[59]  Apostolos P Georgopoulos,et al.  Neural aspects of cognitive motor control , 2000, Current Opinion in Neurobiology.

[60]  Richard J. Brown.  Neuropsychology Mental Structure , 1989 .

[61]  Jérémy Bourgeois,et al.  Effect of visuomotor calibration and uncertainty on the perception of peripersonal space , 2012, Attention, perception & psychophysics.

[62]  Yann Coello,et al.  Effect of structuring the workspace on cognitive and sensorimotor distance estimation: No dissociation between perception and action , 2006, Perception & psychophysics.

[63]  Yann Coello,et al.  Embodiment, spatial categorisation and action , 2007, Consciousness and Cognition.

[64]  Daniel M. Wolpert,et al.  The Cerebellum Contributes to Somatosensory Cortical Activity during Self-Produced Tactile Stimulation , 1999, NeuroImage.

[65]  Joseph S. Gati,et al.  Eye Position Signal Modulates a Human Parietal Pointing Region during Memory-Guided Movements , 2000, The Journal of Neuroscience.

[66]  R. J. Seitz,et al.  A parieto-premotor network for object manipulation: evidence from neuroimaging , 1999, Experimental Brain Research.

[67]  Monica Baciu,et al.  The sensory-motor specificity of taxonomic and thematic conceptual relations: A behavioral and fMRI study , 2009, NeuroImage.

[68]  L S Mark,et al.  Postural dynamics and the preferred critical boundary for visually guided reaching. , 1997, Journal of experimental psychology. Human perception and performance.

[69]  Heft Harry,et al.  A Methodological Note on Overestimates of Reaching Distance: Distinguishing Between Perceptual and Analytical Judgments , 1993 .

[70]  M. Costantini,et al.  Author ' s personal copy Short Communication Which body for embodied cognition ? Affordance and language within actual and perceived reaching space , 2012 .

[71]  M. H. Fischer,et al.  Estimating reachability: Whole body engagement or postural stability? , 2000 .

[72]  Roberta L. Klatzky,et al.  fMRI Investigations of Reaching and Ego Space in Human Superior Parieto-Occipital Cortex , 2008 .

[73]  Masamichi J. Hayashi,et al.  Neural Activity Changes Associated with Impulsive Responding in the Sustained Attention to Response Task , 2013, PloS one.

[74]  Yann Coello,et al.  Reading action word affects the visual perception of biological motion. , 2011, Acta psychologica.

[75]  G Rizzolatti,et al.  The Space Around Us , 1997, Science.

[76]  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 .

[77]  Alex Martin,et al.  Representation of Manipulable Man-Made Objects in the Dorsal Stream , 2000, NeuroImage.

[78]  R. Passingham.  The frontal lobes and voluntary action , 1993 .

[79]  Gaetano Tieri,et al.  Where does an object trigger an action? An investigation about affordances in space , 2010, Experimental Brain Research.

[80]  M. Graziano.  Where is my arm? The relative role of vision and proprioception in the neuronal representation of limb position. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[81]  Yann Coello,et al.  Language and action in cognitive neuroscience , 2012 .

[82]  Jody C Culham,et al.  Is That within Reach? fMRI Reveals That the Human Superior Parieto-Occipital Cortex Encodes Objects Reachable by the Hand , 2009, The Journal of Neuroscience.

[83]  Eric Achten,et al.  Cerebral lateralization of praxis in right‐ and left‐handedness: Same pattern, different strength , 2012, Human brain mapping.

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

[85]  Andrew D. Wilson,et al.  The effect of distance on reaction time in aiming movements , 2007, Experimental Brain Research.

[86]  P. Derambure,et al.  Perceiving What Is Reachable Depends on Motor Representations: Evidence from a Transcranial Magnetic Stimulation Study , 2008, PloS one.