The role of oscillatory brain activity in object processing and figure-ground segmentation in human vision.

The perception of an object as a single entity within a visual scene requires that its features are bound together and segregated from the background and/or other objects. Here, we used magnetoencephalography (MEG) to assess the hypothesis that coherent percepts may arise from the synchronized high frequency (gamma) activity between neurons that code features of the same object. We also assessed the role of low frequency (alpha, beta) activity in object processing. The target stimulus (i.e. object) was a small patch of a concentric grating of 3c/°, viewed eccentrically. The background stimulus was either a blank field or a concentric grating of 3c/° periodicity, viewed centrally. With patterned backgrounds, the target stimulus emerged--through rotation about its own centre--as a circular subsection of the background. Data were acquired using a 275-channel whole-head MEG system and analyzed using Synthetic Aperture Magnetometry (SAM), which allows one to generate images of task-related cortical oscillatory power changes within specific frequency bands. Significant oscillatory activity across a broad range of frequencies was evident at the V1/V2 border, and subsequent analyses were based on a virtual electrode at this location. When the target was presented in isolation, we observed that: (i) contralateral stimulation yielded a sustained power increase in gamma activity; and (ii) both contra- and ipsilateral stimulation yielded near identical transient power changes in alpha (and beta) activity. When the target was presented against a patterned background, we observed that: (i) contralateral stimulation yielded an increase in high-gamma (>55 Hz) power together with a decrease in low-gamma (40-55 Hz) power; and (ii) both contra- and ipsilateral stimulation yielded a transient decrease in alpha (and beta) activity, though the reduction tended to be greatest for contralateral stimulation. The opposing power changes across different regions of the gamma spectrum with 'figure/ground' stimulation suggest a possible dual role for gamma rhythms in visual object coding, and provide general support of the binding-by-synchronization hypothesis. As the power changes in alpha and beta activity were largely independent of the spatial location of the target, however, we conclude that their role in object processing may relate principally to changes in visual attention.

[1]  H. Spekreijse,et al.  Synchrony dynamics in monkey V1 predict success in visual detection. , 2006, Cerebral cortex.

[2]  R. von der Heydt,et al.  Synchrony and the binding problem in macaque visual cortex. , 2008, Journal of vision.

[3]  G. V. Simpson,et al.  Anticipatory Biasing of Visuospatial Attention Indexed by Retinotopically Specific α-Bank Electroencephalography Increases over Occipital Cortex , 2000, The Journal of Neuroscience.

[4]  F. Crick The Astonishing Hypothesis , 1994 .

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

[6]  Krish D. Singh,et al.  Induced visual illusions and gamma oscillations in human primary visual cortex , 2004, The European journal of neuroscience.

[7]  Victor A. F. Lamme,et al.  Figure-ground activity in primary visual cortex is suppressed by anesthesia. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[8]  A. Dale,et al.  Functional Analysis of V3A and Related Areas in Human Visual Cortex , 1997, The Journal of Neuroscience.

[9]  J. Sarvas Basic mathematical and electromagnetic concepts of the biomagnetic inverse problem. , 1987, Physics in medicine and biology.

[10]  A. Thiele,et al.  Neuronal synchrony does not correlate with motion coherence in cortical area MT , 2003, Nature.

[11]  Michael N. Shadlen,et al.  Synchrony Unbound A Critical Evaluation of the Temporal Binding Hypothesis , 1999, Neuron.

[12]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[13]  Matthew J. Brookes,et al.  Source localisation in concurrent EEG/fMRI: Applications at 7T , 2009, NeuroImage.

[14]  Á. Pascual-Leone,et al.  α-Band Electroencephalographic Activity over Occipital Cortex Indexes Visuospatial Attention Bias and Predicts Visual Target Detection , 2006, The Journal of Neuroscience.

[15]  Gareth R. Barnes,et al.  Stimuli of varying spatial scale induce gamma activity with distinct temporal characteristics in human visual cortex , 2007, NeuroImage.

[16]  Manuel Schabus,et al.  A shift of visual spatial attention is selectively associated with human EEG alpha activity , 2005, The European journal of neuroscience.

[17]  S. Anderson,et al.  Cortical oscillatory activity associated with the perception of illusory and real visual contours. , 2009, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[19]  P König,et al.  Direct physiological evidence for scene segmentation by temporal coding. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[20]  G. Pfurtscheller Event-related synchronization (ERS): an electrophysiological correlate of cortical areas at rest. , 1992, Electroencephalography and clinical neurophysiology.

[21]  J. Bullier,et al.  Cortical mapping of gamma oscillations in areas V1 and V4 of the macaque monkey , 2001, Visual Neuroscience.

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

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

[24]  Victor A. F. Lamme,et al.  Neuronal synchrony does not represent texture segregation , 1998, Nature.

[25]  E. Adrian,et al.  THE BERGER RHYTHM: POTENTIAL CHANGES FROM THE OCCIPITAL LOBES IN MAN , 1934 .

[26]  R. Fisher,et al.  Statistical Methods for Research Workers , 1930, Nature.

[27]  Matthias M. Müller,et al.  Human Gamma Band Activity and Perception of a Gestalt , 1999, The Journal of Neuroscience.

[28]  J. Bullier Integrated model of visual processing , 2001, Brain Research Reviews.

[29]  F. Qiu,et al.  Figure-ground mechanisms provide structure for selective attention , 2007, Nature Neuroscience.

[30]  W. Singer,et al.  Stimulus-dependent synchronization of neuronal responses in the visual cortex of the awake macaque monkey , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  Roman Bauer,et al.  Perceptual grouping correlates with short synchronization in monkey prestriate cortex , 2002, Neuroreport.

[32]  Leslie G. Ungerleider,et al.  The neural basis of biased competition in human visual cortex , 2001, Neuropsychologia.

[33]  R. Eckhorn,et al.  Contour decouples gamma activity across texture representation in monkey striate cortex. , 2000, Cerebral cortex.

[34]  A. Dale,et al.  The Representation of Illusory and Real Contours in Human Cortical Visual Areas Revealed by Functional Magnetic Resonance Imaging , 1999, The Journal of Neuroscience.

[35]  A. Engel,et al.  High-frequency activity in human visual cortex is modulated by visual motion strength. , 2007, Cerebral cortex.

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

[37]  Victor A. F. Lamme The neurophysiology of figure-ground segregation in primary visual cortex , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[39]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[40]  K. Fujii,et al.  Visualization for the analysis of fluid motion , 2005, J. Vis..

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

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

[43]  Eric Halgren,et al.  Cortical activation to illusory shapes as measured with magnetoencephalography , 2003, NeuroImage.

[44]  Wolf Singer Binding by synchrony , 2007, Scholarpedia.

[45]  B. Maess,et al.  Sources of synchronized induced Gamma-Band responses during a simple object recognition task: A replication study in human MEG , 2008, Brain Research.

[46]  Victor A. F. Lamme,et al.  Contextual Modulation in Primary Visual Cortex , 1996, The Journal of Neuroscience.

[47]  G. Pfurtscheller,et al.  Event-related synchronization (ERS) in the alpha band--an electrophysiological correlate of cortical idling: a review. , 1996, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[48]  C S Herrmann,et al.  Magnetoencephalographic responses to illusory figures: early evoked gamma is affected by processing of stimulus features. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[49]  A. Thielscher,et al.  Texture segmentation in human perception: A combined modeling and fMRI study , 2008, Neuroscience.

[50]  W. Singer,et al.  Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[51]  C. Gray,et al.  Chattering Cells: Superficial Pyramidal Neurons Contributing to the Generation of Synchronous Oscillations in the Visual Cortex , 1996, Science.

[52]  Stephen J. Anderson,et al.  The spatial distribution and temporal dynamics of brain regions activated during the perception of object and non-object patterns , 2007, NeuroImage.

[53]  Werner Lutzenberger,et al.  Magnetoencephalographic gamma-band responses to illusory triangles in humans , 2004, NeuroImage.

[54]  Gareth R. Barnes,et al.  The missing link: analogous human and primate cortical gamma oscillations , 2005, NeuroImage.

[55]  W. Singer,et al.  Synchronization of oscillatory responses in visual cortex correlates with perception in interocular rivalry. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

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

[57]  Derek K. Jones,et al.  Visual gamma oscillations and evoked responses: Variability, repeatability and structural MRI correlates , 2010, NeuroImage.

[58]  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.

[59]  Robert Oostenveld,et al.  Localizing human visual gamma-band activity in frequency, time and space , 2006, NeuroImage.

[60]  D. Hubel,et al.  Receptive fields and functional architecture of monkey striate cortex , 1968, The Journal of physiology.

[61]  J. Lisman,et al.  Oscillations in the alpha band (9-12 Hz) increase with memory load during retention in a short-term memory task. , 2002, Cerebral cortex.

[62]  P. König,et al.  A Functional Gamma-Band Defined by Stimulus-Dependent Synchronization in Area 18 of Awake Behaving Cats , 2003, The Journal of Neuroscience.

[63]  T. Picton,et al.  Correlates of eye blinking as determined by synthetic aperture magnetometry , 2006, Clinical Neurophysiology.

[64]  R. Hari,et al.  Visual awareness of objects correlates with activity of right occipital cortex , 1996, Neuroreport.

[65]  G. Pfurtscheller,et al.  Motor imagery and action observation: Modulation of sensorimotor brain rhythms during mental control of a brain–computer interface , 2009, Clinical Neurophysiology.

[66]  K. D. Singh,et al.  Spectral properties of induced and evoked gamma oscillations in human early visual cortex to moving and stationary stimuli. , 2009, Journal of neurophysiology.

[67]  Victor A. F. Lamme,et al.  The influence of inattention on the neural correlates of scene segmentation , 2006, Brain Research.

[68]  R. von der Heydt,et al.  A neural model of figure-ground organization. , 2007, Journal of neurophysiology.

[69]  H H Donaldson,et al.  LOCALIZATION IN THE BRAIN. , 1884, Science.

[70]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

[71]  J W Belliveau,et al.  Borders of multiple visual areas in humans revealed by functional magnetic resonance imaging. , 1995, Science.

[72]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[73]  Reinhard Eckhorn,et al.  Neural mechanisms of visual associative processing. , 2004, Acta neurobiologiae experimentalis.

[74]  Catherine Tallon-Baudry,et al.  Visual Grouping and the Focusing of Attention Induce Gamma-band Oscillations at Different Frequencies in Human Magnetoencephalogram Signals , 2006, Journal of Cognitive Neuroscience.

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

[76]  W. Klimesch EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis , 1999, Brain Research Reviews.

[77]  L. M. Ward,et al.  Synchronous neural oscillations and cognitive processes , 2003, Trends in Cognitive Sciences.

[78]  C. Gerloff,et al.  Inhibitory control of acquired motor programmes in the human brain. , 2002, Brain : a journal of neurology.

[79]  Stephen J. Anderson,et al.  Elsevier Editorial System(tm) for Brain Research Manuscript Draft Response Letter Reviewer Number 1 Attentional Changes in Pre-stimulus Oscillatory Activity within Early Visual Cortex Are Predictive of Human Visual Performance , 2007 .

[80]  M. Hallett,et al.  Transient Interhemispheric Neuronal Synchrony Correlates with Object Recognition , 2001, The Journal of Neuroscience.

[81]  Catherine Tallon-Baudry,et al.  Oscillatory synchrony and human visual cognition , 2003, Journal of Physiology-Paris.

[82]  P. Fries,et al.  Is synchronized neuronal gamma activity relevant for selective attention? , 2003, Brain Research Reviews.

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

[84]  Victor A. F. Lamme,et al.  Altered figure-ground perception in monkeys with an extra-striate lesion , 2007, Neuropsychologia.