Two Distinct Scene-Processing Networks Connecting Vision and Memory

Visual Abstract 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 upon two distinct networks that split the classically defined parahippocampal place area (PPA). The first network of strongly connected regions consists of the occipital place area/transverse occipital sulcus and posterior PPA, which contain retinotopic maps and are not strongly coupled to the hippocampus at rest. The second network consists of the caudal inferior parietal lobule, retrosplenial complex, and anterior PPA, which connect to the hippocampus (especially anterior hippocampus), and are implicated in both visual and nonvisual tasks, including episodic memory and navigation. We propose that these two distinct networks capture the primary functional division among scene-processing regions, between those that process visual features from the current view of a scene and those that connect information from a current scene view with a much broader temporal and spatial context. This new framework for understanding the neural substrates of scene-processing bridges results from many lines of research, and makes specific functional predictions.

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

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

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

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

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

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

[7]  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.

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

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

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

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

[12]  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.

[13]  D. Newport,et al.  Transient natural convection in a conducting enclosure heated from above , 2013, J. Vis..

[14]  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.

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

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

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

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

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

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

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

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

[23]  Tal Makovski,et al.  The visual attractor illusion. , 2010, Journal of vision.

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

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

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

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

[28]  Hallvard Røe Evensmoen,et al.  Long-axis specialization of the human hippocampus , 2013, Trends in Cognitive Sciences.

[29]  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.

[30]  Mary Hegarty,et al.  The Human Retrosplenial Cortex and Thalamus Code Head Direction in a Global Reference Frame , 2016, The Journal of Neuroscience.

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

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

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

[34]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

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

[36]  C. Baker,et al.  Scene-Selectivity and Retinotopy in Medial Parietal Cortex , 2016, Front. Hum. Neurosci..

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

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

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

[40]  Daniel D. Dilks,et al.  The occipital place area represents the local elements of scenes , 2016, NeuroImage.

[41]  Chris I. Baker,et al.  Scene selectivity and retinotopy in medial parietal cortex , 2016 .

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

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

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

[45]  F. Yates The Art of Memory , 1969 .

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

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

[68]  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.

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

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

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

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

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

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

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

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

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

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

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

[80]  Fei-Fei Li,et al.  Differential connectivity within the Parahippocampal Place Area , 2013, NeuroImage.

[81]  Giulio Tononi,et al.  Reversal of cortical information flow during visual imagery as compared to visual perception , 2014, NeuroImage.

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

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

[84]  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.

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

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

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

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

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

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

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

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

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

[94]  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.

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

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

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

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

[99]  K. Grill-Spector,et al.  Differential development of high-level visual cortex correlates with category-specific recognition memory , 2007, Nature Neuroscience.

[100]  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.

[101]  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.

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

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

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

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

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