Two distinct scene processing networks connecting vision and memory

A number of regions in the human brain are known to be involved in processing natural scenes, but the field has lacked a unifying framework for understanding how these different regions are organized and interact. We provide evidence from functional connectivity and meta-analyses for a new organizational principle, in which scene processing relies on two distinct networks that split the classically defined Parahippocampal Place Area (PPA). The first network consists of the Occipital Place Area (OPA/TOS) and posterior PPA, which contain retinotopic maps and are related primarily to visual features. The second network consists of the caudal Inferior Parietal Lobule (cIPL), Retrosplenial Cortex (RSC), and anterior PPA, which connect to the hippocampus and are involved in a much broader set of tasks involving episodic memory and navigation. This new framework for understandingthe neural substrates of scene processing bridges results from many lines of research, and makes specific functional predictions.

[1]  J. Robson,et al.  Application of fourier analysis to the visibility of gratings , 1968, The Journal of physiology.

[2]  Leslie G. Ungerleider,et al.  Object vision and spatial vision: two cortical pathways , 1983, Trends in Neurosciences.

[3]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

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

[5]  N. Kanwisher,et al.  Mental Imagery of Faces and Places Activates Corresponding Stimulus-Specific Brain Regions , 2000, Journal of Cognitive Neuroscience.

[6]  T. Schormann,et al.  Functional delineation of the human occipito-temporal areas related to face and scene processing. A PET study. , 2000, Brain : a journal of neurology.

[7]  E. Maguire,et al.  A Temporoparietal and Prefrontal Network for Retrieving the Spatial Context of Lifelike Events , 2001, NeuroImage.

[8]  R. Malach,et al.  The topography of high-order human object areas , 2002, Trends in Cognitive Sciences.

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

[10]  J Marshall,et al.  Hiding in plain view , 2003, The British journal of ophthalmology.

[11]  Neal J. Cohen,et al.  Processing and short-term retention of relational information in amnesia , 2004, Neuropsychologia.

[12]  L. Chalupa,et al.  The visual neurosciences , 2004 .

[13]  E. J. Green,et al.  Head-direction cells in the rat posterior cortex , 1994, Experimental Brain Research.

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

[15]  Andy C. H. Lee,et al.  Specialization in the medial temporal lobe for processing of objects and scenes , 2005, Hippocampus.

[16]  Russell A. Epstein,et al.  Perceptual deficits in amnesia: challenging the medial temporal lobe ‘mnemonic’ view , 2005, Neuropsychologia.

[17]  B. McNaughton,et al.  Declarative memory consolidation in humans: a prospective functional magnetic resonance imaging study. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[18]  Andy C. H. Lee,et al.  Abnormal Categorization and Perceptual Learning in Patients with Hippocampal Damage , 2006, The Journal of Neuroscience.

[19]  D. Montaldi,et al.  The neural system that mediates familiarity memory , 2006, Hippocampus.

[20]  Russell A. Epstein,et al.  Where Am I Now? Distinct Roles for Parahippocampal and Retrosplenial Cortices in Place Recognition , 2007, The Journal of Neuroscience.

[21]  Russell A. Epstein,et al.  Visual scene processing in familiar and unfamiliar environments. , 2007, Journal of neurophysiology.

[22]  Jeffrey D. Johnson,et al.  Recollection and the reinstatement of encoding-related cortical activity. , 2007, Cerebral cortex.

[23]  S. Becker,et al.  Remembering the past and imagining the future: a neural model of spatial memory and imagery. , 2007, Psychological review.

[24]  D. Hassabis,et al.  Using Imagination to Understand the Neural Basis of Episodic Memory , 2007, The Journal of Neuroscience.

[25]  D. Hassabis,et al.  Deconstructing episodic memory with construction , 2007, Trends in Cognitive Sciences.

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

[27]  R. Nathan Spreng,et al.  The Common Neural Basis of Autobiographical Memory, Prospection, Navigation, Theory of Mind, and the Default Mode: A Quantitative Meta-analysis , 2009, Journal of Cognitive Neuroscience.

[28]  Soojin Park,et al.  Different roles of the parahippocampal place area (PPA) and retrosplenial cortex (RSC) in panoramic scene perception , 2009, NeuroImage.

[29]  K. Szpunar,et al.  Contextual processing in episodic future thought. , 2009, Cerebral cortex.

[30]  E. Maguire,et al.  What does the retrosplenial cortex do? , 2009, Nature Reviews Neuroscience.

[31]  Hongkeun Kim,et al.  Dissociating the roles of the default-mode, dorsal, and ventral networks in episodic memory retrieval , 2010, NeuroImage.

[32]  Emily J. Ward,et al.  Eye-centered encoding of visual space in scene-selective regions. , 2010, Journal of vision.

[33]  Hans P. Op de Beeck,et al.  Continuous mapping of the cortical object vision pathway using traveling waves in object space , 2010, NeuroImage.

[34]  R. Buckner,et al.  Functional-Anatomic Fractionation of the Brain's Default Network , 2010, Neuron.

[35]  Philippe Lefèvre,et al.  Biological motion drives perception and action. , 2010, Journal of vision.

[36]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[37]  Russell A. Poldrack,et al.  Large-scale automated synthesis of human functional neuroimaging data , 2011, Nature Methods.

[38]  Russell A. Epstein,et al.  Distances between Real-World Locations Are Represented in the Human Hippocampus , 2011, The Journal of Neuroscience.

[39]  C. Honey,et al.  Topographic Mapping of a Hierarchy of Temporal Receptive Windows Using a Narrated Story , 2011, The Journal of Neuroscience.

[40]  Dwight J. Kravitz,et al.  A new neural framework for visuospatial processing , 2011, Nature Reviews Neuroscience.

[41]  Natalia Y. Bilenko,et al.  The “Parahippocampal Place Area” Responds Preferentially to High Spatial Frequencies in Humans and Monkeys , 2011, PLoS biology.

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

[43]  Nadim Joni Shah,et al.  Probabilistic fibre tract analysis of cytoarchitectonically defined human inferior parietal lobule areas reveals similarities to macaques , 2011, NeuroImage.

[44]  Lily Riggs,et al.  The hippocampus supports multiple cognitive processes through relational binding and comparison , 2012, Front. Hum. Neurosci..

[45]  Kelly Baker,et al.  Identity, Memory and Place , 2012 .

[46]  C. Ranganath,et al.  Two cortical systems for memory-guided behaviour , 2012, Nature Reviews Neuroscience.

[47]  Brian Barton,et al.  Visual Field Map Organization in Human Visual Cortex , 2012 .

[48]  Kaia L. Vilberg,et al.  Age differences in the neural correlates of recollection: transient versus sustained fMRI effects , 2012, Neurobiology of Aging.

[49]  Jean Rouat,et al.  Visual Cortex - Current Status and Perspectives , 2012 .

[50]  Neal J Cohen,et al.  Hiding in plain view: Lesions of the medial temporal lobe impair online representation , 2012, Hippocampus.

[51]  Nancy Kanwisher,et al.  Cerebral Cortex doi:10.1093/cercor/bhr357 Higher Level Visual Cortex Represents Retinotopic, Not Spatiotopic, Object Location , 2011 .

[52]  D. Schacter,et al.  Remembering the Past and Imagining the Future in the Elderly , 2012, Gerontology.

[53]  A. Caramazza,et al.  Tripartite Organization of the Ventral Stream by Animacy and Object Size , 2013, The Journal of Neuroscience.

[54]  Dominique Hasboun,et al.  Resting State Networks' Corticotopy: The Dual Intertwined Rings Architecture , 2013, PloS one.

[55]  A. Schleicher,et al.  Organization of the Human Inferior Parietal Lobule Based on Receptor Architectonics , 2012, Cerebral cortex.

[56]  Li Fei-Fei,et al.  Differential Connectivity Within the Parahippocampal Place Area , 2013 .

[57]  Essa Yacoub,et al.  The WU-Minn Human Connectome Project: An overview , 2013, NeuroImage.

[58]  Russell A. Epstein,et al.  Abstract Representations of Location and Facing Direction in the Human Brain , 2013, The Journal of Neuroscience.

[59]  A. Bartels,et al.  Parietal Cortex Codes for Egocentric Space beyond the Field of View , 2012, Current Biology.

[60]  Yaoda Xu,et al.  The Role of Transverse Occipital Sulcus in Scene Perception and Its Relationship to Object Individuation in Inferior Intraparietal Sulcus , 2013, Journal of Cognitive Neuroscience.

[61]  Roger B. H. Tootell,et al.  Spatial encoding and underlying circuitry in scene-selective cortex , 2013, NeuroImage.

[62]  Dwight J. Kravitz,et al.  The ventral visual pathway: an expanded neural framework for the processing of object quality , 2013, Trends in Cognitive Sciences.

[63]  Arthur P. Shimamura,et al.  Dynamic changes in parietal activation during encoding: Implications for human learning and memory , 2013, NeuroImage.

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

[65]  R. Tootell,et al.  Thinking Outside the Box: Rectilinear Shapes Selectively Activate Scene-Selective Cortex , 2014, The Journal of Neuroscience.

[66]  Ludovica Griffanti,et al.  Automatic denoising of functional MRI data: Combining independent component analysis and hierarchical fusion of classifiers , 2014, NeuroImage.

[67]  R. N. Spreng,et al.  The default network and self‐generated thought: component processes, dynamic control, and clinical relevance , 2014, Annals of the New York Academy of Sciences.

[68]  Russell A. Epstein,et al.  Neural systems for landmark-based wayfinding in humans , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[69]  Russell A. Epstein,et al.  Anchoring the neural compass: Coding of local spatial reference frames in human medial parietal lobe , 2014, Nature Neuroscience.

[70]  Alfonso Caramazza,et al.  Person- and place-selective neural substrates for entity-specific semantic access. , 2014, Cerebral cortex.

[71]  Aapo Hyvärinen,et al.  Group-PCA for very large fMRI datasets , 2014, NeuroImage.

[72]  H. Eichenbaum,et al.  Can We Reconcile the Declarative Memory and Spatial Navigation Views on Hippocampal Function? , 2014, Neuron.

[73]  Lily M. Solomon-Harris,et al.  TMS to object cortex affects both object and scene remote networks while TMS to scene cortex only affects scene networks , 2015, Neuropsychologia.

[74]  Aude Oliva,et al.  Parametric Coding of the Size and Clutter of Natural Scenes in the Human Brain. , 2014, Cerebral cortex.

[75]  C. Honey,et al.  Hierarchical process memory: memory as an integral component of information processing , 2015, Trends in Cognitive Sciences.

[76]  Christopher L. Asplund,et al.  Functional Specialization and Flexibility in Human Association Cortex. , 2015, Cerebral cortex.

[77]  Li Fei-Fei,et al.  Parcellating connectivity in spatial maps , 2015, PeerJ.

[78]  Aiden E. G. F. Arnold,et al.  Spatial and temporal functional connectivity changes between resting and attentive states , 2015, Human brain mapping.

[79]  Michael J. Tarr,et al.  Associative Processing Is Inherent in Scene Perception , 2015, PloS one.

[80]  Drew Linsley,et al.  Encoding-Stage Crosstalk Between Object- and Spatial Property-Based Scene Processing Pathways. , 2015, Cerebral cortex.

[81]  Nathalie Guyader,et al.  Spatial frequency processing in scene-selective cortical regions , 2015, NeuroImage.

[82]  Dwight J. Kravitz,et al.  A Retinotopic Basis for the Division of High-Level Scene Processing between Lateral and Ventral Human Occipitotemporal Cortex , 2015, The Journal of Neuroscience.

[83]  Russell A. Epstein,et al.  Outside Looking In: Landmark Generalization in the Human Navigational System , 2015, The Journal of Neuroscience.

[84]  David J. Foster,et al.  Memory and Space: Towards an Understanding of the Cognitive Map , 2015, The Journal of Neuroscience.

[85]  J. Knierim The hippocampus , 2015, Current Biology.

[86]  E. Maguire,et al.  Constructing, Perceiving, and Maintaining Scenes: Hippocampal Activity and Connectivity , 2014, Cerebral cortex.

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

[88]  Tom Hartley,et al.  Patterns of neural response in scene-selective regions of the human brain are affected by low-level manipulations of spatial frequency , 2016, NeuroImage.

[89]  Sophie-Carolin Wagner,et al.  The Neural System , 2016 .

[90]  A. Lawrence,et al.  Evidencing a place for the hippocampus within the core scene processing network , 2016, Human brain mapping.

[91]  Patrik Vuilleumier,et al.  Functional Dissociations Within Posterior Parietal Cortex During Scene Integration and Viewpoint Changes. , 2014, Cerebral cortex.

[92]  E. Maguire,et al.  Anterior hippocampus: the anatomy of perception, imagination and episodic memory , 2016, Nature Reviews Neuroscience.

[93]  Ryan V. Ringer,et al.  Impairing the useful field of view in natural scenes: Tunnel vision versus general interference. , 2016, Journal of vision.

[94]  Christopher A. Baldassano,et al.  Pinpointing the peripheral bias in neural scene-processing networks during natural viewing. , 2016, Journal of vision.

[95]  Chris I. Baker,et al.  Evaluating the correspondence between face-, scene-, and object-selectivity and retinotopic organization within lateral occipitotemporal cortex , 2016, Journal of vision.

[96]  Moshe Bar,et al.  Cortical Integration of Contextual Information across Objects , 2016, Journal of Cognitive Neuroscience.

[97]  Russell A. Epstein,et al.  The Occipital Place Area Is Causally Involved in Representing Environmental Boundaries during Navigation , 2016, Current Biology.

[98]  Christopher L. Asplund,et al.  Functional Specialization and Flexibility in Human Association Cortex. , 2016, Cerebral cortex.

[99]  Russell A. Epstein,et al.  Rectilinear Edge Selectivity Is Insufficient to Explain the Category Selectivity of the Parahippocampal Place Area , 2016, Front. Hum. Neurosci..

[100]  Christopher Baldassano,et al.  Human‐Object Interactions Are More than the Sum of Their Parts , 2016, Cerebral cortex.