A Probabilistic Functional Atlas of Human Occipito-Temporal Visual Cortex

Human visual cortex contains many retinotopic and category-specific regions. These brain regions have been the focus of a large body of functional MRI research, significantly expanding our understanding of visual processing. As studying these regions requires accurate localization of their cortical location, researchers perform functional localizer scans to identify these regions in each individual. However, it not always possible to conduct these localizer scans. Here, we developed and validated a functional region of interest atlas of early visual and category-selective regions in human ventral and lateral occipito-temporal cortex. Results show that for the majority of fROIs, cortex-based alignment results in lower between-subject variability compared to nonlinear volumetric alignment. Furthermore, we demonstrate that (1) the atlas accurately predicts the location of an independent dataset of ventral temporal cortex ROIs and other atlases of place-selectivity, motion-selectivity, and retinotopy. Next, (2) we show that the majority of voxel within our atlas are responding mostly to the labelled category in a left-out subject cross-validation, demonstrating the utility of this atlas. The functional atlas is publicly available (download.brainvoyager.com/data/visfAtlas.zip) and can help identify the location of these regions in healthy subjects as well as populations (e.g. blind people, infants) in which functional localizers cannot be run.

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

[2]  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.

[3]  S. Kasper,et al.  Prediction of Autopsy Verified Neuropathological Change of Alzheimer’s Disease Using Machine Learning and MRI , 2018, Front. Aging Neurosci..

[4]  Karl J. Friston,et al.  A direct demonstration of functional specialization in human visual cortex , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[5]  Brian A. Wandell,et al.  Population receptive field estimates in human visual cortex , 2008, NeuroImage.

[6]  K. Grill-Spector,et al.  Two New Cytoarchitectonic Areas on the Human Mid‐Fusiform Gyrus , 2015, Cerebral cortex.

[7]  Lawrence L. Wald,et al.  Accurate prediction of V1 location from cortical folds in a surface coordinate system , 2008, NeuroImage.

[8]  Katrin Amunts,et al.  The mid-fusiform sulcus: A landmark identifying both cytoarchitectonic and functional divisions of human ventral temporal cortex , 2014, NeuroImage.

[9]  Benjamin D. Singer,et al.  Retinotopic Organization of Human Ventral Visual Cortex , 2009, The Journal of Neuroscience.

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

[11]  S. Hillyard,et al.  Attending to global versus local stimulus features modulates neural processing of low versus high spatial frequencies: an analysis with event-related brain potentials , 2014, Front. Psychol..

[12]  Rebecca F. Schwarzlose,et al.  Separate Face and Body Selectivity on the Fusiform Gyrus , 2005, The Journal of Neuroscience.

[13]  R. Goebel,et al.  Mapping the Organization of Axis of Motion Selective Features in Human Area MT Using High-Field fMRI , 2011, PloS one.

[14]  Bevil R. Conway,et al.  Color-Biased Regions of the Ventral Visual Pathway Lie between Face- and Place-Selective Regions in Humans, as in Macaques , 2016, The Journal of Neuroscience.

[15]  Alex R. Wade,et al.  Visual field maps and stimulus selectivity in human ventral occipital cortex , 2005, Nature Neuroscience.

[16]  Rafael Malach,et al.  Seeing with profoundly deactivated mid-level visual areas: non-hierarchical functioning in the human visual cortex. , 2009, Cerebral Cortex.

[17]  M. D’Esposito,et al.  An Area within Human Ventral Cortex Sensitive to “Building” Stimuli Evidence and Implications , 1998, Neuron.

[18]  E. DeYoe,et al.  Mapping striate and extrastriate visual areas in human cerebral cortex. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Rainer Goebel,et al.  Functionally informed cortex based alignment: An integrated approach for whole-cortex macro-anatomical and ROI-based functional alignment , 2013, NeuroImage.

[20]  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.

[21]  Rainer Goebel,et al.  Data on a cytoarchitectonic brain atlas: effects of brain template and a comparison to a multimodal atlas , 2017, Data in brief.

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

[23]  Bruno Rossion,et al.  Understanding the functional neuroanatomy of acquired prosopagnosia , 2007, NeuroImage.

[24]  N. Kanwisher,et al.  A Cortical Area Selective for Visual Processing of the Human Body , 2001, Science.

[25]  Rainer Goebel,et al.  Analysis of functional image analysis contest (FIAC) data with brainvoyager QX: From single‐subject to cortically aligned group general linear model analysis and self‐organizing group independent component analysis , 2006, Human brain mapping.

[26]  David J. Anderson,et al.  Ventromedial hypothalamic neurons control a defensive emotion state , 2015, eLife.

[27]  Kalanit Grill-Spector,et al.  Not one extrastriate body area: Using anatomical landmarks, hMT+, and visual field maps to parcellate limb-selective activations in human lateral occipitotemporal cortex , 2011, NeuroImage.

[28]  Jonathan Winawer,et al.  Imaging retinotopic maps in the human brain , 2011, Vision Research.

[29]  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 .

[30]  Guy A. Orban,et al.  The transition in the ventral stream from feature to real-world entity representations , 2014, Front. Psychol..

[31]  Rafael Malach,et al.  Large-Scale Mirror-Symmetry Organization of Human Occipito-Temporal Object Areas , 2003, Neuron.

[32]  Daniel D. Dilks,et al.  Differential selectivity for dynamic versus static information in face-selective cortical regions , 2011, NeuroImage.

[33]  Andrew D. Engell,et al.  Probabilistic atlases for face and biological motion perception: An analysis of their reliability and overlap , 2013, NeuroImage.

[34]  J. L. de la Pompa,et al.  A novel source of arterial valve cells linked to bicuspid aortic valve without raphe in mice , 2018, eLife.

[35]  David C Van Essen,et al.  The impact of traditional neuroimaging methods on the spatial localization of cortical areas , 2018, Proceedings of the National Academy of Sciences.

[36]  Scott D. Slotnick,et al.  The Fusiform Face Area , 2013 .

[37]  G. Orban,et al.  Comparative mapping of higher visual areas in monkeys and humans , 2004, Trends in Cognitive Sciences.

[38]  Karen F. LaRocque,et al.  Where is human V4? Predicting the location of hV4 and VO1 from cortical folding. , 2014, Cerebral cortex.

[39]  Katrin Amunts,et al.  The Cytoarchitecture of Domain-specific Regions in Human High-level Visual Cortex , 2016, Cerebral cortex.

[40]  A. Schleicher,et al.  Ventral visual cortex in humans: Cytoarchitectonic mapping of two extrastriate areas , 2007, Human brain mapping.

[41]  Edward G. Jones Brodmann’s Areas , 2004 .

[42]  Leslie G. Ungerleider,et al.  Scene-Selective Cortical Regions in Human and Nonhuman Primates , 2011, The Journal of Neuroscience.

[43]  Katrin Amunts,et al.  Defining the most probable location of the parahippocampal place area using cortex-based alignment and cross-validation , 2017, NeuroImage.

[44]  P. Downing,et al.  Selectivity for the human body in the fusiform gyrus. , 2005, Journal of neurophysiology.

[45]  J. Haxby,et al.  fMRI Responses to Video and Point-Light Displays of Moving Humans and Manipulable Objects , 2003, Journal of Cognitive Neuroscience.

[46]  Liang Wang,et al.  Probabilistic Maps of Visual Topography in Human Cortex. , 2015, Cerebral cortex.

[47]  Taicheng Huang,et al.  Quantifying the variability of scene‐selective regions: Interindividual, interhemispheric, and sex differences , 2017, Human brain mapping.

[48]  R. Blake,et al.  Brain Areas Active during Visual Perception of Biological Motion , 2002, Neuron.

[49]  Bruno Rossion,et al.  The Face-Processing Network Is Resilient to Focal Resection of Human Visual Cortex , 2016, The Journal of Neuroscience.

[50]  Stefan Geyer,et al.  Brodmann's Areas , 2003 .

[51]  K. Grill-Spector,et al.  Neural representations of faces and limbs neighbor in human high-level visual cortex: evidence for a new organization principle , 2011, Psychological Research.

[52]  Nancy Kanwisher,et al.  Divide and conquer: A defense of functional localizers , 2006, NeuroImage.

[53]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[54]  Jonathan E. Jennings,et al.  An fMRI version of the Farnsworth-Munsell 100-Hue test reveals multiple color-selective areas in human ventral occipitotemporal cortex. , 1999, Cerebral cortex.

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

[56]  Rainer Goebel,et al.  Evaluating Population Receptive Field Estimation Frameworks in Terms of Robustness and Reproducibility , 2014, PloS one.

[57]  A. Caramazza,et al.  Category-Specific Organization in the Human Brain Does Not Require Visual Experience , 2009, Neuron.

[58]  Kalanit Grill-Spector,et al.  Task alters category representations in prefrontal but not high-level visual cortex , 2017, NeuroImage.

[59]  R. Malach,et al.  Object-related activity revealed by functional magnetic resonance imaging in human occipital cortex. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[60]  Kalanit Grill-Spector,et al.  Temporal Processing Capacity in High-Level Visual Cortex Is Domain Specific , 2015, The Journal of Neuroscience.

[61]  Bettina Sorger,et al.  Decoding the direction of imagined visual motion using 7 T ultra-high field fMRI , 2016, NeuroImage.

[62]  Nancy Kanwisher,et al.  Structural Connectivity Fingerprints Predict Cortical Selectivity for Multiple Visual Categories across Cortex. , 2016, Cerebral cortex.

[63]  Rainer Goebel,et al.  A cross-validated cytoarchitectonic atlas of the human ventral visual stream , 2017, NeuroImage.

[64]  Rainer Goebel,et al.  Measuring structural–functional correspondence: Spatial variability of specialised brain regions after macro-anatomical alignment , 2012, NeuroImage.

[65]  D. V. van Essen,et al.  Mapping Human Cortical Areas In Vivo Based on Myelin Content as Revealed by T1- and T2-Weighted MRI , 2011, The Journal of Neuroscience.

[66]  Kalanit Grill-Spector,et al.  Representation of shapes, edges, and surfaces across multiple cues in the human visual cortex. , 2008, Journal of neurophysiology.

[67]  Evelina Fedorenko,et al.  Subject-specific functional localizers increase . . . , 2012 .

[68]  Jia Liu,et al.  A probabilistic atlas of the human motion complex built from large‐scale functional localizer data , 2019, Human brain mapping.

[69]  H. O. D. Beeck,et al.  Development of visual category selectivity in ventral visual cortex does not require visual experience , 2017 .

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

[71]  Ricardo Nitrini,et al.  NeuroImage: Clinical , 2022 .

[72]  S. Edelman,et al.  Cue-Invariant Activation in Object-Related Areas of the Human Occipital Lobe , 1998, Neuron.

[73]  R. Saxe,et al.  Language processing in the occipital cortex of congenitally blind adults , 2011, Proceedings of the National Academy of Sciences.

[74]  K. Amunts,et al.  Brodmann's Areas 17 and 18 Brought into Stereotaxic Space—Where and How Variable? , 2000, NeuroImage.

[75]  A. Amedi,et al.  The large-scale organization of "visual" streams emerges without visual experience. , 2012, Cerebral cortex.

[76]  Sebastián M. Real,et al.  E2F1 Regulates Cellular Growth by mTORC1 Signaling , 2011, PloS one.

[77]  Patrik Vuilleumier,et al.  Differential development of selectivity for faces and bodies in the fusiform gyrus. , 2009, Developmental science.

[78]  Brian A Wandell,et al.  Visual field map clusters in human cortex , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[79]  Alan C. Evans,et al.  A new anatomical landmark for reliable identification of human area V5/MT: a quantitative analysis of sulcal patterning. , 2000, Cerebral cortex.

[80]  Bryan R. Conroy,et al.  A Common, High-Dimensional Model of the Representational Space in Human Ventral Temporal Cortex , 2011, Neuron.

[81]  A. Schleicher,et al.  Cytoarchitectonic mapping of the human dorsal extrastriate cortex , 2012, Brain Structure and Function.

[82]  A. Schleicher,et al.  Cytoarchitectonical analysis and probabilistic mapping of two extrastriate areas of the human posterior fusiform gyrus , 2012, Brain Structure and Function.

[83]  Bruno Rossion,et al.  Faces are represented holistically in the human occipito-temporal cortex , 2006, NeuroImage.

[84]  Amir Amedi,et al.  Reading with Sounds: Sensory Substitution Selectively Activates the Visual Word Form Area in the Blind , 2012, Neuron.

[85]  Petra Hermann,et al.  Transfer learning improves resting-state functional connectivity pattern analysis using convolutional neural networks , 2018, GigaScience.

[86]  A. Dale,et al.  Functional Analysis of V3A and Related Areas in Human Visual Cortex , 1997, The Journal of Neuroscience.

[87]  David H. Brainard,et al.  Correction of Distortion in Flattened Representations of the Cortical Surface Allows Prediction of V1-V3 Functional Organization from Anatomy , 2014, PLoS Comput. Biol..

[88]  Bruno Rossion,et al.  Figures and figure supplements , 2014 .

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

[90]  Jonathan Winawer,et al.  Bayesian analysis of retinotopic maps , 2018, bioRxiv.

[91]  Kenneth F. Valyear,et al.  The fusiform face area is not sufficient for face recognition: Evidence from a patient with dense prosopagnosia and no occipital face area , 2006, Neuropsychologia.

[92]  Rebecca F. Schwarzlose,et al.  Separate face and body selectivity on the fusiform gyrus. , 2010, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[93]  Nancy Kanwisher,et al.  An algorithmic method for functionally defining regions of interest in the ventral visual pathway , 2012, NeuroImage.

[94]  Kalanit Grill-Spector,et al.  Sparsely-distributed organization of face and limb activations in human ventral temporal cortex , 2010, NeuroImage.

[95]  Omar H. Butt,et al.  The Retinotopic Organization of Striate Cortex Is Well Predicted by Surface Topology , 2012, Current Biology.

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

[97]  Russell A. Poldrack,et al.  Deconvolving BOLD activation in event-related designs for multivoxel pattern classification analyses , 2012, NeuroImage.

[98]  Hua Yang,et al.  Normal Body Perception despite the Loss of Right Fusiform Gyrus , 2015, Journal of Cognitive Neuroscience.

[99]  K. Grill-Spector,et al.  The functional architecture of the ventral temporal cortex and its role in categorization , 2014, Nature Reviews Neuroscience.

[100]  Nathan Witthoft,et al.  Where Is Human V 4 ? Predicting the Location of hV 4 and VO 1 from Cortical Folding , 2013 .

[101]  Larry H Hollier,et al.  Review of "A Multi-Modal Parcellation of Human Cerebral Cortex" by Glasser M, Coalson TS, Robinson EC, Hacker CD, Harwell J, Yacoub E, Ugurbil K, Andersson J, Beckmann CF, Jenkinson M, Smith SM, Van Essen DC in Nature 536: 171-181, 2016. , 2017, The Journal of craniofacial surgery.