Literature DB >> 33262244

Causal Evidence for a Double Dissociation between Object- and Scene-Selective Regions of Visual Cortex: A Preregistered TMS Replication Study.

Miles Wischnewski1,2, Marius V Peelen3.   

Abstract

Natural scenes are characterized by individual objects as well as by global scene properties such as spatial layout. Functional neuroimaging research has shown that this distinction between object and scene processing is one of the main organizing principles of human high-level visual cortex. For example, object-selective regions, including the lateral occipital complex (LOC), were shown to represent object content (but not scene layout), while scene-selective regions, including the occipital place area (OPA), were shown to represent scene layout (but not object content). Causal evidence for a double dissociation between LOC and OPA in representing objects and scenes is currently limited, however. One TMS experiment, conducted in a relatively small sample (N = 13), reported an interaction between LOC and OPA stimulation and object and scene recognition performance (Dilks et al., 2013). Here, we present a high-powered preregistered replication of this study (N = 72, including male and female human participants), using group-average fMRI coordinates to target LOC and OPA. Results revealed unambiguous evidence for a double dissociation between LOC and OPA: relative to vertex stimulation, TMS over LOC selectively impaired the recognition of objects, while TMS over OPA selectively impaired the recognition of scenes. Furthermore, we found that these effects were stable over time and consistent across individual objects and scenes. These results show that LOC and OPA can be reliably and selectively targeted with TMS, even when defined based on group-average fMRI coordinates. More generally, they support the distinction between object and scene processing as an organizing principle of human high-level visual cortex.SIGNIFICANCE STATEMENT Our daily-life environments are characterized both by individual objects and by global scene properties. The distinction between object and scene processing features prominently in visual cognitive neuroscience, with fMRI studies showing that this distinction is one of the main organizing principles of human high-level visual cortex. However, causal evidence for the selective involvement of object- and scene-selective regions in processing their preferred category is less conclusive. Here, testing a large sample (N = 72) using an established paradigm and a preregistered protocol, we found that TMS over object-selective cortex (lateral occipital complex) selectively impaired object recognition, while TMS over scene-selective cortex (occipital place area) selectively impaired scene recognition. These results provide strong causal evidence for the distinction between object and scene processing in human visual cortex.
Copyright © 2021 the authors.

Entities:  

Keywords:  lateral occipital cortex; object recognition; occipital place area; scene recognition; transcranial magnetic stimulation

Mesh:

Year:  2020        PMID: 33262244      PMCID: PMC7842759          DOI: 10.1523/JNEUROSCI.2162-20.2020

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


  32 in total

1.  Center-periphery organization of human object areas.

Authors:  I Levy; U Hasson; G Avidan; T Hendler; R Malach
Journal:  Nat Neurosci       Date:  2001-05       Impact factor: 24.884

Review 2.  The neural basis of object perception.

Authors:  Kalanit Grill-Spector
Journal:  Curr Opin Neurobiol       Date:  2003-04       Impact factor: 6.627

3.  Disentangling scene content from spatial boundary: complementary roles for the parahippocampal place area and lateral occipital complex in representing real-world scenes.

Authors:  Soojin Park; Timothy F Brady; Michelle R Greene; Aude Oliva
Journal:  J Neurosci       Date:  2011-01-26       Impact factor: 6.167

Review 4.  Power failure: why small sample size undermines the reliability of neuroscience.

Authors:  Katherine S Button; John P A Ioannidis; Claire Mokrysz; Brian A Nosek; Jonathan Flint; Emma S J Robinson; Marcus R Munafò
Journal:  Nat Rev Neurosci       Date:  2013-04-10       Impact factor: 34.870

5.  Thinking outside the box: rectilinear shapes selectively activate scene-selective cortex.

Authors:  Shahin Nasr; Cesar E Echavarria; Roger B H Tootell
Journal:  J Neurosci       Date:  2014-05-14       Impact factor: 6.167

6.  Attention to form or surface properties modulates different regions of human occipitotemporal cortex.

Authors:  Jonathan S Cant; Melvyn A Goodale
Journal:  Cereb Cortex       Date:  2006-04-28       Impact factor: 5.357

7.  Interaction between Scene and Object Processing Revealed by Human fMRI and MEG Decoding.

Authors:  Talia Brandman; Marius V Peelen
Journal:  J Neurosci       Date:  2017-07-07       Impact factor: 6.167

8.  Real-world scene representations in high-level visual cortex: it's the spaces more than the places.

Authors:  Dwight J Kravitz; Cynthia S Peng; Chris I Baker
Journal:  J Neurosci       Date:  2011-05-18       Impact factor: 6.167

9.  The Occipital Place Area Is Causally Involved in Representing Environmental Boundaries during Navigation.

Authors:  Joshua B Julian; Jack Ryan; Roy H Hamilton; Russell A Epstein
Journal:  Curr Biol       Date:  2016-04-25       Impact factor: 10.834

10.  Dynamics of scene representations in the human brain revealed by magnetoencephalography and deep neural networks.

Authors:  Radoslaw Martin Cichy; Aditya Khosla; Dimitrios Pantazis; Aude Oliva
Journal:  Neuroimage       Date:  2016-04-01       Impact factor: 6.556

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