Top-Down Modulations from Dorsal Stream in Lexical Recognition: An Effective Connectivity fMRI Study

Both the ventral and dorsal visual streams in the human brain are known to be involved in reading. However, the interaction of these two pathways and their responses to different cognitive demands remains unclear. In this study, activation of neural pathways during Chinese character reading was acquired by using a functional magnetic resonance imaging (fMRI) technique. Visual-spatial analysis (mediated by the dorsal pathway) was disassociated from lexical recognition (mediated by the ventral pathway) via a spatial-based lexical decision task and effective connectivity analysis. Connectivity results revealed that, during spatial processing, the left superior parietal lobule (SPL) positively modulated the left fusiform gyrus (FG), while during lexical processing, the left SPL received positive modulatory input from the left inferior frontal gyrus (IFG) and sent negative modulatory output to the left FG. These findings suggest that the dorsal stream is highly involved in lexical recognition and acts as a top-down modulator for lexical processing.

[1]  J. F. Stein,et al.  Magnocellular visual function and children's single word reading , 1998, Vision Research.

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

[3]  R. Buckner,et al.  Common Prefrontal Regions Coactivate with Dissociable Posterior Regions during Controlled Semantic and Phonological Tasks , 2002, Neuron.

[4]  P. Cornelissen,et al.  Motion detection, letter position encoding, and single word reading , 1998 .

[5]  R. Farivar.  Dorsal–ventral integration in object recognition , 2009, Brain Research Reviews.

[6]  Vincent L. Gracco,et al.  On the selection of words and oral motor responses: Evidence of a response-independent fronto-parietal network , 2010, Cortex.

[7]  S. Petersen,et al.  Effects of Lexicality, Frequency, and Spelling-to-Sound Consistency on the Functional Anatomy of Reading , 1999, Neuron.

[8]  K. Pammer,et al.  Spelling and Reading: Using Visual Sensitivity to Explore Shared or Separate Orthographic Representations , 2010, Perception.

[9]  M. Paradiso,et al.  Neuroscience: Exploring the Brain , 1996 .

[10]  C. Price,et al.  The Interactive Account of ventral occipitotemporal contributions to reading , 2011, Trends in Cognitive Sciences.

[11]  Cathy J. Price,et al.  Top-down modulation of ventral occipito-temporal responses during visual word recognition , 2011, NeuroImage.

[12]  S. Dehaene.  Reading in the Brain: The Science and Evolution of a Human Invention , 2009 .

[13]  S. Crewther,et al.  A role for the ‘magnocellular advantage’ in visual impairments in neurodevelopmental and psychiatric disorders , 2007, Neuroscience & Biobehavioral Reviews.

[14]  Trichur Raman Vidyasagar.  A neuronal model of attentional spotlight: parietal guiding the temporal , 1999, Brain Research Reviews.

[15]  J. Booth,et al.  Item-specific and generalization effects on brain activation when learning Chinese characters , 2008, Neuropsychologia.

[16]  R. Desimone,et al.  High-Frequency, Long-Range Coupling Between Prefrontal and Visual Cortex During Attention , 2009, Science.

[17]  Robert Oostenveld,et al.  Neural Mechanisms of Visual Attention : How Top-Down Feedback Highlights Relevant Locations , 2007 .

[18]  C. Whitney.  Serial letter-order encoding is bottom-up, not top-down: Comment on Vidyasagar and Pammer , 2010, Trends in Cognitive Sciences.

[19]  LiLi Wu,et al.  Effective connectivity of dorsal and ventral visual pathways in chunk decomposition , 2010, Science China Life Sciences.

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

[21]  T. Allison,et al.  Differential Sensitivity of Human Visual Cortex to Faces, Letterstrings, and Textures: A Functional Magnetic Resonance Imaging Study , 1996, The Journal of Neuroscience.

[22]  E. Miller,et al.  Response to Comment on "Top-Down Versus Bottom-Up Control of Attention in the Prefrontal and Posterior Parietal Cortices" , 2007, Science.

[23]  Emily B. Myers,et al.  The role of the left inferior frontal gyrus in implicit semantic competition and selection: An event-related fMRI study , 2008, Brain Research.

[24]  T R Vidyasagar,et al.  Impaired visual search in dyslexia relates to the role of the magnocellular pathway in attention. , 1999, Neuroreport.

[25]  Kwok-wing Tang,et al.  Hierarchical coding of characters in the ventral and dorsal visual streams of Chinese language processing , 2009, NeuroImage.

[26]  Florent Aubry,et al.  Testing for the Dual-Route Cascade Reading Model in the Brain: An fMRI Effective Connectivity Account of an Efficient Reading Style , 2009, PloS one.

[27]  T. Allison,et al.  Functional magnetic resonance imaging of the differential sensitivity of human visual cortex to faces, letterstrings, and textures , 1996, NeuroImage.

[28]  Tzu-Chen Yeh,et al.  Frequency effects of Chinese character processing in the brain: an event-related fMRI study , 2003, NeuroImage.

[29]  C. Price.  The anatomy of language: a review of 100 fMRI studies published in 2009 , 2010, Annals of the New York Academy of Sciences.

[30]  M. Mesulam,et al.  Shifts of Effective Connectivity within a Language Network during Rhyming and Spelling , 2005, The Journal of Neuroscience.

[31]  Trichur Raman Vidyasagar,et al.  Dyslexia: a deficit in visuo-spatial attention, not in phonological processing , 2010, Trends in Cognitive Sciences.

[32]  R. Salmelin,et al.  Dynamics of letter string perception in the human occipitotemporal cortex. , 1999, Brain : a journal of neurology.

[33]  M. Taft,et al.  The nature of the mental representation of radicals in Chinese: a priming study. , 2004, Journal of experimental psychology. Learning, memory, and cognition.

[34]  Karl J. Friston,et al.  Top-down Modulations in the Visual Form Pathway Revealed with Dynamic Causal Modeling , 2010, Cerebral cortex.

[35]  S. Petersen,et al.  Activation of extrastriate and frontal cortical areas by visual words and word-like stimuli. , 1990, Science.

[36]  K. Pammer,et al.  Attentional shifting and the role of the dorsal pathway in visual word recognition , 2006, Neuropsychologia.

[37]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

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

[39]  Marcus Taft,et al.  Positional Specificity of Radicals in Chinese Character Recognition , 1999 .

[40]  P. Cornelissen,et al.  Coherent motion detection and letter position encoding , 1998, Vision Research.

[41]  T. Allison,et al.  Word recognition in the human inferior temporal lobe , 1994, Nature.

[42]  Tai-Li Chou,et al.  Interaction Between Brain Regions During Semantic Processing in Chinese Adults , 2010 .

[43]  P. Matthews,et al.  Semantic Processing in the Left Inferior Prefrontal Cortex: A Combined Functional Magnetic Resonance Imaging and Transcranial Magnetic Stimulation Study , 2003, Journal of Cognitive Neuroscience.

[44]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[45]  J. Desmond,et al.  Functional Specialization for Semantic and Phonological Processing in the Left Inferior Prefrontal Cortex , 1999, NeuroImage.

[46]  Trichur Raman Vidyasagar,et al.  Letter-order encoding is both bottom-up and top-down: Response to Whitney , 2010, Trends in Cognitive Sciences.

[47]  Gui Xue,et al.  Language experience shapes fusiform activation when processing a logographic artificial language: An fMRI training study , 2006, NeuroImage.

[48]  Eliot Hazeltine,et al.  Dissociable Contributions of Prefrontal and Parietal Cortices to Response Selection , 2002, NeuroImage.

[49]  M. Farah,et al.  Role of left inferior prefrontal cortex in retrieval of semantic knowledge: a reevaluation. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[50]  K. Amunts,et al.  Left cytoarchitectonic area 44 supports selection in the mental lexicon during language production , 2009, Brain Structure and Function.

[51]  Po-Lei Lee,et al.  Orthographic and phonological processing of Chinese characters: an fMRI study , 2004, NeuroImage.