Dissociation of Sensitivity to Spatial Frequency in Word and Face Preferential Areas of the Fusiform Gyrus

Different cortical regions within the ventral occipitotemporal junction have been reported to show preferential responses to particular objects. Thus, it is argued that there is evidence for a left-lateralized visual word form area and a right-lateralized fusiform face area, but the unique specialization of these areas remains controversial. Words are characterized by greater power in the high spatial frequency (SF) range, whereas faces comprise a broader range of high and low frequencies. We investigated how these high-order visual association areas respond to simple sine-wave gratings that varied in SF. Using functional magnetic resonance imaging, we demonstrated lateralization of activity that was concordant with the low-level visual property of words and faces; left occipitotemporal cortex is more strongly activated by high than by low SF gratings, whereas the right occipitotemporal cortex responded more to low than high spatial frequencies. Therefore, the SF of a visual stimulus may bias the lateralization of processing irrespective of its higher order properties.

[1]  J. C. Meadows The anatomical basis of prosopagnosia , 1974, Journal of neurology, neurosurgery, and psychiatry.

[2]  B Milner,et al.  THE ROLE OF EARLY LEFT‐BRAIN INJURY IN DETERMINING LATERALIZATION OF CEREBRAL SPEECH FUNCTIONS , 1977, Annals of the New York Academy of Sciences.

[3]  Genjiro Hirose,et al.  Alexia without agraphia associated with right occipital lesion. , 1977, Journal of neurology, neurosurgery, and psychiatry.

[4]  S. Erkulvrawatr Alexia and left homonymous hemianopia in a non‐right‐hander , 1978, Annals of neurology.

[5]  J. Polich,et al.  Hemispheric differences in stimulus identification , 1978, Perception & psychophysics.

[6]  G. Tassinari,et al.  Iconic storage in the two hemispheres. , 1979, Journal of experimental psychology. Human perception and performance.

[7]  J Sergent,et al.  Theoretical and methodological consequences of variations in exposure duration in visual laterality studies , 1982, Perception & psychophysics.

[8]  G. V. Van Hoesen,et al.  Prosopagnosia , 1982, Neurology.

[9]  A. Damasio,et al.  The anatomic basis of pure alexia , 1983, Neurology.

[10]  J Sergent,et al.  Role of the input in visual hemispheric asymmetries. , 1983, Psychological bulletin.

[11]  M. Winkelman,et al.  Unilateral right cerebral representation of reading in a familial left-hander , 1984, Neuropsychologia.

[12]  W. Lovegrove,et al.  Spatial frequency processing and the prediction of reading ability: A preliminary investigation , 1986, Perception & psychophysics.

[13]  B. Pillon,et al.  Alexia without agraphia in a left-handed patient with a right occipital lesion. , 1987, Archives of neurology.

[14]  A. Benton Facial Recognition 1990 , 1990, Cortex.

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

[16]  J. Binder,et al.  The topography of callosal reading pathways. A case-control analysis. , 1992, Brain : a journal of neurology.

[17]  J. Sergent,et al.  Functional neuroanatomy of face and object processing. A positron emission tomography study. , 1992, Brain : a journal of neurology.

[18]  R. Groner,et al.  Facets of dyslexia and its remediation , 1993 .

[19]  P. Cornelissen Fixation, Contrast Sensitivity and Children's Reading , 1993 .

[20]  Leslie G. Ungerleider,et al.  ‘What’ and ‘where’ in the human brain , 1994, Current Opinion in Neurobiology.

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

[22]  T. Allison,et al.  Face-Specific Processing in the Human Fusiform Gyrus , 1997, Journal of Cognitive Neuroscience.

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

[24]  M. Mesulam,et al.  From sensation to cognition. , 1998, Brain : a journal of neurology.

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

[26]  Anders M. Dale,et al.  Cortical Surface-Based Analysis I. Segmentation and Surface Reconstruction , 1999, NeuroImage.

[27]  D. Loring,et al.  The occurrence of depressive symptoms in the preclinical phase of AD , 1999, Neurology.

[28]  R W Cox,et al.  Real‐time 3D image registration for functional MRI , 1999, Magnetic resonance in medicine.

[29]  A. Dale,et al.  Cortical Surface-Based Analysis II: Inflation, Flattening, and a Surface-Based Coordinate System , 1999, NeuroImage.

[30]  J. Grafman,et al.  A Case of Prosopagnosia Following Moderate Closed Head Injury with Left Hemisphere Focal Lesion , 2000, Cortex.

[31]  B. Skottun,et al.  The magnocellular deficit theory of dyslexia: the evidence from contrast sensitivity , 2000, Vision Research.

[32]  S Lehéricy,et al.  The visual word form area: spatial and temporal characterization of an initial stage of reading in normal subjects and posterior split-brain patients. , 2000, Brain : a journal of neurology.

[33]  Keith J. Worsley,et al.  Statistical analysis of activation images , 2001 .

[34]  Talma Hendler,et al.  Center–periphery organization of human object areas , 2001, Nature Neuroscience.

[35]  S Marrett,et al.  Local and global attention are mapped retinotopically in human occipital cortex. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Michael Wilson MRC Psycholinguistic Database , 2001 .

[37]  Talma Hendler,et al.  Eccentricity Bias as an Organizing Principle for Human High-Order Object Areas , 2002, Neuron.

[38]  S. Dehaene,et al.  Language-specific tuning of visual cortex? Functional properties of the Visual Word Form Area. , 2002, Brain : a journal of neurology.

[39]  Stephen M. Smith,et al.  Functional MRI : an introduction to methods , 2002 .

[40]  G Jobard,et al.  Evaluation of the dual route theory of reading: a metanalysis of 35 neuroimaging studies , 2003, NeuroImage.

[41]  Franc Solina,et al.  COLOR-BASED FACE DETECTION IN THE "15 SECONDS OF FAME" ART INSTALLATION , 2003 .

[42]  Mark W. Woolrich,et al.  Advances in functional and structural MR image analysis and implementation as FSL , 2004, NeuroImage.

[43]  W. Levelt,et al.  The spatial and temporal signatures of word production components , 2004, Cognition.

[44]  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.

[45]  Raymond J. Dolan,et al.  Familiarity enhances invariance of face representations in human ventral visual cortex: fMRI evidence , 2005, NeuroImage.

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

[47]  A. Leff,et al.  Structural anatomy of pure and hemianopic alexia , 2006, Journal of Neurology, Neurosurgery & Psychiatry.

[48]  Nathalie Guyader,et al.  Neural correlates of spatial frequency processing: A neuropsychological approach , 2006, Brain Research.

[49]  A. Hyvärinen,et al.  Spatial frequency tuning in human retinotopic visual areas. , 2008, Journal of vision.

[50]  Frederic Dick,et al.  Differential Lateralization for Words and Faces: Category or Psychophysics? , 2008, Journal of Cognitive Neuroscience.

[51]  Jason J.S. Barton,et al.  Prosopagnosia associated with a left occipitotemporal lesion , 2008, Neuropsychologia.

[52]  J. Barton Structure and function in acquired prosopagnosia: lessons from a series of 10 patients with brain damage. , 2008, Journal of neuropsychology.

[53]  Marc Brysbaert,et al.  Cerebral Lateralization of Frontal Lobe Language Processes and Lateralization of the Posterior Visual Word Processing System , 2008, Journal of Cognitive Neuroscience.

[54]  Marlene Behrmann,et al.  Visuoperceptual deficits in letter-by-letter reading? , 2009, Neuropsychologia.

[55]  Alexander P. Leff,et al.  Too Little, Too Late: Reduced Visual Span and Speed Characterize Pure Alexia , 2009, Cerebral cortex.

[56]  Roel M. Willems,et al.  Cerebral lateralization of face-selective and body-selective visual areas depends on handedness. , 2010, Cerebral cortex.

[57]  Tom Hartley,et al.  Selectivity for low-level features of objects in the human ventral stream , 2010, NeuroImage.

[58]  Philippe Pinel,et al.  Cortical representations of symbols, objects, and faces are pruned back during early childhood. , 2011, Cerebral cortex.