The Neural Substrates and Timing of Top–Down Processes during Coarse-to-Fine Categorization of Visual Scenes: A Combined fMRI and ERP Study

Abstract Spatial frequencies in an image influence visual analysis across a distributed, hierarchically organized brain network. Low spatial frequency (LSF) information may rapidly reach high-order areas to allow an initial coarse parsing of the visual scene, which could then be “retroinjected” through feedback into lower level visual areas to guide finer analysis on the basis of high spatial frequency (HSF). To test this “coarse-to-fine” processing scheme and to identify its neural substrates in the human brain, we presented sequences of two spatial-frequency-filtered scenes in rapid succession (LSF followed by HSF or vice versa) during fMRI and ERPs in the same participants. We show that for low-to-high sequences (but not for high-to-low sequences), LSF produces a first increase of activity in prefrontal and temporo-parietal areas, followed by enhanced responses to HSF in primary visual cortex. This pattern is consistent with retroactive influences on low-level areas that process HSF after initial activation of higher order areas by LSF.

[1]  Sheng Li,et al.  Learning shapes spatiotemporal brain patterns for flexible categorical decisions. , 2012, Cerebral cortex.

[2]  J. Kaiser,et al.  Separable neural bases for subprocesses of recognition in working memory. , 2012, Cerebral cortex.

[3]  Simone R. Caljouw,et al.  Differential effects of a visual illusion on online visual guidance in a stable environment and online adjustments to perturbations , 2011, Consciousness and Cognition.

[4]  N. Guyader,et al.  Residual abilities in age-related macular degeneration to process spatial frequencies during natural scene categorization , 2011, Visual Neuroscience.

[5]  S. Rousset,et al.  Global precedence effect in audition and vision: evidence for similar cognitive styles across modalities. , 2011, Acta psychologica.

[6]  Ming-Liang Gong,et al.  Scene Consistency Effect and Its Mechanisms*: Scene Consistency Effect and Its Mechanisms* , 2011 .

[7]  O. Houdé,et al.  ERP evidence of a meaningfulness impact on visual global/local processing: When meaning captures attention , 2011, Neuropsychologia.

[8]  Moshe Bar,et al.  See it with feeling: affective predictions during object perception , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[9]  J. Hegdé Time course of visual perception: Coarse-to-fine processing and beyond , 2008, Progress in Neurobiology.

[10]  E. Halgren,et al.  Top-down facilitation of visual recognition. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[11]  Christoph M. Michel,et al.  Hemispheric specialization of human inferior temporal cortex during coarse-to-fine and fine-to-coarse analysis of natural visual scenes , 2005, NeuroImage.

[12]  F. Hamker The reentry hypothesis: the putative interaction of the frontal eye field, ventrolateral prefrontal cortex, and areas V4, IT for attention and eye movement. , 2005, Cerebral cortex.

[13]  M. Murray,et al.  EEG source imaging , 2004, Clinical Neurophysiology.

[14]  Monica Baciu,et al.  Cerebral regions and hemispheric specialization for processing spatial frequencies during natural scene recognition. An event-related fMRI study , 2004, NeuroImage.

[15]  Andreas Kleinschmidt,et al.  Scale invariant adaptation in fusiform face-responsive regions , 2004, NeuroImage.

[16]  Christoph M. Michel,et al.  Electrical neuroimaging based on biophysical constraints , 2004, NeuroImage.

[17]  Carole Peyrin,et al.  Hemispheric specialization for spatial frequency processing in the analysis of natural scenes , 2003, Brain and Cognition.

[18]  M. Bar A Cortical Mechanism for Triggering Top-Down Facilitation in Visual Object Recognition , 2003, Journal of Cognitive Neuroscience.

[19]  J. Schall The neural selection and control of saccades by the frontal eye field. , 2002, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[20]  R. Henson,et al.  Multiple levels of visual object constancy revealed by event-related fMRI of repetition priming , 2002, Nature Neuroscience.

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

[22]  R. Poldrack,et al.  Recovering Meaning Left Prefrontal Cortex Guides Controlled Semantic Retrieval , 2001, Neuron.

[23]  R. Henson,et al.  Frontal lobes and human memory: insights from functional neuroimaging. , 2001, Brain : a journal of neurology.

[24]  M. Bar,et al.  Cortical Mechanisms Specific to Explicit Visual Object Recognition , 2001, Neuron.

[25]  David J. Freedman,et al.  Categorical representation of visual stimuli in the primate prefrontal cortex. , 2001, Science.

[26]  O. Blanke,et al.  Location of the human frontal eye field as defined by electrical cortical stimulation: anatomical, functional and electrophysiological characteristics , 2000, Neuroreport.

[27]  Shingo Yamagata,et al.  Cerebral Asymmetry of the “Top-Down” Allocation of Attention to Global and Local Features , 2000, The Journal of Neuroscience.

[28]  Margot J. Taylor,et al.  Guidelines for using human event-related potentials to study cognition: recording standards and publication criteria. , 2000, Psychophysiology.

[29]  T. Poggio,et al.  Hierarchical models of object recognition in cortex , 1999, Nature Neuroscience.

[30]  Karl J. Friston,et al.  Stochastic Designs in Event-Related fMRI , 1999, NeuroImage.

[31]  S. Edelman,et al.  Differential Processing of Objects under Various Viewing Conditions in the Human Lateral Occipital Complex , 1999, Neuron.

[32]  O Josephs,et al.  Event-related functional magnetic resonance imaging: modelling, inference and optimization. , 1999, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[33]  C. Price,et al.  Functional Neuroanatomy of the Semantic System: Divisible by What? , 1998, Journal of Cognitive Neuroscience.

[34]  P H Schiller,et al.  Visual representations during saccadic eye movements. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[35]  A. Oliva,et al.  Flexible, Diagnosticity-Driven, Rather Than Fixed, Perceptually Determined Scale Selection in Scene and Face Recognition , 1997, Perception.

[36]  Richard S. J. Frackowiak,et al.  Where in the brain does visual attention select the forest and the trees? , 1996, Nature.

[37]  T. Paus Location and function of the human frontal eye-field: A selective review , 1996, Neuropsychologia.

[38]  J. Bullier,et al.  Functional streams in occipito-frontal connections in the monkey , 1996, Behavioural Brain Research.

[39]  E. Bizzi,et al.  The Cognitive Neurosciences , 1996 .

[40]  D. Lehmann,et al.  Segmentation of brain electrical activity into microstates: model estimation and validation , 1995, IEEE Transactions on Biomedical Engineering.

[41]  A. Oliva,et al.  From Blobs to Boundary Edges: Evidence for Time- and Spatial-Scale-Dependent Scene Recognition , 1994 .

[42]  Shimon Ullman,et al.  Visual object recognition , 1993 .

[43]  E W Yund,et al.  The role of spatial frequency in the processing of hierarchically organized stimuli , 1993, Perception & psychophysics.

[44]  J R Lishman,et al.  Temporal Integration of Spatially Filtered Visual Images , 1992, Perception.

[45]  D R Badcock,et al.  Low-Frequency Filtering and the Processing of Local—Global Stimuli , 1990, Perception.

[46]  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 .

[47]  L. Robertson,et al.  Effects of lesions of temporal-parietal junction on perceptual and attentional processing in humans , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[48]  Antoine Rémond,et al.  Methods of Analysis of Brain Electrical and Magnetic Signals , 1987 .

[49]  G L Shulman,et al.  The Role of Spatial-Frequency Channels in the Perception of Local and Global Structure , 1986, Perception.

[50]  J. Robson,et al.  Probability summation and regional variation in contrast sensitivity across the visual field , 1981, Vision Research.

[51]  D. Lehmann,et al.  Reference-free identification of components of checkerboard-evoked multichannel potential fields. , 1980, Electroencephalography and clinical neurophysiology.

[52]  G. Pfurtscheller Handbook of electroencephalography and clinical neurophysiology: A. Rémond (Editor). Vol. 4, Part A: Sampling, Conversion and Measurement of Bioelectrical Phenomena. — F.H. Lopes da Silva (Editor). (Elsevier, Amsterdam, 1976, 70 p., 16 Fig., Hfl 25.00) , 1978 .

[53]  D. Navon Forest before trees: The precedence of global features in visual perception , 1977, Cognitive Psychology.

[54]  Bruno G. Breitmeyer,et al.  Simple reaction time as a measure of the temporal response properties of transient and sustained channels , 1975, Vision Research.

[55]  F. Plum Handbook of Electroencephalography and Clinical Neurophysiology , 1972 .

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

[57]  L. Sobin,et al.  CO-PLANAR STEREOTAXIC ATLAS OF THE HUMAN BRAIN 3-DIMENSIONAL PROPORTIONAL SYSTEM: AN APPROACH TO CEREBRAL IMAGING 1988 GUIDE TO THE TNM/pTNM-CLASSIFICATION OF MALIGNANT TUMOURS THIRD EDITION , 2007 .

[58]  C. Michel,et al.  Noninvasive Localization of Electromagnetic Epileptic Activity. I. Method Descriptions and Simulations , 2004, Brain Topography.

[59]  C. Michel,et al.  Noninvasive Localization of Electromagnetic Epileptic Activity. II. Demonstration of Sublobar Accuracy in Patients with Simultaneous Surface and Depth Recordings , 2004, Brain Topography.

[60]  L. Chalupa,et al.  The visual neurosciences , 2004 .

[61]  Rolando Grave de Peralta,et al.  Comparison of Algorithms for the Localization of Focal Sources: Evaluation with simulated data and analysis of experimental data. , 2002 .

[62]  G. V. Simpson,et al.  Flow of activation from V1 to frontal cortex in humans , 2001, Experimental Brain Research.

[63]  P Girard,et al.  Feedback connections act on the early part of the responses in monkey visual cortex. , 2001, Journal of neurophysiology.

[64]  E. DeYoe,et al.  Concurrent processing in the primate visual cortex. , 1995 .

[65]  M. Posner,et al.  The attention system of the human brain. , 1990, Annual review of neuroscience.

[66]  F. Perrin,et al.  Mapping of scalp potentials by surface spline interpolation. , 1987, Electroencephalography and clinical neurophysiology.

[67]  D. Lehmann,et al.  Principles of spatial analysis , 1987 .

[68]  G. Westheimer Spatial vision. , 1984, Annual review of psychology.

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