The spatial distribution and temporal dynamics of brain regions activated during the perception of object and non-object patterns

Both animal and human studies suggest that the efficiency with which we are able to grasp objects is attributable to a repertoire of motor signals derived directly from vision. This is in general agreement with the long-held belief that the automatic generation of motor signals by the perception of objects is based on the actions they afford. In this study, we used magnetoencephalography (MEG) to determine the spatial distribution and temporal dynamics of brain regions activated during passive viewing of object and non-object targets that varied in the extent to which they afforded a grasping action. Synthetic Aperture Magnetometry (SAM) was used to localize task-related oscillatory power changes within specific frequency bands, and the time course of activity within given regions-of-interest was determined by calculating time-frequency plots using a Morlet wavelet transform. Both single subject and group-averaged data on the spatial distribution of brain activity are presented. We show that: (i) significant reductions in 10-25 Hz activity within extrastriate cortex, occipito-temporal cortex, sensori-motor cortex and cerebellum were evident with passive viewing of both objects and non-objects; and (ii) reductions in oscillatory activity within the posterior part of the superior parietal cortex (area Ba7) were only evident with the perception of objects. Assuming that focal reductions in low-frequency oscillations (<30 Hz) reflect areas of heightened neural activity, we conclude that: (i) activity within a network of brain areas, including the sensori-motor cortex, is not critically dependent on stimulus type and may reflect general changes in visual attention; and (ii) the posterior part of the superior parietal cortex, area Ba7, is activated preferentially by objects and may play a role in computations related to grasping.

[1]  E. Reed The Ecological Approach to Visual Perception , 1989 .

[2]  Gareth R. Barnes,et al.  Group imaging of task-related changes in cortical synchronisation using nonparametric permutation testing , 2003, NeuroImage.

[3]  G. Rizzolatti,et al.  Evidence for visuomotor priming effect , 1996, Neuroreport.

[4]  Thomas E. Nichols,et al.  Nonparametric permutation tests for functional neuroimaging: A primer with examples , 2002, Human brain mapping.

[5]  F. Varela,et al.  Perception's shadow: long-distance synchronization of human brain activity , 1999, Nature.

[6]  S. Tipper,et al.  Selective reaching: evidence for action-centered attention. , 1992, Journal of experimental psychology. Human perception and performance.

[7]  H. Sakata,et al.  Parietal control of hand action , 1994, Current Opinion in Neurobiology.

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

[9]  Norihiko Fujita,et al.  Movement-Related Desynchronization of the Cerebral Cortex Studied with Spatially Filtered Magnetoencephalography , 2000, NeuroImage.

[10]  C. Umilta,et al.  Splitting visual space with attention. , 1989, Journal of experimental psychology. Human perception and performance.

[11]  R. Eckhorn,et al.  Coherent oscillations: A mechanism of feature linking in the visual cortex? , 1988, Biological Cybernetics.

[12]  J. Haxby,et al.  Parallel Visual Motion Processing Streams for Manipulable Objects and Human Movements , 2002, Neuron.

[13]  R. Ellis,et al.  Action priming by briefly presented objects. , 2004, Acta psychologica.

[14]  F. Varela,et al.  Neuromagnetic imaging of cortical oscillations accompanying tactile stimulation. , 2003, Brain research. Cognitive brain research.

[15]  J. Vrba,et al.  Signal processing in magnetoencephalography. , 2001, Methods.

[16]  David J. Turk,et al.  Placing a tool in the spotlight: spatial attention modulates visuomotor responses in cortex , 2005, NeuroImage.

[17]  M. Arbib,et al.  Grasping objects: the cortical mechanisms of visuomotor transformation , 1995, Trends in Neurosciences.

[18]  Robin L. Hill,et al.  Eye-movement research: An overview of current and past developments , 2007 .

[19]  David Poeppel,et al.  Asymptotic SNR of scalar and vector minimum-variance beamformers for neuromagnetic source reconstruction , 2004, IEEE Transactions on Biomedical Engineering.

[20]  R. Ellis,et al.  On the relations between seen objects and components of potential actions. , 1998, Journal of experimental psychology. Human perception and performance.

[21]  M. Breakspear Nonlinear phase desynchronization in human electroencephalographic data , 2002, Human brain mapping.

[22]  H. Petsche,et al.  Phase-coupling of theta-gamma EEG rhythms during short-term memory processing. , 2002, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[23]  F. H. Lopes da Silva Neural mechanisms underlying brain waves: from neural membranes to networks. , 1991, Electroencephalography and clinical neurophysiology.

[24]  J E Joseph,et al.  Functional neuroimaging studies of category specificity in object recognition: A critical review and meta-analysis , 2001, Cognitive, affective & behavioral neuroscience.

[25]  G. Pfurtscheller,et al.  Motor imagery activates primary sensorimotor area in humans , 1997, Neuroscience Letters.

[26]  B. Hommel Event files: feature binding in and across perception and action , 2004, Trends in Cognitive Sciences.

[27]  S P Tipper,et al.  Action-based mechanisms of attention. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[28]  Carlo Umiltà,et al.  Attention shifts produce spatial stimulus codes , 1994, Psychological research.

[29]  P. Derambure,et al.  Basic mechanisms of central rhythms reactivity to preparation and execution of a voluntary movement: a stereoelectroencephalographic study , 2003, Clinical Neurophysiology.

[30]  Karl J. Friston,et al.  Modulation of excitatory synaptic coupling facilitates synchronization and complex dynamics in a biophysical model of neuronal dynamics , 2003, Network.

[31]  C F Michaels,et al.  S-R compatibility between response position and destination of apparent motion: evidence of the detection of affordances. , 1988, Journal of experimental psychology. Human perception and performance.

[32]  Gareth R. Barnes,et al.  The use of anatomical constraints with MEG beamformers , 2003, NeuroImage.

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

[34]  A Treisman,et al.  Feature binding, attention and object perception. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[35]  M. Jüptner,et al.  A review of differences between basal ganglia and cerebellar control of movements as revealed by functional imaging studies. , 1998, Brain : a journal of neurology.

[36]  M-X Huang,et al.  Commonalities and Differences Among Vectorized Beamformers in Electromagnetic Source Imaging , 2003, Brain Topography.

[37]  R. Wallace,et al.  S-R compatibility and the idea of a response code. , 1971, Journal of experimental psychology.

[38]  David Poeppel,et al.  Reconstructing spatio-temporal activities of neural sources using an MEG vector beamformer technique , 2001, IEEE Transactions on Biomedical Engineering.

[39]  G. Rizzolatti,et al.  Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention , 1987, Neuropsychologia.

[40]  Sang Joon Kim,et al.  A Mathematical Theory of Communication , 2006 .

[41]  N. Kanwisher,et al.  The lateral occipital complex and its role in object recognition , 2001, Vision Research.

[42]  D. P. Russell,et al.  Increased Synchronization of Neuromagnetic Responses during Conscious Perception , 1999, The Journal of Neuroscience.

[43]  M. Kawato,et al.  Attentional shifts towards an expected visual target alter the level of alpha-band oscillatory activity in the human calcarine cortex. , 2005, Brain research. Cognitive brain research.

[44]  W. Singer,et al.  Reduced Synchronization in the Visual Cortex of Cats with Strabismic Amblyopia , 1994, The European journal of neuroscience.

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

[46]  W. Singer,et al.  Visuomotor integration is associated with zero time-lag synchronization among cortical areas , 1997, Nature.

[47]  G. Pfurtscheller,et al.  Functional brain imaging based on ERD/ERS , 2001, Vision Research.

[48]  Gert Pfurtscheller,et al.  Basic concepts on EEG synchronization and desynchronization , 1999 .

[49]  P König,et al.  Synchronization of oscillatory neuronal responses between striate and extrastriate visual cortical areas of the cat. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[50]  John C. Rothwell,et al.  Left posterior BA37 is involved in object recognition: a TMS study , 2001, Neuropsychologia.

[51]  Karl J. Friston The labile brain. I. Neuronal transients and nonlinear coupling. , 2000, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[52]  M. Corbetta,et al.  Human cortical mechanisms of visual attention during orienting and search. , 1998, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[53]  G. Pfurtscheller,et al.  Evaluation of event-related desynchronization (ERD) preceding and following voluntary self-paced movement. , 1979, Electroencephalography and clinical neurophysiology.

[54]  G. R. Barnes,et al.  A Quantitative Assessment of the Sensitivity of Whole-Head MEG to Activity in the Adult Human Cortex , 2002, NeuroImage.

[55]  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 .

[56]  J L Lancaster,et al.  Automated Talairach Atlas labels for functional brain mapping , 2000, Human brain mapping.

[57]  Stephen J. Anderson,et al.  Attentional modulation of oscillatory activity in human visual cortex , 2003, NeuroImage.

[58]  R. E Passingham,et al.  Activations related to “mirror” and “canonical” neurones in the human brain: an fMRI study , 2003, NeuroImage.

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

[60]  S. M. Williams,et al.  The Premotor Cortex , 2001 .

[61]  G. Barnes,et al.  Realistic spatial sampling for MEG beamformer images , 2004, Human brain mapping.

[62]  H. Freund,et al.  Variation of perisylvian and calcarine anatomic landmarks within stereotaxic proportional coordinates. , 1990, AJNR. American journal of neuroradiology.

[63]  G. Rizzolatti,et al.  Effects of spatial attention on directional manual and ocular responses , 1997, Experimental Brain Research.

[64]  J R Simon,et al.  Processing symbolic information from a visual display: interference from an irrelevant directional cue. , 1970, Journal of experimental psychology.

[65]  O. Bertrand,et al.  Oscillatory gamma activity in humans and its role in object representation , 1999, Trends in Cognitive Sciences.

[66]  W. Drongelen,et al.  A spatial filtering technique to detect and localize multiple sources in the brain , 1996, Brain Topography.

[67]  T. Stoffer Attentional focussing and spatial stimulus-response compatibility , 1991, Psychological research.

[68]  T Kizuka,et al.  Automatic activation in the human primary motor cortex synchronized with movement preparation. , 1999, Brain research. Cognitive brain research.

[69]  B.D. Van Veen,et al.  Beamforming: a versatile approach to spatial filtering , 1988, IEEE ASSP Magazine.

[70]  R. Hari,et al.  Modulated Activation of the Human SI and SII Cortices during Observation of Hand Actions , 2002, NeuroImage.

[71]  P. Hazemann,et al.  Handbook of Electroencephalography and Clinical Neurophysiology , 1975 .

[72]  M. Goldberg,et al.  Visuospatial and motor attention in the monkey , 1987, Neuropsychologia.

[73]  Adrian L. Williams,et al.  Task-Related Changes in Cortical Synchronization Are Spatially Coincident with the Hemodynamic Response , 2002, NeuroImage.

[74]  R W Proctor,et al.  Referential coding and attention-shifting accounts of the Simon effect , 1994, Psychological research.

[75]  S. Anderson,et al.  Attentional processes link perception and action , 2002, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[76]  Arjan Hillebrand,et al.  Beamformer analysis of MEG data. , 2005, International review of neurobiology.

[77]  F. L. D. Silva,et al.  Event-Related Desynchronization , 1999 .

[78]  H. Sakata,et al.  The TINS Lecture The parietal association cortex in depth perception and visual control of hand action , 1997, Trends in Neurosciences.

[79]  R. Woods Modeling for Intergroup Comparisons of Imaging Data , 1996, NeuroImage.

[80]  石井 良平 Medial prefrontal cortex generates frontal midline theta rhythm , 1999 .

[81]  E. Capaldi,et al.  The organization of behavior. , 1992, Journal of applied behavior analysis.

[82]  A. Treisman The binding problem , 1996, Current Opinion in Neurobiology.

[83]  Michael Breakspear,et al.  A Novel Method for the Topographic Analysis of Neural Activity Reveals Formation and Dissolution of ‘Dynamic Cell Assemblies’ , 2004, Journal of Computational Neuroscience.

[84]  M. Gentilucci Object motor representation and reaching–grasping control , 2002, Neuropsychologia.

[85]  G. Rizzolatti,et al.  Space and selective attention , 1994 .

[86]  R. Ellis,et al.  Micro-affordance: the potentiation of components of action by seen objects. , 2000, British journal of psychology.

[87]  V. Jousmäki,et al.  Modulation of Human Cortical Rolandic Rhythms during Natural Sensorimotor Tasks , 1997, NeuroImage.

[88]  G. V. Simpson,et al.  Parieto‐occipital ∼1 0Hz activity reflects anticipatory state of visual attention mechanisms , 1998 .

[89]  A. von Stein,et al.  Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[90]  Joachim Gross,et al.  The cerebral oscillatory network associated with auditorily paced finger movements , 2005, NeuroImage.

[91]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[92]  R. Hari,et al.  Synchronous cortical oscillatory activity during motor action , 2003, Current Opinion in Neurobiology.

[93]  J. F. Stein,et al.  Role of the cerebellum in the visual guidance of movement , 1986, Nature.

[94]  K. D. Singh,et al.  Co-registration of magnetoencephalography with magnetic resonance imaging using bite-bar-based fiducials and surface-matching , 2004, Clinical Neurophysiology.

[95]  Christa Neuper,et al.  Motor imagery and ERD , 1999 .

[96]  J. R. Simon,et al.  Reactions toward the source of stimulation. , 1969, Journal of experimental psychology.

[97]  G. Rizzolatti,et al.  Activation of human primary motor cortex during action observation: a neuromagnetic study. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[98]  W. Freeman,et al.  Fine temporal resolution of analytic phase reveals episodic synchronization by state transitions in gamma EEGs. , 2002, Journal of neurophysiology.

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

[100]  J. Kable,et al.  Neural Substrates of Action Event Knowledge , 2002, Journal of Cognitive Neuroscience.

[101]  W. Drongelen,et al.  Localization of brain electrical activity via linearly constrained minimum variance spatial filtering , 1997, IEEE Transactions on Biomedical Engineering.

[102]  G Pfurtscheller,et al.  Visualization of significant ERD/ERS patterns in multichannel EEG and ECoG data , 2002, Clinical Neurophysiology.

[103]  R. Malach,et al.  Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[104]  Matthew J. Brookes,et al.  A general linear model for MEG beamformer imaging , 2004, NeuroImage.

[105]  William Bialek,et al.  Spikes: Exploring the Neural Code , 1996 .

[106]  Marcel C. M. Bastiaansen,et al.  ERD as an index of anticipatory behaviour. , 1999 .

[107]  G. Pfurtscheller,et al.  ERD and ERS in voluntary movement of different limbs , 1999 .

[108]  S. Zeki A vision of the brain , 1993 .

[109]  P. König,et al.  Top-down processing mediated by interareal synchronization. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[110]  R. Passingham,et al.  Objects automatically potentiate action: an fMRI study of implicit processing , 2003, The European journal of neuroscience.

[111]  G. Barnes,et al.  Statistical flattening of MEG beamformer images , 2003, Human brain mapping.

[112]  G. Pfurtscheller Handbook of electroencephalography and clinical neurophysiology , 1978 .

[113]  Bernhard Hommel,et al.  Responding to object files: Automatic integration of spatial information revealed by stimulus-response compatibility effects , 2002, The Quarterly journal of experimental psychology. A, Human experimental psychology.

[114]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[115]  G. Rizzolatti,et al.  Functional organization of inferior area 6 in the macaque monkey , 1988, Experimental Brain Research.

[116]  R. Ellis,et al.  The potentiation of grasp types during visual object categorization , 2001 .

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

[118]  Se Robinson,et al.  Functional neuroimaging by Synthetic Aperture Magnetometry (SAM) , 1999 .

[119]  Leslie G. Ungerleider,et al.  Neural correlates of category-specific knowledge , 1996, Nature.

[120]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[121]  J. Vrba Magnetoencephalography: the art of finding a needle in a haystack , 2002 .

[122]  F. D. Silva Neural mechanisms underlying brain waves: from neural membranes to networks. , 1991 .

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

[124]  B. Breitmeyer,et al.  Mechanisms of visual attention revealed by saccadic eye movements , 1987, Neuropsychologia.

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

[126]  S. Bressler,et al.  Episodic multiregional cortical coherence at multiple frequencies during visual task performance , 1993, Nature.

[127]  G. Rizzolatti,et al.  Object representation in the ventral premotor cortex (area F5) of the monkey. , 1997, Journal of neurophysiology.

[128]  Wolfgang Klimesch,et al.  Individual differences in brain dynamics: important implications for the calculation of event-related band power , 1998, Biological Cybernetics.

[129]  J. Haxby,et al.  Attribute-based neural substrates in temporal cortex for perceiving and knowing about objects , 1999, Nature Neuroscience.

[130]  F. L. D. Silva,et al.  Basic mechanisms of cerebral rhythmic activities , 1990 .

[131]  R. Hari,et al.  Modulation of the Parieto-Occipital Alpha Rhythm during Object Detection , 1997, The Journal of Neuroscience.

[132]  Krish D. Singh,et al.  A new approach to neuroimaging with magnetoencephalography , 2005, Human brain mapping.

[133]  Conrad V. Kufta,et al.  Event-related desynchronization and movement-related cortical potentials on the ECoG and EEG. , 1994, Electroencephalography and clinical neurophysiology.

[134]  H. Deubel,et al.  Visual attention and saccadic eye movements: Evidence for obligatory and selective spatial coupling , 1995 .

[135]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

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

[137]  C Iani,et al.  The Simon effect occurs relative to the direction of an attention shift. , 1997, Journal of experimental psychology. Human perception and performance.

[138]  J. G. Snodgrass,et al.  A standardized set of 260 pictures: norms for name agreement, image agreement, familiarity, and visual complexity. , 1980, Journal of experimental psychology. Human learning and memory.