Kobe University Repository : Kernel Tit le Temporal dynamics of neural act ivity underlyingunconscious processing of manipulable objects

Brief running title: Unconscious processing of tool images Number of figures: 5 (with 2 tables) Number of pages: 35 (including figure legends) Abstract The primate visual system is assumed to comprise two main pathways: a ventral pathway for shape and color perception and a dorsal pathway for spatial processing and visuomotor control. Previous studies consistently reported strong activation in the dorsal pathway (especially in the inferior parietal region) induced by manipulable object images such as tools. However, it is controversial whether the dorsal pathway retains this preferential activity to tool images under unconscious perception. In the present study, we used magnetoencephalography (MEG) and investigated spatio-temporal dynamics of neural responses to visible and invisible tool images. A presentation of visible tool images elicited a strong neural response over the parietal regions in the left hemisphere peaking at 400 ms. This response unique to the processing of tool information in the left parietal regions was still observed when conscious perception of tool images was inhibited by interocular suppression. Furthermore, analyses of neural oscillation signals revealed a suppression of μ rhythm (8 – 13 Hz), a neural index of movement execution or imagery, induced by both visible and invisible tools. Those results indicated that the neural circuit to process the tool information was preserved under unconscious perception, highlighting an implicit aspect of the dorsal pathway.

[1]  F. Binkofski,et al.  Two action systems in the human brain , 2013, Brain and Language.

[2]  Michael Andres,et al.  Distinct contribution of the parietal and temporal cortex to hand configuration and contextual judgements about tools , 2013, Cortex.

[3]  Y. Noguchi,et al.  Unconscious processing of direct gaze: Evidence from an ERP study , 2013, Neuropsychologia.

[4]  Riitta Hari,et al.  Coherence between magnetoencephalography and hand-action-related acceleration, force, pressure, and electromyogram , 2013, NeuroImage.

[5]  Yasuki Noguchi,et al.  Reversal of the face-inversion effect in N170 under unconscious visual processing , 2013, Neuropsychologia.

[6]  Marc Brysbaert,et al.  Praxis and language are linked: Evidence from co-lateralization in individuals with atypical language dominance , 2013, Cortex.

[7]  Shinichi Kita,et al.  Temporal Dynamics of Neural Activity at the Moment of Emergence of Conscious Percept , 2012, Journal of Cognitive Neuroscience.

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

[9]  A. Milner,et al.  Is visual processing in the dorsal stream accessible to consciousness? , 2012, Proceedings of the Royal Society B: Biological Sciences.

[10]  A. Oliva,et al.  A Real-World Size Organization of Object Responses in Occipitotemporal Cortex , 2012, Neuron.

[11]  R. Malach,et al.  The link between fMRI-BOLD activation and perceptual awareness is "stream-invariant" in the human visual system. , 2011, Cerebral cortex.

[12]  Brian J. Murphy,et al.  Intercepting the First Pass: Rapid Categorization is Suppressed for Unseen Stimuli , 2011, Front. Psychology.

[13]  Galit Yovel,et al.  Why is the N170 enhanced for inverted faces? An ERP competition experiment , 2010, NeuroImage.

[14]  Alice Mado Proverbio,et al.  Face Coding Is Bilateral in the Female Brain , 2010, PloS one.

[15]  Marius V. Peelen,et al.  On the Role of Object Information in Action Observation: An fMRI Study , 2010, Cerebral cortex.

[16]  L. Buxbaum,et al.  Action knowledge, visuomotor activation, and embodiment in the two action systems , 2010, Annals of the New York Academy of Sciences.

[17]  Stefan J. Kiebel,et al.  Amygdala damage affects event‐related potentials for fearful faces at specific time windows , 2009, Human brain mapping.

[18]  Akio Kimura,et al.  Modulation of mu rhythm desynchronization during motor imagery by transcranial direct current stimulation , 2010, Journal of NeuroEngineering and Rehabilitation.

[19]  Geraint Rees,et al.  Electromagnetic responses to invisible face stimuli during binocular suppression , 2009, NeuroImage.

[20]  Hiroki Nakata,et al.  Centrifugal modulation of human LEP components to a task-relevant noxious stimulation triggering voluntary movement , 2009, NeuroImage.

[21]  Sheng He,et al.  Dynamics of processing invisible faces in the brain: Automatic neural encoding of facial expression information , 2009, NeuroImage.

[22]  Sheng He,et al.  Seeing the invisible: The scope and limits of unconscious processing in binocular rivalry , 2008, Progress in Neurobiology.

[23]  Alfonso Caramazza,et al.  Unconscious processing dissociates along categorical lines , 2008, Proceedings of the National Academy of Sciences.

[24]  Karl J. Friston,et al.  Multiple sparse priors for the M/EEG inverse problem , 2008, NeuroImage.

[25]  S. Frey What Puts the How in Where? Tool Use and the Divided Visual Streams Hypothesis , 2007, Cortex.

[26]  Karl J. Friston,et al.  Population-level inferences for distributed MEG source localization under multiple constraints: Application to face-evoked fields , 2007, NeuroImage.

[27]  Elana Zion-Golumbic,et al.  Electrophysiological neural mechanisms for detection, configural analysis and recognition of faces , 2007, NeuroImage.

[28]  Bradford Z. Mahon,et al.  Action-Related Properties Shape Object Representations in the Ventral Stream , 2007, Neuron.

[29]  Ryusuke Kakigi,et al.  Effects of face contour and features on early occipitotemporal activity when viewing eye movement , 2007, NeuroImage.

[30]  Sheng He,et al.  Cortical Responses to Invisible Faces: Dissociating Subsystems for Facial-Information Processing , 2006, Current Biology.

[31]  Koji Inui,et al.  Centrifugal regulation of human cortical responses to a task-relevant somatosensory signal triggering voluntary movement , 2006, NeuroImage.

[32]  J. Changeux,et al.  Opinion TRENDS in Cognitive Sciences Vol.10 No.5 May 2006 Conscious, preconscious, and subliminal processing: a testable taxonomy , 2022 .

[33]  Doris Y. Tsao,et al.  A Cortical Region Consisting Entirely of Face-Selective Cells , 2006, Science.

[34]  J. Haxby,et al.  Dissociation of face-selective cortical responses by attention. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[35]  Ole Jensen,et al.  Altered generation of spontaneous oscillations in Alzheimer's disease , 2005, NeuroImage.

[36]  F. Fang,et al.  Cortical responses to invisible objects in the human dorsal and ventral pathways , 2005, Nature Neuroscience.

[37]  C. Koch,et al.  Continuous flash suppression reduces negative afterimages , 2005, Nature Neuroscience.

[38]  Sarah H. Creem-Regehr,et al.  Neural representations of graspable objects: are tools special? , 2005, Brain research. Cognitive brain research.

[39]  N. Block Two neural correlates of consciousness , 2005, Trends in Cognitive Sciences.

[40]  Koji Inui,et al.  Temporal Dynamics of Neural Adaptation Effect in the Human Visual Ventral Stream , 2004, The Journal of Neuroscience.

[41]  Brian N. Pasley,et al.  Subcortical Discrimination of Unperceived Objects during Binocular Rivalry , 2004, Neuron.

[42]  Margot J. Taylor,et al.  N170 or N1? Spatiotemporal differences between object and face processing using ERPs. , 2004, Cerebral cortex.

[43]  Hiroki Nakata,et al.  Gating of somatosensory evoked magnetic fields during the preparatory period of self-initiated finger movement , 2003, NeuroImage.

[44]  Bruno Rossion,et al.  Early lateralization and orientation tuning for face, word, and object processing in the visual cortex , 2003, NeuroImage.

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

[46]  C. Koch,et al.  A framework for consciousness , 2003, Nature Neuroscience.

[47]  M. Brett,et al.  Actions Speak Louder Than Functions: The Importance of Manipulability and Action in Tool Representation , 2003, Journal of Cognitive Neuroscience.

[48]  J. Decety,et al.  Does visual perception of object afford action? Evidence from a neuroimaging study , 2002, Neuropsychologia.

[49]  R. Hari,et al.  Viewing Lip Forms Cortical Dynamics , 2002, Neuron.

[50]  N. Kanwisher,et al.  Stages of processing in face perception: an MEG study , 2002, Nature Neuroscience.

[51]  J B Poline,et al.  Cerebral mechanisms of word masking and unconscious repetition priming , 2001, Nature Neuroscience.

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

[53]  M. Eimer Effects of face inversion on the structural encoding and recognition of faces. Evidence from event-related brain potentials. , 2000, Brain research. Cognitive brain research.

[54]  T. Allison,et al.  Electrophysiological studies of human face perception. II: Response properties of face-specific potentials generated in occipitotemporal cortex. , 1999, Cerebral cortex.

[55]  Nancy Kanwisher,et al.  A cortical representation of the local visual environment , 1998, Nature.

[56]  G. Rizzolatti,et al.  The organization of the cortical motor system: new concepts. , 1998, Electroencephalography and clinical neurophysiology.

[57]  Scott T. Grafton,et al.  Premotor Cortex Activation during Observation and Naming of Familiar Tools , 1997, NeuroImage.

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

[59]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

[60]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[61]  T. Allison,et al.  Electrophysiological Studies of Face Perception in Humans , 1996, Journal of Cognitive Neuroscience.

[62]  Minami Ito,et al.  Columns for visual features of objects in monkey inferotemporal cortex , 1992, Nature.

[63]  M. Goodale,et al.  Separate visual pathways for perception and action , 1992, Trends in Neurosciences.

[64]  L. Jakobson,et al.  A neurological dissociation between perceiving objects and grasping them , 1991, Nature.

[65]  A. J. Mistlin,et al.  Visual cells in the temporal cortex sensitive to face view and gaze direction , 1985, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[66]  Leslie G. Ungerleider Two cortical visual systems , 1982 .