Different roles of the parahippocampal place area (PPA) and retrosplenial cortex (RSC) in panoramic scene perception

AbstractThe aging brain is characterized by neural dedifferentiation – an apparent decrease in the functional selectivity of category-selective cortical regions. Age-related reductions in neural differentiation have been proposed to play a causal role in cognitive aging. Recent findings suggest, however, that age-related dedifferentiation is not equally evident for all stimulus categories and, additionally, that the relationship between neural differentiation and cognitive performance is not moderated by age. In light of these findings, in the present experiment younger and older human adults (males and females) underwent fMRI as they studied words paired with images of scenes or faces prior to a subsequent memory task. Neural selectivity was measured in two scene-selective (parahippocampal place area and retrosplenial cortex) and two face-selective (fusiform and occipital face areas) regions of interest using both a univariate differentiation index and multivoxel pattern similarity analysis. Both methods provided highly convergent results which revealed evidence of age-related reductions in neural dedifferentiation in scene-selective but not face-selective cortical regions. Additionally, neural differentiation in the parahippocampal place area demonstrated a positive, age-invariant relationship with subsequent source memory performance (recall of the image category paired with each recognized test word). These findings extend prior findings suggesting that age-related neural dedifferentiation is not a ubiquitous phenomenon, and that the specificity of neural responses to scenes is predictive subsequent memory performance independently of age.Significance StatementIncreasing age is associated with reduced neural specificity in cortical regions that are selectively responsive to a given perceptual stimulus category (age-related neural dedifferentiation), a phenomenon which has been proposed to contribute to cognitive aging. Recent findings reveal that age-related neural dedifferentiation is not present for all types of visual stimulus categories, and the factors which determine when the phenomenon arises remain unclear. Here, we demonstrate that scene- but not face-selective cortical regions exhibit age-related neural dedifferentiation during an attentionally-demanding task. Additionally, we report that higher neural selectivity in the scene-selective ‘parahippocampal place area’ is associated with better memory performance after controlling for variance associated with age group, adding to evidence that neural differentiation impacts cognition across the adult lifespan.

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Behavioral and Neuroimaging Evidence for a Contribution of Color and Texture Information to Scene Classification in a Patient with Visual Form Agnosia

Journal of Cognitive Neuroscience ◽

10.1162/0898929041502715 ◽

2004 ◽

Vol 16 (6) ◽

pp. 955-965 ◽

Cited By ~ 51

Author(s):

Jennifer K. E. Steeves ◽

G. Keith Humphrey ◽

Jody C. Culham ◽

Ravi S. Menon ◽

A. David Milner ◽

...

Keyword(s):

Scene Perception ◽

Object Perception ◽

Visual Texture ◽

Visual Form ◽

Black And White ◽

Form Vision ◽

Common Notion ◽

Vision Deficits ◽

Behavioral Evidence ◽

Parahippocampal Place Area

A common notion is that object perception is a necessary precursor to scene perception. Behavioral evidence suggests, however, that scene perception can operate independently of object perception. Further, neuroimaging has revealed a specialized human cortical area for viewing scenes that is anatomically distinct from areas activated by viewing objects. Here we show that an individual with visual form agnosia, D.F., who has a profound deficit in object recognition but spared color and visual texture perception, could still classify scenes and that she was fastest when the scenes were presented in the appropriate color. When scenes were presented as black-and-white images, she made a large number of errors in classification. Functional magnetic resonance imaging revealed selective activation in the parahippocampal place area (PPA) when D.F. viewed scenes. Unlike control observers, D.F. demonstrated higher activation in the PPA for scenes presented in the appropriate color than for black-and-white versions. The results demonstrate that an individual with profound form vision deficits can still use visual texture and color to classify scenes—and that this intact ability is reflected in differential activation of the PPA with colored versions of scenes.

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Neural Correlates of Fixated Low- and High-level Scene Properties during Active Scene Viewing

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_01599 ◽

2020 ◽

Vol 32 (10) ◽

pp. 2013-2023

Author(s):

John M. Henderson ◽

Jessica E. Goold ◽

Wonil Choi ◽

Taylor R. Hayes

Keyword(s):

Real World ◽

Visual Analysis ◽

Scene Perception ◽

Active Vision ◽

Semantic Content ◽

Retrosplenial Cortex ◽

Edge Density ◽

Visual Stream ◽

Lateral Occipital Complex ◽

High Level

During real-world scene perception, viewers actively direct their attention through a scene in a controlled sequence of eye fixations. During each fixation, local scene properties are attended, analyzed, and interpreted. What is the relationship between fixated scene properties and neural activity in the visual cortex? Participants inspected photographs of real-world scenes in an MRI scanner while their eye movements were recorded. Fixation-related fMRI was used to measure activation as a function of lower- and higher-level scene properties at fixation, operationalized as edge density and meaning maps, respectively. We found that edge density at fixation was most associated with activation in early visual areas, whereas semantic content at fixation was most associated with activation along the ventral visual stream including core object and scene-selective areas (lateral occipital complex, parahippocampal place area, occipital place area, and retrosplenial cortex). The observed activation from semantic content was not accounted for by differences in edge density. The results are consistent with active vision models in which fixation gates detailed visual analysis for fixated scene regions, and this gating influences both lower and higher levels of scene analysis.

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Refreshing and Integrating Visual Scenes in Scene-selective Cortex

Journal of Cognitive Neuroscience ◽

10.1162/jocn.2009.21406 ◽

2010 ◽

Vol 22 (12) ◽

pp. 2813-2822 ◽

Cited By ~ 11

Author(s):

Soojin Park ◽

Marvin M. Chun ◽

Marcia K. Johnson

Keyword(s):

Visual Information ◽

Visual Experience ◽

Specific Activity ◽

Retrosplenial Cortex ◽

Current View ◽

Multiple Views ◽

Visual Areas ◽

Visual Scenes ◽

The Mind ◽

Parahippocampal Place Area

Constructing a rich and coherent visual experience involves maintaining visual information that is not perceptually available in the current view. Recent studies suggest that briefly thinking about a stimulus (refreshing) can modulate activity in category-specific visual areas. Here, we tested the nature of such perceptually refreshed representations in the parahippocampal place area (PPA) and retrosplenial cortex (RSC) using fMRI. We asked whether a refreshed representation is specific to a restricted view of a scene, or more view-invariant. Participants saw a panoramic scene and were asked to think back to (refresh) a part of the scene after it disappeared. In some trials, the refresh cue appeared twice on the same side (e.g., refresh left–refresh left), and other trials, the refresh cue appeared on different sides (e.g., refresh left–refresh right). A control condition presented halves of the scene twice on same sides (e.g., perceive left–perceive left) or different sides (e.g., perceive left–perceive right). When scenes were physically repeated, both the PPA and RSC showed greater activation for the different-side repetition than the same-side repetition, suggesting view-specific representations. When participants refreshed scenes, the PPA showed view-specific activity just as in the physical repeat conditions, whereas RSC showed an equal amount of activation for different- and same-side conditions. This finding suggests that in RSC, refreshed representations were not restricted to a specific view of a scene, but extended beyond the target half into the entire scene. Thus, RSC activity associated with refreshing may provide a mechanism for integrating multiple views in the mind.

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Transcranial Magnetic Stimulation to the Transverse Occipital Sulcus Affects Scene but Not Object Processing

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_00372 ◽

2013 ◽

Vol 25 (6) ◽

pp. 961-968 ◽

Cited By ~ 32

Author(s):

Rachel E. Ganaden ◽

Caitlin R. Mullin ◽

Jennifer K. E. Steeves

Keyword(s):

Scene Perception ◽

Occipital Cortex ◽

Control Site ◽

Image Features ◽

Retrosplenial Cortex ◽

Scene Recognition ◽

Scene Categorization ◽

Object Processing ◽

Inhibitory Mechanisms ◽

Scene Processing

Traditionally, it has been theorized that the human visual system identifies and classifies scenes in an object-centered approach, such that scene recognition can only occur once key objects within a scene are identified. Recent research points toward an alternative approach, suggesting that the global image features of a scene are sufficient for the recognition and categorization of a scene. We have previously shown that disrupting object processing with repetitive TMS to object-selective cortex enhances scene processing possibly through a release of inhibitory mechanisms between object and scene pathways [Mullin, C. R., & Steeves, J. K. E. TMS to the lateral occipital cortex disrupts object processing but facilitates scene processing. Journal of Cognitive Neuroscience, 23, 4174–4184, 2011]. Here we show the effects of TMS to the transverse occipital sulcus (TOS), an area implicated in scene perception, on scene and object processing. TMS was delivered to the TOS or the vertex (control site) while participants performed an object and scene natural/nonnatural categorization task. Transiently interrupting the TOS resulted in significantly lower accuracies for scene categorization compared with control conditions. This demonstrates a causal role of the TOS in scene processing and indicates its importance, in addition to the parahippocampal place area and retrosplenial cortex, in the scene processing network. Unlike TMS to object-selective cortex, which facilitates scene categorization, disrupting scene processing through stimulation of the TOS did not affect object categorization. Further analysis revealed a higher proportion of errors for nonnatural scenes that led us to speculate that the TOS may be involved in processing the higher spatial frequency content of a scene. This supports a nonhierarchical model of scene recognition.

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Scene Perception in the Human Brain

Annual Review of Vision Science ◽

10.1146/annurev-vision-091718-014809 ◽

2019 ◽

Vol 5 (1) ◽

pp. 373-397 ◽

Cited By ~ 30

Author(s):

Russell A. Epstein ◽

Chris I. Baker

Keyword(s):

Information Processing ◽

Computational Models ◽

Scene Perception ◽

Visual Features ◽

Important Goal ◽

Neural Basis ◽

Brain Areas ◽

Vision Science ◽

Cortical Regions ◽

Parahippocampal Place Area

Humans are remarkably adept at perceiving and understanding complex real-world scenes. Uncovering the neural basis of this ability is an important goal of vision science. Neuroimaging studies have identified three cortical regions that respond selectively to scenes: parahippocampal place area, retrosplenial complex/medial place area, and occipital place area. Here, we review what is known about the visual and functional properties of these brain areas. Scene-selective regions exhibit retinotopic properties and sensitivity to low-level visual features that are characteristic of scenes. They also mediate higher-level representations of layout, objects, and surface properties that allow individual scenes to be recognized and their spatial structure ascertained. Challenges for the future include developing computational models of information processing in scene regions, investigating how these regions support scene perception under ecologically realistic conditions, and understanding how they operate in the context of larger brain networks.

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Unraveling Representations in Scene-selective Brain Regions Using Scene-Parsing Deep Neural Networks

Journal of Cognitive Neuroscience ◽

10.1162/jocn_a_01624 ◽

2020 ◽

pp. 1-12 ◽

Cited By ~ 1

Author(s):

Kshitij Dwivedi ◽

Radoslaw Martin Cichy ◽

Gemma Roig

Keyword(s):

Scene Perception ◽

Research Question ◽

Brain Regions ◽

Computational Approach ◽

Differential Sensitivity ◽

Neural Basis ◽

Cortical Regions ◽

Differential Contribution ◽

Parahippocampal Place Area ◽

Variance Explained

Visual scene perception is mediated by a set of cortical regions that respond preferentially to images of scenes, including the occipital place area (OPA) and parahippocampal place area (PPA). However, the differential contribution of OPA and PPA to scene perception remains an open research question. In this study, we take a deep neural network (DNN)-based computational approach to investigate the differences in OPA and PPA function. In a first step, we search for a computational model that predicts fMRI responses to scenes in OPA and PPA well. We find that DNNs trained to predict scene components (e.g., wall, ceiling, floor) explain higher variance uniquely in OPA and PPA than a DNN trained to predict scene category (e.g., bathroom, kitchen, office). This result is robust across several DNN architectures. On this basis, we then determine whether particular scene components predicted by DNNs differentially account for unique variance in OPA and PPA. We find that variance in OPA responses uniquely explained by the navigation-related floor component is higher compared to the variance explained by the wall and ceiling components. In contrast, PPA responses are better explained by the combination of wall and floor, that is, scene components that together contain the structure and texture of the scene. This differential sensitivity to scene components suggests differential functions of OPA and PPA in scene processing. Moreover, our results further highlight the potential of the proposed computational approach as a general tool in the investigation of the neural basis of human scene perception.

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Unravelling Representations in Scene-selective Brain Regions Using Scene Parsing Deep Neural Networks

10.1101/2020.03.10.985309 ◽

2020 ◽

Author(s):

Kshitij Dwivedi ◽

Radoslaw Martin Cichy ◽

Gemma Roig

Keyword(s):

Scene Perception ◽

Research Question ◽

Brain Regions ◽

Computational Approach ◽

Differential Sensitivity ◽

Neural Basis ◽

Cortical Regions ◽

Differential Contribution ◽

Parahippocampal Place Area ◽

Variance Explained

Visual scene perception is mediated by a set of cortical regions that respond preferentially to images of scenes, including the occipital place area (OPA) and parahippocampal place area (PPA). However, the differential contribution of OPA and PPA to scene perception remains an open research question. In this study, we take a deep neural network (DNN)-based computational approach to investigate the differences in OPA and PPA function. In a first step we search for a computational model that predicts fMRI responses to scenes in OPA and PPA well. We find that DNNs trained to predict scene components (e.g., wall, ceiling, floor) explain higher variance uniquely in OPA and PPA than a DNN trained to predict scene category (e.g., bathroom, kitchen, office). This result is robust across several DNN architectures. On this basis, we then determine whether particular scene components predicted by DNNs differentially account for unique variance in OPA and PPA. We find that variance in OPA responses uniquely explained by the navigation-related floor component is higher compared to the variance explained by the wall and ceiling components. In contrast, PPA responses are better explained by the combination of wall and floor, that is scene components that together contain the structure and texture of the scene. This differential sensitivity to scene components suggests differential functions of OPA and PPA in scene processing. Moreover, our results further highlight the potential of the proposed computational approach as a general tool in the investigation of the neural basis of human scene perception.

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Visual Scene Processing in Familiar and Unfamiliar Environments

Journal of Neurophysiology ◽

10.1152/jn.00003.2007 ◽

2007 ◽

Vol 97 (5) ◽

pp. 3670-3683 ◽

Cited By ~ 86

Author(s):

Russell A. Epstein ◽

J. Stephen Higgins ◽

Karen Jablonski ◽

Alana M. Feiler

Keyword(s):

Spatial Information ◽

Scene Perception ◽

Retrosplenial Cortex ◽

Visual Scene ◽

Neural Systems ◽

Repetition Suppression ◽

Neural Representations ◽

Parahippocampal Cortex ◽

Scene Processing ◽

Viewpoint Invariance

Humans and animals use information obtained from the local visual scene to orient themselves in the wider world. Although neural systems involved in scene perception have been identified, the extent to which processing in these systems is affected by previous experience is unclear. We addressed this issue by scanning subjects with functional magnetic resonance imaging (fMRI) while they viewed photographs of familiar and unfamiliar locations. Scene-selective regions in parahippocampal cortex (the parahippocampal place area, or PPA), retrosplenial cortex (RSC), and the transverse occipital sulcus (TOS) responded more strongly to images of familiar locations than to images of unfamiliar locations with the strongest effects (>50% increase) in RSC. Examination of fMRI repetition suppression (RS) effects indicated that images of familiar and unfamiliar locations were processed with the same degree of viewpoint specificity; however, increased viewpoint invariance was observed as individual scenes became more familiar over the course of a scan session. Surprisingly, these within-scan-session viewpoint-invariant RS effects were only observed when scenes were repeated across different trials but not when scenes were repeated within a trial, suggesting that within- and between-trial RS effects may index different aspects of visual scene processing. The sensitivity to environmental familiarity observed in the PPA, RSC, and TOS supports earlier claims that these regions mediate the extraction of navigationally relevant spatial information from visual scenes. As locations become familiar, the neural representations of these locations become enriched, but the viewpoint invariance of these representations does not change.

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