Dataset Information

Fourier power, subjective distance, and object categories all provide plausible models of BOLD responses in scene-selective visual areas.

ABSTRACT: Perception of natural visual scenes activates several functional areas in the human brain, including the Parahippocampal Place Area (PPA), Retrosplenial Complex (RSC), and the Occipital Place Area (OPA). It is currently unclear what specific scene-related features are represented in these areas. Previous studies have suggested that PPA, RSC, and/or OPA might represent at least three qualitatively different classes of features: (1) 2D features related to Fourier power; (2) 3D spatial features such as the distance to objects in a scene; or (3) abstract features such as the categories of objects in a scene. To determine which of these hypotheses best describes the visual representation in scene-selective areas, we applied voxel-wise modeling (VM) to BOLD fMRI responses elicited by a set of 1386 images of natural scenes. VM provides an efficient method for testing competing hypotheses by comparing predictions of brain activity based on encoding models that instantiate each hypothesis. Here we evaluated three different encoding models that instantiate each of the three hypotheses listed above. We used linear regression to fit each encoding model to the fMRI data recorded from each voxel, and we evaluated each fit model by estimating the amount of variance it predicted in a withheld portion of the data set. We found that voxel-wise models based on Fourier power or the subjective distance to objects in each scene predicted much of the variance predicted by a model based on object categories. Furthermore, the response variance explained by these three models is largely shared, and the individual models explain little unique variance in responses. Based on an evaluation of previous studies and the data we present here, we conclude that there is currently no good basis to favor any one of the three alternative hypotheses about visual representation in scene-selective areas. We offer suggestions for further studies that may help resolve this issue.

SUBMITTER: Lescroart MD

PROVIDER: S-EPMC4633487 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Publications

Fourier power, subjective distance, and object categories all provide plausible models of BOLD responses in scene-selective visual areas.

Lescroart Mark D MD Stansbury Dustin E DE Gallant Jack L JL

Frontiers in computational neuroscience 20151105

Perception of natural visual scenes activates several functional areas in the human brain, including the Parahippocampal Place Area (PPA), Retrosplenial Complex (RSC), and the Occipital Place Area (OPA). It is currently unclear what specific scene-related features are represented in these areas. Previous studies have suggested that PPA, RSC, and/or OPA might represent at least three qualitatively different classes of features: (1) 2D features related to Fourier power; (2) 3D spatial features suc ...[more]

PMID: 26594164

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Project description:Natural environments convey information through multiple sensory modalities, all of which contribute to people's percepts. Although it has been shown that visual or auditory content of scene categories can be decoded from brain activity, it remains unclear how humans represent scene information beyond a specific sensory modality domain. To address this question, we investigated how categories of scene images and sounds are represented in several brain regions. A group of healthy human subjects (both sexes) participated in the present study, where their brain activity was measured with fMRI while viewing images or listening to sounds of different real-world environments. We found that both visual and auditory scene categories can be decoded not only from modality-specific areas, but also from several brain regions in the temporal, parietal, and prefrontal cortex (PFC). Intriguingly, only in the PFC, but not in any other regions, categories of scene images and sounds appear to be represented in similar activation patterns, suggesting that scene representations in PFC are modality-independent. Furthermore, the error patterns of neural decoders indicate that category-specific neural activity patterns in the middle and superior frontal gyri are tightly linked to categorization behavior. Our findings demonstrate that complex scene information is represented at an abstract level in the PFC, regardless of the sensory modality of the stimulus.SIGNIFICANCE STATEMENT Our experience in daily life includes multiple sensory inputs, such as images, sounds, or scents from the surroundings, which all contribute to our understanding of the environment. Here, for the first time, we investigated where and how in the brain information about the natural environment from multiple senses is merged to form modality-independent representations of scene categories. We show direct decoding of scene categories across sensory modalities from patterns of neural activity in the prefrontal cortex (PFC). We also conclusively tie these neural representations to human categorization behavior by comparing patterns of errors between a neural decoder and behavior. Our findings suggest that PFC is a central hub for integrating sensory information and computing modality-independent representations of scene categories.

Dataset Information

Fourier power, subjective distance, and object categories all provide plausible models of BOLD responses in scene-selective visual areas.

Publications

Fourier power, subjective distance, and object categories all provide plausible models of BOLD responses in scene-selective visual areas.

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