Dataset Information

Modality-independent coding of spatial layout in the human brain.

ABSTRACT: In many nonhuman species, neural computations of navigational information such as position and orientation are not tied to a specific sensory modality [1, 2]. Rather, spatial signals are integrated from multiple input sources, likely leading to abstract representations of space. In contrast, the potential for abstract spatial representations in humans is not known, because most neuroscientific experiments on human navigation have focused exclusively on visual cues. Here, we tested the modality independence hypothesis with two functional magnetic resonance imaging (fMRI) experiments that characterized computations in regions implicated in processing spatial layout [3]. According to the hypothesis, such regions should be recruited for spatial computation of 3D geometric configuration, independent of a specific sensory modality. In support of this view, sighted participants showed strong activation of the parahippocampal place area (PPA) and the retrosplenial cortex (RSC) for visual and haptic exploration of information-matched scenes but not objects. Functional connectivity analyses suggested that these effects were not related to visual recoding, which was further supported by a similar preference for haptic scenes found with blind participants. Taken together, these findings establish the PPA/RSC network as critical in modality-independent spatial computations and provide important evidence for a theory of high-level abstract spatial information processing in the human brain.

SUBMITTER: Wolbers T

PROVIDER: S-EPMC3119034 | biostudies-literature | 2011 Jun

REPOSITORIES: biostudies-literature

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Modality-independent coding of spatial layout in the human brain.

Wolbers Thomas T Klatzky Roberta L RL Loomis Jack M JM Wutte Magdalena G MG Giudice Nicholas A NA

Current biology : CB 20110527 11

In many nonhuman species, neural computations of navigational information such as position and orientation are not tied to a specific sensory modality [1, 2]. Rather, spatial signals are integrated from multiple input sources, likely leading to abstract representations of space. In contrast, the potential for abstract spatial representations in humans is not known, because most neuroscientific experiments on human navigation have focused exclusively on visual cues. Here, we tested the modality i ...[more]

PMID: 21620708

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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

Modality-independent coding of spatial layout in the human brain.

Publications

Modality-independent coding of spatial layout in the human brain.

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