Distinct role of spatial frequency in dissociative reading of ideograms and phonograms: An fMRI study

It has been proposed that distinct neural circuits are activated by reading Japanese ideograms (Kanji) and phonograms (Kana). By measuring high-density event-related potentials, we recently reported that spatial frequency (SF) information is responsible for the dissociation between Kanji and Kana reading. In particular, we found close links between Kana and low SF (LSF) information and between Kanji and high SF (HSF) information. However, it remains unclear which brain regions contribute to this dissociation. To determine this, we performed functional magnetic resonance imaging while presenting unfiltered or spatially filtered Kanji and Kana word stimuli to healthy native Japanese subjects. Fourier analysis revealed that Kanji and Kana stimuli were characterized by HSF and LSF information, respectively. When presented with either type of unfiltered stimulus (Kanji or Kana), the bilateral inferior temporal (IT, BA 37) regions were activated compared to the resting condition. Kana but not Kanji reading also activated the bilateral inferior parietal lobules (IPL, BA 40). When we compared Kanji and Kana reading directly, the left IT region was significantly activated by Kanji reading, while significant activation of the left IPL was observed during Kana reading. In response to filtered HSF stimuli, the Kanji reading minus Kana reading comparison revealed significant activation of the left IT region but not the left IPL. Conversely, significant activation of the left IPL but not the left IT region occurred in the Kana reading minus Kanji reading comparison for filtered LSF stimuli. These results suggest that Kanji and Kana engage a relatively overlapping network, within which the left IT is more involved in Kanji processing, while the left IPL contributes more to Kana processing. The preferential engagements of these brain regions could reflect the close links between Kana and LSF information, and between Kanji and HSF information. Therefore, this study provides further evidence that SF contributes to the dissociation between Kanji and Kana reading.

[1]  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.

[2]  Makoto Iwata,et al.  Kanji versus Kananeuropsychological correlates of the Japanese writing system , 1984, Trends in Neurosciences.

[3]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[4]  M. Bar,et al.  Magnocellular Projections as the Trigger of Top-Down Facilitation in Recognition , 2007, The Journal of Neuroscience.

[5]  Fumio Shishido,et al.  Alexia with agraphia due to the left posterior inferior temporal lobe lesion—Neuropsychological analysis and its pathogenetic mechanisms , 1988, Brain and Language.

[6]  A. Friederici.  Event-related brain potential studies in language , 2004, Current neurology and neuroscience reports.

[7]  S. Tobimatsu,et al.  Studies of human visual pathophysiology with visual evoked potentials , 2006, Clinical Neurophysiology.

[8]  M. Sereno,et al.  Dissociation of Sensitivity to Spatial Frequency in Word and Face Preferential Areas of the Fusiform Gyrus , 2011, Cerebral cortex.

[9]  Masune Sukigara,et al.  Visual Word Form Familiarity and Attention in Lateral Difference during Processing Japanese Kana Words , 2000, Brain and Language.

[10]  Hai Zhao,et al.  Character-Level Dependencies in Chinese: Usefulness and Learning , 2009, EACL.

[11]  D. Hubel,et al.  Segregation of form, color, movement, and depth: anatomy, physiology, and perception. , 1988, Science.

[12]  S. Petersen,et al.  The left occipitotemporal cortex does not show preferential activity for words. , 2012, Cerebral cortex.

[13]  Shozo Tobimatsu.  Visual Gnosis and Face Perception , 2012 .

[14]  Cathy J. Price,et al.  Explaining Left Lateralization for Words in the Ventral Occipitotemporal Cortex , 2011, The Journal of Neuroscience.

[15]  Hidenao Fukuyama,et al.  Temporal Dynamics of Japanese Morphogram and Syllabogram Processing in the Left Basal Temporal Area Studied by Event-Related Potentials , 2009, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[16]  Hideaki Fujita,et al.  Left supramarginal/angular gyri activation during reading of syllabograms in the Japanese language , 1991, Journal of Neurolinguistics.

[17]  D. Giaschi,et al.  The role of low-spatial frequencies in lexical decision and masked priming , 2009, Brain and Cognition.

[18]  I. Kanazawa,et al.  Different cortical activity in reading of Kanji words, Kana words and Kana nonwords. , 2000, Brain research. Cognitive brain research.

[19]  Hidenao Fukuyama,et al.  Transient Functional Suppression and Facilitation of Japanese Ideogram Writing Induced by Repetitive Transcranial Magnetic Stimulation of Posterior Inferior Temporal Cortex , 2006, The Journal of Neuroscience.

[20]  Hidenao Fukuyama,et al.  Implicit and explicit processing of kanji and kana words and non-words studied with fMRI , 2004, NeuroImage.

[21]  Shoji Tsuji,et al.  Pure alexia for kana. Characterization of alexia with lesions of the inferior occipital cortex , 2008, Journal of the Neurological Sciences.

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

[23]  R. Hari,et al.  What differs in visual recognition of handwritten vs. printed letters? An fMRI study , 2011, Human brain mapping.

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

[25]  A Yamadori,et al.  Ideogram reading in alexia. , 1975, Brain : a journal of neurology.

[26]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[27]  Stanislas Dehaene,et al.  Subliminal Convergence of Kanji and Kana Words: Further Evidence for Functional Parcellation of the Posterior Temporal Cortex in Visual Word Perception , 2005, Journal of Cognitive Neuroscience.

[28]  Stanislas Dehaene,et al.  Task-specific change of unconscious neural priming in the cerebral language network , 2007, Proceedings of the National Academy of Sciences.

[29]  Katsuya Ogata,et al.  Differential roles of spatial frequency on reading processes for ideograms and phonograms: A high-density ERP study , 2012, Neuroscience Research.

[30]  L. Pylkkänen,et al.  Tracking the time course of word recognition with MEG , 2003, Trends in Cognitive Sciences.

[31]  M. Sugishita,et al.  A critical appraisal of neuropsychological correlates of Japanese ideogram (kanji) and phonogram (kana) reading. , 1992, Brain : a journal of neurology.

[32]  R. Salmelin.  Clinical neurophysiology of language: The MEG approach , 2007, Clinical Neurophysiology.

[33]  Mei-Ching Lien,et al.  A multistream model of visual word recognition , 2009, Attention, perception & psychophysics.

[34]  W. Schneider,et al.  Cross‐cultural effect on the brain revisited: Universal structures plus writing system variation , 2005, Human brain mapping.

[35]  Ron Borowsky,et al.  Neuroimaging of language processes: fMRI of silent and overt lexical processing and the promise of multiple process imaging in single brain studies. , 2005, Canadian Association of Radiologists journal = Journal l'Association canadienne des radiologistes.

[36]  D. Pelli,et al.  The role of spatial frequency channels in letter identification , 2002, Vision Research.

[37]  K. Alexander,et al.  Spatial-frequency characteristics of letter identification. , 1994, Journal of the Optical Society of America. A, Optics, image science, and vision.

[38]  Denis G. Pelli,et al.  The visual filter mediating letter identification , 1994, Nature.

[39]  Hidenao Fukuyama,et al.  Recognition and reading aloud of kana and kanji word: An fMRI study , 2009, Brain Research Bulletin.

[40]  N Osaka,et al.  Size of saccade and fixation duration of eye movements during reading: psychophysics of Japanese text processing. , 1992, Journal of the Optical Society of America. A, Optics and image science.

[41]  Kensuke Sekihara,et al.  Activation of Lateral Extrastriate Areas during Orthographic Processing of Japanese Characters Studied with fMRI , 1999, NeuroImage.