Cerebral regions and hemispheric specialization for processing spatial frequencies during natural scene recognition. An event-related fMRI study

It has been suggested that visual scene recognition is mainly based on spatial frequency (Fourier) analysis of the image. This analysis starts with processing low spatial frequencies (LSF), followed by processing high spatial frequencies (HSF). Within the framework of the spatial frequency analysis, the right/left hemisphere would be predominantly involved in LSF/HSF analysis, respectively. The aim of this event-related fMRI study was to evaluate neural correlates and hemispheric specialization of spatial frequency analysis during recognition of nonfiltered (NF) and filtered, either in LSF or HSF, natural scenes. Comparing LSF or NF to HSF scene recognition, significant activation was obtained within right anterior temporal cortex and right parahippocampal gyrus. As these regions are known to be involved in scene processing, we interpret this result as suggesting that scene recognition is mainly based on LSF extraction and analysis. When LSF scene was compared to HSF scene recognition, supplementary activation was obtained within the right inferior parietal lobule that likely reflects attentional modulation on spatial frequency processing. A direct interhemispheric comparison for each particular band of spatial frequencies highlighted predominance within the early visual areas (such as the middle occipital gyrus) to the right for LSF processing and to the left for HSF processing. This result provides supplementary evidence for hemispheric specialization at early levels of visual analysis when spatial frequencies are processed.

[1]  J. Marshall,et al.  Hemispheric asymmetries in global⧹local processing are modulated by perceptual salience , 1998, Neuropsychologia.

[2]  Patrik Vuilleumier,et al.  Effects of Low-Spatial Frequency Components of Fearful Faces on Fusiform Cortex Activity , 2003, Current Biology.

[3]  A. Oliva,et al.  Dr. Angry and Mr. Smile: when categorization flexibly modifies the perception of faces in rapid visual presentations , 1999, Cognition.

[4]  R. Näsänen.  Spatial frequency bandwidth used in the recognition of facial images , 1999, Vision Research.

[5]  E. Maguire,et al.  Topographical disorientation following unilateral temporal lobe lesions in humans , 1996, Neuropsychologia.

[6]  M. D’Esposito,et al.  The parahippocampus subserves topographical learning in man , 1996, NeuroImage.

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

[8]  R. A. Kinchla,et al.  Detecting target elements in multielement arrays: A confusability model , 1974 .

[9]  R Kawashima,et al.  Different time course between scene processing and face processing: a MEG study. , 1999, Neuroreport.

[10]  C. Malsburg,et al.  The role of complex cells in object recognition , 2002, Vision Research.

[11]  S. Thorpe,et al.  Speed of processing in the human visual system , 1996, Nature.

[12]  R. Knight,et al.  Component mechanisms underlying the processing of hierarchically organized patterns: inferences from patients with unilateral cortical lesions. , 1990, Journal of experimental psychology. Learning, memory, and cognition.

[13]  A. Sirigu,et al.  Pure Topographical Disorientation: A Definition and Anatomical Basis , 1987, Cortex.

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

[15]  Richard S. J. Frackowiak,et al.  Knowing where and getting there: a human navigation network. , 1998, Science.

[16]  Tetsuya Iidaka,et al.  Spatial frequency of visual image modulates neural responses in the temporo-occipital lobe. An investigation with event-related fMRI. , 2004, Brain research. Cognitive brain research.

[17]  R. Dolan,et al.  Distinct spatial frequency sensitivities for processing faces and emotional expressions , 2003, Nature Neuroscience.

[18]  T. Schormann,et al.  Functional delineation of the human occipito-temporal areas related to face and scene processing. A PET study. , 2000, Brain : a journal of neurology.

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

[20]  Joseph B. Hellige,et al.  Hemispheric differences are found in the identification, but not the detection, of low versus high spatial frequencies , 1990, Perception & psychophysics.

[21]  S. Bricogne,et al.  Neural Correlates of Topographic Mental Exploration: The Impact of Route versus Survey Perspective Learning , 2000, NeuroImage.

[22]  Antonio Torralba,et al.  Statistics of natural image categories , 2003, Network.

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

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

[25]  Arthur P. Ginsburg,et al.  Spatial filtering and visual form perception. , 1986 .

[26]  L. Robertson,et al.  Neuropsychological contributions to theories of part/whole organization , 1991, Cognitive Psychology.

[27]  J Sergent.  Influence of task and input factors on hemispheric involvement in face processing. , 1985, Journal of experimental psychology. Human perception and performance.

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

[29]  Stephen E. Palmer,et al.  Modern Theories of Gestalt Perception , 1990 .

[30]  L. Kaufman,et al.  Handbook of perception and human performance , 1986 .

[31]  Jonas Persson,et al.  Common prefrontal activations during working memory, episodic memory, and semantic memory , 2003, Neuropsychologia.

[32]  Richard S. J. Frackowiak,et al.  Age-related changes in the neural correlates of motor performance. , 2003, Brain : a journal of neurology.

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

[34]  H. Hughes,et al.  Global Precedence, Spatial Frequency Channels, and the Statistics of Natural Images , 1996, Journal of Cognitive Neuroscience.

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

[36]  Matthew Flatt,et al.  PsyScope: An interactive graphic system for designing and controlling experiments in the psychology laboratory using Macintosh computers , 1993 .

[37]  R. Cabeza,et al.  Imaging Cognition II: An Empirical Review of 275 PET and fMRI Studies , 2000, Journal of Cognitive Neuroscience.

[38]  J. Sergent.  The cerebral balance of power: confrontation or cooperation? , 1982, Journal of experimental psychology. Human perception and performance.

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

[40]  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.

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

[42]  Russell A. Epstein,et al.  The Parahippocampal Place Area Recognition, Navigation, or Encoding? , 1999, Neuron.

[43]  F. Di Russo,et al.  Electrophysiological analysis of cortical mechanisms of selective attention to high and low spatial frequencies , 2001, Clinical Neurophysiology.

[44]  D. G. Albrecht,et al.  Spatial frequency selectivity of cells in macaque visual cortex , 1982, Vision Research.

[45]  H. Hughes,et al.  Asymmetric interference between components of suprathreshold compound gratings , 1986, Perception & psychophysics.

[46]  Russell A. Epstein,et al.  Neuropsychological evidence for a topographical learning mechanism in parahippocampal cortex , 2001, Cognitive neuropsychology.

[47]  Scott O. Murray,et al.  Hemispheric Asymmetry in Global/Local Processing: Effects of Stimulus Position and Spatial Frequency , 2002, NeuroImage.

[48]  B M Gaymard,et al.  Lesions affecting the parahippocampal cortex yield spatial memory deficits in humans. , 2000, Cerebral cortex.

[49]  G. R Mangun,et al.  On the processing of spatial frequencies as revealed by evoked-potential source modeling , 2000, Clinical Neurophysiology.

[50]  Antígona Martínez,et al.  Hemispneric asymmetries in global and local processing: evidence from fMRI , 1997, Neuroreport.

[51]  Michèle Fabre-Thorpe,et al.  Brain Areas Involved in Rapid Categorization of Natural Images: An Event-Related fMRI Study , 2000, NeuroImage.

[52]  G. Mangun,et al.  Neural Mechanisms of Global and Local Processing: A Combined PET and ERP Study , 1998, Journal of Cognitive Neuroscience.

[53]  L. Nadel,et al.  Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex , 1998, Neuropsychologia.

[54]  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 .

[55]  K Zilles,et al.  A functional magnetic resonance imaging study of local/global processing with stimulus presentation in the peripheral visual hemifields , 2004, Neuroscience.

[56]  Richard S. J. Frackowiak,et al.  Recalling Routes around London: Activation of the Right Hippocampus in Taxi Drivers , 1997, The Journal of Neuroscience.

[57]  C D Frith,et al.  Neural mechanisms involved in the processing of global and local aspects of hierarchically organized visual stimuli. , 1997, Brain : a journal of neurology.

[58]  Nathalie Guyader,et al.  Image phase or amplitude? Rapid scene categorization is an amplitude-based process. , 2004, Comptes rendus biologies.

[59]  J. Sergent,et al.  Role of task factors in visual field asymmetries , 1986, Brain and Cognition.

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