Areas activated during naturalistic reading comprehension overlap topological visual, auditory, and somatotomotor maps

Cortical mapping techniques using fMRI have been instrumental in identifying the boundaries of topological (neighbor-preserving) maps in early sensory areas. The presence of topological maps beyond early sensory areas raises the possibility that they might play a significant role in other cognitive systems, and that topological mapping might help to delineate areas involved in higher cognitive processes. In this study, we combine surface based visual, auditory, and somatomotor mapping methods with a naturalistic reading comprehension task in the same group of subjects to provide a qualitative and quantitative assessment of the cortical overlap between sensory-motor maps in all major sensory modalities, and reading processing regions. Our results suggest that cortical activation during naturalistic reading comprehension overlaps more extensively with topological sensory-motor maps than has been heretofore appreciated. Reading activation in regions adjacent to occipital lobe and inferior parietal lobe completely overlaps visual maps, whereas most of frontal activation for reading in dorsolateral and ventral prefrontal cortex overlaps both visual and auditory maps. Even classical language regions in superior temporal cortex are partially overlapped by topological visual and auditory maps. By contrast, the main overlap with somatomotor maps is restricted to dorsolateral frontal cortex.

[1]  Sergio E. Chaigneau,et al.  THE SIMILARITY-IN-TOPOGRAPHY PRINCIPLE: RECONCILING THEORIES OF CONCEPTUAL DEFICITS , 2003, Cognitive neuropsychology.

[2]  K. Müller,et al.  Functional architecture of verbal and tonal working memory: An FMRI study , 2009, Human brain mapping.

[3]  Lars Riecke,et al.  Parietal and superior frontal visuospatial maps activated by pointing and saccades , 2007, NeuroImage.

[4]  J. Knott The organization of behavior: A neuropsychological theory , 1951 .

[5]  Lutz Jäncke,et al.  Functional anatomy of pitch memory—an fMRI study with sparse temporal sampling , 2003, NeuroImage.

[6]  Timothy E. J. Behrens,et al.  Dissociable effects of surprise and model update in parietal and anterior cingulate cortex , 2013, Proceedings of the National Academy of Sciences.

[7]  A. Dale,et al.  High‐resolution intersubject averaging and a coordinate system for the cortical surface , 1999, Human brain mapping.

[8]  Alexander G. Huth,et al.  Attention During Natural Vision Warps Semantic Representation Across the Human Brain , 2013, Nature Neuroscience.

[9]  K. Kiehl,et al.  Neural sources involved in auditory target detection and novelty processing: an event-related fMRI study. , 2001, Psychophysiology.

[10]  Adrian T. Lee,et al.  fMRI of human visual cortex , 1994, Nature.

[11]  R. Zatorre,et al.  Voice-selective areas in human auditory cortex , 2000, Nature.

[12]  P. H. Schiller,et al.  The effects of frontal eye field and dorsomedial frontal cortex lesions on visually guided eye movements , 1998, Nature Neuroscience.

[13]  J. Kaas,et al.  Prefrontal connections of the parabelt auditory cortex in macaque monkeys , 1999, Brain Research.

[14]  M. Mishkin,et al.  Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex , 1999, Nature Neuroscience.

[15]  M. Posner,et al.  Orienting of Attention* , 1980, The Quarterly journal of experimental psychology.

[16]  C. Pierrot-Deseilligny,et al.  Eye movement control by the cerebral cortex , 2004, Current opinion in neurology.

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

[18]  Claude Alain,et al.  Assessing the auditory dual-pathway model in humans , 2004, NeuroImage.

[19]  Cathy J. Price,et al.  Auditory-Motor Expertise Alters “Speech Selectivity” in Professional Musicians and Actors , 2010, Cerebral cortex.

[20]  S. Scott,et al.  Retrieving meaning after temporal lobe infarction: The role of the basal language area , 2004, Annals of neurology.

[21]  R. Sperry Effect of 180 degree rotation of the retinal field on visuomotor coordination , 1943 .

[22]  M. Sereno,et al.  Mapping multisensory parietal face and body areas in humans , 2012, Proceedings of the National Academy of Sciences.

[23]  F. Dick,et al.  Mapping the Human Cortical Surface by Combining Quantitative T1 with Retinotopy† , 2012, Cerebral cortex.

[24]  Robert W. Cox,et al.  AFNI: What a long strange trip it's been , 2012, NeuroImage.

[25]  D. J. Felleman,et al.  Distributed hierarchical processing in the primate cerebral cortex. , 1991, Cerebral cortex.

[26]  A. Kertesz,et al.  Localization in transcortical sensory aphasia. , 1982, Archives of neurology.

[27]  Juan R. Vidal,et al.  How Silent Is Silent Reading? Intracerebral Evidence for Top-Down Activation of Temporal Voice Areas during Reading , 2012, The Journal of Neuroscience.

[28]  Brian S. Schnitzer,et al.  Eye movements and attention: The role of pre-saccadic shifts of attention in perception, memory and the control of saccades , 2012, Vision Research.

[29]  Lizabeth M. Romanski,et al.  Auditory connections and functions of prefrontal cortex , 2014, Front. Neurosci..

[30]  Stephen M. Smith,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[31]  A. Nobre,et al.  Heterogeneity of Cingulate Contributions to Spatial Attention , 2001, NeuroImage.

[32]  S. Gori,et al.  A Causal Link between Visual Spatial Attention and Reading Acquisition , 2012, Current Biology.

[33]  R P Lesser,et al.  Cognitive Effects of Resecting Basal Temporal Language Areas , 1996, Epilepsia.

[34]  K. Pammer,et al.  Making the link between dorsal stream sensitivity and reading , 2008, Neuroreport.

[35]  H. Lüders,et al.  Basal temporal language area. , 1991, Brain : a journal of neurology.

[36]  Elia Formisano,et al.  Processing of Natural Sounds in Human Auditory Cortex: Tonotopy, Spectral Tuning, and Relation to Voice Sensitivity , 2012, The Journal of Neuroscience.

[37]  Sabine Kastner,et al.  Topographic maps in human frontal cortex revealed in memory-guided saccade and spatial working-memory tasks. , 2007, Journal of neurophysiology.

[38]  René M. Müri,et al.  Neurophysiology and neuroanatomy of reflexive and volitional saccades as revealed by lesion studies with neurological patients and transcranial magnetic stimulation (TMS) , 2008, Brain and Cognition.

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

[40]  E. Courchesne,et al.  Broca's Area and the Discrimination of Frequency Transitions: A Functional MRI Study , 2001, Brain and Language.

[41]  E C Wong,et al.  Processing strategies for time‐course data sets in functional mri of the human brain , 1993, Magnetic resonance in medicine.

[42]  Noah D. Brenowitz,et al.  Whole-brain, time-locked activation with simple tasks revealed using massive averaging and model-free analysis , 2012, Proceedings of the National Academy of Sciences.

[43]  S. Kastner,et al.  Topographic maps in human frontal and parietal cortex , 2009, Trends in Cognitive Sciences.

[44]  Martin I. Sereno,et al.  Spatial maps in frontal and prefrontal cortex , 2006, NeuroImage.

[45]  B. Spehar,et al.  The Foveal Confluence in Human Visual Cortex , 2009, The Journal of Neuroscience.

[46]  F. Gosselin,et al.  The Montreal Affective Voices: A validated set of nonverbal affect bursts for research on auditory affective processing , 2008, Behavior research methods.

[47]  D. Heeger,et al.  A Hierarchy of Temporal Receptive Windows in Human Cortex , 2008, The Journal of Neuroscience.

[48]  C. Colby,et al.  Trans-saccadic perception , 2008, Trends in Cognitive Sciences.

[49]  G. Glover,et al.  Retinotopic organization in human visual cortex and the spatial precision of functional MRI. , 1997, Cerebral cortex.

[50]  Rutvik H. Desai,et al.  The neural substrates of natural reading: a comparison of normal and nonword text using eyetracking and fMRI , 2014, Front. Hum. Neurosci..

[51]  P. van Dijk,et al.  Mapping the Tonotopic Organization in Human Auditory Cortex with Minimally Salient Acoustic Stimulation , 2011, Cerebral cortex.

[52]  D. Heeger,et al.  Topographic maps of visual spatial attention in human parietal cortex. , 2005, Journal of neurophysiology.

[53]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

[54]  Jeffrey D. Schall,et al.  Supplementary Eye Field during Visual Search: Salience, Cognitive Control, and Performance Monitoring , 2012, The Journal of Neuroscience.

[55]  B. Clementz,et al.  Neurophysiology and neuroanatomy of reflexive and volitional saccades: Evidence from studies of humans , 2008, Brain and Cognition.

[56]  T. Flash,et al.  Negative blood oxygenation level dependent homunculus and somatotopic information in primary motor cortex and supplementary motor area , 2012, Proceedings of the National Academy of Sciences.

[57]  Lotfi B Merabet,et al.  Visual Topography of Human Intraparietal Sulcus , 2007, The Journal of Neuroscience.

[58]  Richard S. J. Frackowiak,et al.  Human Primary Auditory Cortex Follows the Shape of Heschl's Gyrus , 2011, The Journal of Neuroscience.

[59]  A. Dale,et al.  Tonotopic organization in human auditory cortex revealed by progressions of frequency sensitivity. , 2004, Journal of neurophysiology.

[60]  G. Egan,et al.  Quantitative meta-analysis of fMRI and PET studies reveals consistent activation in fronto-striatal-parietal regions and cerebellum during antisaccades and prosaccades , 2013, Front. Psychol..

[61]  Steen Moeller,et al.  Multiband multislice GE‐EPI at 7 tesla, with 16‐fold acceleration using partial parallel imaging with application to high spatial and temporal whole‐brain fMRI , 2010, Magnetic resonance in medicine.

[62]  M. Sereno,et al.  Retinotopy and Attention in Human Occipital, Temporal, Parietal, and Frontal Cortex , 2008 .

[63]  Jon H Kaas,et al.  Topographic Maps are Fundamental to Sensory Processing , 1997, Brain Research Bulletin.

[64]  H. Lüders,et al.  Evidence for a basal temporal visual language center , 2008, Neurology.

[65]  J. Gabrieli,et al.  Reading Abilities: Importance of Visual-Spatial Attention , 2012, Current Biology.

[66]  R. Goebel,et al.  Mirror-Symmetric Tonotopic Maps in Human Primary Auditory Cortex , 2003, Neuron.

[67]  Henry Kennedy,et al.  A Predictive Network Model of Cerebral Cortical Connectivity Based on a Distance Rule , 2013, Neuron.

[68]  Colin Humphries,et al.  Tonotopic organization of human auditory cortex , 2010, NeuroImage.

[69]  F. Dick,et al.  In Vivo Functional and Myeloarchitectonic Mapping of Human Primary Auditory Areas , 2012, The Journal of Neuroscience.

[70]  M. Sereno,et al.  Mapping of Contralateral Space in Retinotopic Coordinates by a Parietal Cortical Area in Humans , 2001, Science.

[71]  J. B. Levitt,et al.  Comparison of intrinsic connectivity in different areas of macaque monkey cerebral cortex. , 1993, Cerebral cortex.

[72]  Joseph B. Sala,et al.  Dissociable functional cortical topographies for working memory maintenance of voice identity and location. , 2004, Cerebral cortex.

[73]  Richard S. J. Frackowiak,et al.  The structural components of music perception. A functional anatomical study. , 1997, Brain : a journal of neurology.

[74]  D. Heeger,et al.  Retinotopy and Functional Subdivision of Human Areas MT and MST , 2002, The Journal of Neuroscience.

[75]  S. Kastner,et al.  Attention in the real world: toward understanding its neural basis , 2014, Trends in Cognitive Sciences.

[76]  G. Marcus,et al.  The topographic brain: from neural connectivity to cognition , 2007, Trends in Neurosciences.

[77]  M. Potter,et al.  Pictures in sentences: understanding without words. , 1986, Journal of experimental psychology. General.

[78]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

[79]  Ruey-Song Huang,et al.  Bottom-up Retinotopic Organization Supports Top-down Mental Imagery , 2013, The open neuroimaging journal.

[80]  C. Grady,et al.  “What” and “where” in the human auditory system , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[81]  R. Luján Fiber Pathways of the Brain, J.D. Schmahmann, D.N. Pandya (Eds.). Oxford University Press (2006), ISBN: 0-19-510423-4 , 2008 .

[82]  Bruce Fischl,et al.  Accurate and robust brain image alignment using boundary-based registration , 2009, NeuroImage.

[83]  B. Wandell,et al.  Visual Field Maps in Human Cortex , 2007, Neuron.

[84]  Martin I. Sereno,et al.  Cortical visual areas in mammals , 1991 .

[85]  R P Lesser,et al.  Characterization of the basal temporal language area in patients with left temporal lobe epilepsy , 1990, Neurology.

[86]  D. Heeger,et al.  Topographic organization for delayed saccades in human posterior parietal cortex. , 2005, Journal of neurophysiology.