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Scene-selectivity in CA1/subicular complex: Multivoxel pattern analysis at 7T

Marie-Lucie Read Orcid Logo, Samuel C. Berry, Kim S. Graham, Natalie L. Voets, Jiaxiang Zhang Orcid Logo, John P. Aggleton, Andrew D. Lawrence, Carl J. Hodgetts

Neuropsychologia, Volume: 194, Start page: 108783

Swansea University Author: Jiaxiang Zhang Orcid Logo

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Abstract

Prior univariate functional magnetic resonance imaging (fMRI) studies in humans suggest that the anteromedial subicular complex of the hippocampus is a hub for scene-based cognition. However, it is possible that univariate approaches were not sufficiently sensitive to detect scene-related activity i...

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Published in: Neuropsychologia
ISSN: 0028-3932
Published: Elsevier BV 2024
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URI: https://cronfa.swan.ac.uk/Record/cronfa65434
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However, it is possible that univariate approaches were not sufficiently sensitive to detect scene-related activity in other subfields that have been implicated in spatial processing (e.g., CA1). Further, as connectivity-based functional gradients in the hippocampus do not respect classical subfield boundary definitions, category selectivity may be distributed across anatomical subfields. Region-of-interest approaches, therefore, may limit our ability to observe category selectivity across discrete subfield boundaries. To address these issues, we applied searchlight multivariate pattern analysis to 7T fMRI data of healthy adults who undertook a simultaneous visual odd-one-out discrimination task for scene and non-scene (including face) visual stimuli, hypothesising that scene classification would be possible in multiple hippocampal regions within, but not constrained to, anteromedial subicular complex and CA1. Indeed, we found that the scene-selective searchlight map overlapped not only with anteromedial subicular complex (distal subiculum, pre/para subiculum), but also inferior CA1, alongside posteromedial (including retrosplenial) and parahippocampal cortices. Probabilistic overlap maps revealed gradients of scene category selectivity, with the strongest overlap located in the medial hippocampus, converging with searchlight findings. This was contrasted with gradients of face category selectivity, which had stronger overlap in more lateral hippocampus, supporting ideas of parallel processing streams for these two categories. Our work helps to map the scene, in contrast to, face processing networks within, and connected to, the human hippocampus.</abstract><type>Journal Article</type><journal>Neuropsychologia</journal><volume>194</volume><journalNumber/><paginationStart>108783</paginationStart><paginationEnd/><publisher>Elsevier BV</publisher><placeOfPublication/><isbnPrint/><isbnElectronic/><issnPrint>0028-3932</issnPrint><issnElectronic/><keywords>Visual perception; Memory; Medial temporal lobe; Hippocampus; Scene processing; MVPA</keywords><publishedDay>15</publishedDay><publishedMonth>2</publishedMonth><publishedYear>2024</publishedYear><publishedDate>2024-02-15</publishedDate><doi>10.1016/j.neuropsychologia.2023.108783</doi><url/><notes>Data availability:Due to ethical concerns, supporting data cannot be made openly available. 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spelling v2 65434 2024-01-10 Scene-selectivity in CA1/subicular complex: Multivoxel pattern analysis at 7T 555e06e0ed9a87608f2d035b3bde3a87 0000-0002-4758-0394 Jiaxiang Zhang Jiaxiang Zhang true false 2024-01-10 SCS Prior univariate functional magnetic resonance imaging (fMRI) studies in humans suggest that the anteromedial subicular complex of the hippocampus is a hub for scene-based cognition. However, it is possible that univariate approaches were not sufficiently sensitive to detect scene-related activity in other subfields that have been implicated in spatial processing (e.g., CA1). Further, as connectivity-based functional gradients in the hippocampus do not respect classical subfield boundary definitions, category selectivity may be distributed across anatomical subfields. Region-of-interest approaches, therefore, may limit our ability to observe category selectivity across discrete subfield boundaries. To address these issues, we applied searchlight multivariate pattern analysis to 7T fMRI data of healthy adults who undertook a simultaneous visual odd-one-out discrimination task for scene and non-scene (including face) visual stimuli, hypothesising that scene classification would be possible in multiple hippocampal regions within, but not constrained to, anteromedial subicular complex and CA1. Indeed, we found that the scene-selective searchlight map overlapped not only with anteromedial subicular complex (distal subiculum, pre/para subiculum), but also inferior CA1, alongside posteromedial (including retrosplenial) and parahippocampal cortices. Probabilistic overlap maps revealed gradients of scene category selectivity, with the strongest overlap located in the medial hippocampus, converging with searchlight findings. This was contrasted with gradients of face category selectivity, which had stronger overlap in more lateral hippocampus, supporting ideas of parallel processing streams for these two categories. Our work helps to map the scene, in contrast to, face processing networks within, and connected to, the human hippocampus. Journal Article Neuropsychologia 194 108783 Elsevier BV 0028-3932 Visual perception; Memory; Medial temporal lobe; Hippocampus; Scene processing; MVPA 15 2 2024 2024-02-15 10.1016/j.neuropsychologia.2023.108783 Data availability:Due to ethical concerns, supporting data cannot be made openly available. Further information about the data and conditions for access are available at https://osf.io/4vgk9/ DOI: 10.17605/OSF.IO/4VGK9 COLLEGE NANME Computer Science COLLEGE CODE SCS Swansea University Another institution paid the OA fee This work was supported by the Biotechnology and Biological Sciences Research Council (BBSRC) [BB/V010549/1; BB/V008242/1; to C.J.H., A.D.L.], the Medical Research Council (G1002149; to K.S.G., C.J.H.), and a Wellcome Trust Strategic Support Fund fellowship (C.J.H.). We would like to thank attendees of British Neuroscience Association Festival of Neuroscience (2023) for their feedback on this work. 2024-03-21T11:42:51.7311570 2024-01-10T15:06:14.0190110 Faculty of Science and Engineering School of Mathematics and Computer Science - Computer Science Marie-Lucie Read 0000-0003-4809-5937 1 Samuel C. Berry 2 Kim S. Graham 3 Natalie L. Voets 4 Jiaxiang Zhang 0000-0002-4758-0394 5 John P. Aggleton 6 Andrew D. Lawrence 7 Carl J. Hodgetts 8 65434__29779__f93bf0f81d184bc9893fbe0b9ce54799.pdf 65434_VoR.pdf 2024-03-21T11:41:23.6985234 Output 9201928 application/pdf Version of Record true ©2024 The Authors. This is an open access article under the CC BY license. true eng http://creativecommons.org/licenses/by/4.0/
title Scene-selectivity in CA1/subicular complex: Multivoxel pattern analysis at 7T
spellingShingle Scene-selectivity in CA1/subicular complex: Multivoxel pattern analysis at 7T
Jiaxiang Zhang
title_short Scene-selectivity in CA1/subicular complex: Multivoxel pattern analysis at 7T
title_full Scene-selectivity in CA1/subicular complex: Multivoxel pattern analysis at 7T
title_fullStr Scene-selectivity in CA1/subicular complex: Multivoxel pattern analysis at 7T
title_full_unstemmed Scene-selectivity in CA1/subicular complex: Multivoxel pattern analysis at 7T
title_sort Scene-selectivity in CA1/subicular complex: Multivoxel pattern analysis at 7T
author_id_str_mv 555e06e0ed9a87608f2d035b3bde3a87
author_id_fullname_str_mv 555e06e0ed9a87608f2d035b3bde3a87_***_Jiaxiang Zhang
author Jiaxiang Zhang
author2 Marie-Lucie Read
Samuel C. Berry
Kim S. Graham
Natalie L. Voets
Jiaxiang Zhang
John P. Aggleton
Andrew D. Lawrence
Carl J. Hodgetts
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publishDate 2024
institution Swansea University
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doi_str_mv 10.1016/j.neuropsychologia.2023.108783
publisher Elsevier BV
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hierarchy_parent_id facultyofscienceandengineering
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description Prior univariate functional magnetic resonance imaging (fMRI) studies in humans suggest that the anteromedial subicular complex of the hippocampus is a hub for scene-based cognition. However, it is possible that univariate approaches were not sufficiently sensitive to detect scene-related activity in other subfields that have been implicated in spatial processing (e.g., CA1). Further, as connectivity-based functional gradients in the hippocampus do not respect classical subfield boundary definitions, category selectivity may be distributed across anatomical subfields. Region-of-interest approaches, therefore, may limit our ability to observe category selectivity across discrete subfield boundaries. To address these issues, we applied searchlight multivariate pattern analysis to 7T fMRI data of healthy adults who undertook a simultaneous visual odd-one-out discrimination task for scene and non-scene (including face) visual stimuli, hypothesising that scene classification would be possible in multiple hippocampal regions within, but not constrained to, anteromedial subicular complex and CA1. Indeed, we found that the scene-selective searchlight map overlapped not only with anteromedial subicular complex (distal subiculum, pre/para subiculum), but also inferior CA1, alongside posteromedial (including retrosplenial) and parahippocampal cortices. Probabilistic overlap maps revealed gradients of scene category selectivity, with the strongest overlap located in the medial hippocampus, converging with searchlight findings. This was contrasted with gradients of face category selectivity, which had stronger overlap in more lateral hippocampus, supporting ideas of parallel processing streams for these two categories. Our work helps to map the scene, in contrast to, face processing networks within, and connected to, the human hippocampus.
published_date 2024-02-15T11:42:48Z
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