Literature DB >> 29858483

Modality-Independent Coding of Scene Categories in Prefrontal Cortex.

Yaelan Jung1, Bart Larsen2, Dirk B Walther3.   

Abstract

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.
Copyright © 2018 the authors 0270-6474/18/385969-13$15.00/0.

Entities:  

Keywords:  PFC; cross-modal; fMRI; modality-independent representation; multivoxel pattern analysis; scene perception

Mesh:

Year:  2018        PMID: 29858483      PMCID: PMC6595974          DOI: 10.1523/JNEUROSCI.0272-18.2018

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  49 in total

1.  Categorical representation of visual stimuli in the primate prefrontal cortex.

Authors:  D J Freedman; M Riesenhuber; T Poggio; E K Miller
Journal:  Science       Date:  2001-01-12       Impact factor: 47.728

2.  Spatial pattern of BOLD fMRI activation reveals cross-modal information in auditory cortex.

Authors:  P-J Hsieh; J T Colas; N Kanwisher
Journal:  J Neurophysiol       Date:  2012-04-18       Impact factor: 2.714

3.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages.

Authors:  R W Cox
Journal:  Comput Biomed Res       Date:  1996-06

4.  A cortical representation of the local visual environment.

Authors:  R Epstein; N Kanwisher
Journal:  Nature       Date:  1998-04-09       Impact factor: 49.962

5.  Detection of audio-visual integration sites in humans by application of electrophysiological criteria to the BOLD effect.

Authors:  G A Calvert; P C Hansen; S D Iversen; M J Brammer
Journal:  Neuroimage       Date:  2001-08       Impact factor: 6.556

Review 6.  Machine learning classifiers and fMRI: a tutorial overview.

Authors:  Francisco Pereira; Tom Mitchell; Matthew Botvinick
Journal:  Neuroimage       Date:  2008-11-21       Impact factor: 6.556

7.  The occipital place area is causally and selectively involved in scene perception.

Authors:  Daniel D Dilks; Joshua B Julian; Alexander M Paunov; Nancy Kanwisher
Journal:  J Neurosci       Date:  2013-01-23       Impact factor: 6.167

8.  Contour junctions underlie neural representations of scene categories in high-level human visual cortex.

Authors:  Heeyoung Choo; Dirk B Walther
Journal:  Neuroimage       Date:  2016-04-23       Impact factor: 6.556

9.  Mechanisms of directed attention in the human extrastriate cortex as revealed by functional MRI.

Authors:  S Kastner; P De Weerd; R Desimone; L G Ungerleider
Journal:  Science       Date:  1998-10-02       Impact factor: 47.728

Review 10.  Multisensory interplay reveals crossmodal influences on 'sensory-specific' brain regions, neural responses, and judgments.

Authors:  Jon Driver; Toemme Noesselt
Journal:  Neuron       Date:  2008-01-10       Impact factor: 17.173

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  9 in total

Review 1.  Scene Perception in the Human Brain.

Authors:  Russell A Epstein; Chris I Baker
Journal:  Annu Rev Vis Sci       Date:  2019-06-21       Impact factor: 6.422

2.  Monkey Prefrontal Single-Unit Activity Reflecting Category-Based Logical Thinking Process and Its Neural Network Model.

Authors:  Takayuki Hosokawa; Muyuan Xu; Yuichi Katori; Munekazu Yamada; Kazuyuki Aihara; Ken-Ichiro Tsutsui
Journal:  J Neurosci       Date:  2022-07-08       Impact factor: 6.709

3.  Cortical networks of dynamic scene category representation in the human brain.

Authors:  Emin Çelik; Umit Keles; İbrahim Kiremitçi; Jack L Gallant; Tolga Çukur
Journal:  Cortex       Date:  2021-07-24       Impact factor: 4.644

4.  Resolving the time course of visual and auditory object categorization.

Authors:  Polina Iamshchinina; Agnessa Karapetian; Daniel Kaiser; Radoslaw M Cichy
Journal:  J Neurophysiol       Date:  2022-05-18       Impact factor: 2.974

5.  Viewing images of foods evokes taste quality-specific activity in gustatory insular cortex.

Authors:  Jason A Avery; Alexander G Liu; John E Ingeholm; Stephen J Gotts; Alex Martin
Journal:  Proc Natl Acad Sci U S A       Date:  2021-01-12       Impact factor: 12.779

6.  Differential Rapid Plasticity in Auditory and Visual Responses in the Primarily Multisensory Orbitofrontal Cortex.

Authors:  Sudha Sharma; Sharba Bandyopadhyay
Journal:  eNeuro       Date:  2020-06-12

7.  Neural Representations in the Prefrontal Cortex Are Task Dependent for Scene Attributes But Not for Scene Categories.

Authors:  Yaelan Jung; Dirk B Walther
Journal:  J Neurosci       Date:  2021-06-08       Impact factor: 6.167

8.  Supramodal Mechanisms of the Cognitive Control Network in Uncertainty Processing.

Authors:  Tingting Wu; Alfredo Spagna; Chao Chen; Kurt P Schulz; Patrick R Hof; Jin Fan
Journal:  Cereb Cortex       Date:  2020-11-03       Impact factor: 5.357

Review 9.  Visual Influences on Auditory Behavioral, Neural, and Perceptual Processes: A Review.

Authors:  Collins Opoku-Baah; Adriana M Schoenhaut; Sarah G Vassall; David A Tovar; Ramnarayan Ramachandran; Mark T Wallace
Journal:  J Assoc Res Otolaryngol       Date:  2021-05-20
  9 in total

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