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The role of the fornix in human navigational learning

Carl J. Hodgetts, Martina Stefani, Angharad N. Williams, Branden S. Kolarik, Andrew P. Yonelinas, Arne D. Ekstrom, Andrew D. Lawrence, Jiaxiang Zhang Orcid Logo, Kim S. Graham

Cortex, Volume: 124, Pages: 97 - 110

Swansea University Author: Jiaxiang Zhang Orcid Logo

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DOI (Published version): 10.1016/j.cortex.2019.10.017

Abstract

Experiments on rodents have demonstrated that transecting the white matter fibre pathway linking the hippocampus with an array of cortical and subcortical structures - the fornix - impairs flexible navigational learning in the Morris Water Maze (MWM), as well as similar spatial learning tasks. While...

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Published in: Cortex
ISSN: 0010-9452
Published: Elsevier BV 2020
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URI: https://cronfa.swan.ac.uk/Record/cronfa61205
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While diffusion magnetic resonance imaging (dMRI) studies in humans have linked inter-individual differences in fornix microstructure to episodic memory abilities, its role in human spatial learning is currently unknown. We used high-angular resolution diffusion MRI combined with constrained spherical deconvolution-based tractography, to ask whether inter-individual differences in fornix microstructure in healthy young adults would be associated with spatial learning in a virtual reality navigation task. To efficiently capture individual learning across trials, we adopted a novel curve fitting approach to estimate a single index of learning rate. We found a statistically significant correlation between learning rate and the microstructure (mean diffusivity) of the fornix, but not that of a comparison tract linking occipital and anterior temporal cortices (the inferior longitudinal fasciculus, ILF). Further, this correlation remained significant when controlling for both hippocampal volume and participant gender. These findings extend previous animal studies by demonstrating the functional relevance of the fornix for human spatial learning in a virtual reality environment, and highlight the importance of a distributed neuroanatomical network, underpinned by key white matter pathways, such as the fornix, in complex spatial behaviour.</abstract><type>Journal Article</type><journal>Cortex</journal><volume>124</volume><journalNumber/><paginationStart>97</paginationStart><paginationEnd>110</paginationEnd><publisher>Elsevier BV</publisher><placeOfPublication/><isbnPrint/><isbnElectronic/><issnPrint>0010-9452</issnPrint><issnElectronic/><keywords>Hippocampus; Spatial navigation; Spatial learning; Episodic memory; Diffusion MRI</keywords><publishedDay>1</publishedDay><publishedMonth>3</publishedMonth><publishedYear>2020</publishedYear><publishedDate>2020-03-01</publishedDate><doi>10.1016/j.cortex.2019.10.017</doi><url/><notes/><college>COLLEGE NANME</college><department>Computer Science</department><CollegeCode>COLLEGE CODE</CollegeCode><DepartmentCode>SCS</DepartmentCode><institution>Swansea University</institution><apcterm/><funders>This work was supported by funds from the Medical Research Council (G1002149; MR/N01233X/1), a Wellcome Strategic Award (104943/Z/14/Z), the National Institutes of Health (R01EY025999; R01NS076856), the National Institute of Neurological Disorders and Stroke (NSF BCS-1630296), the European Research Council ERC starting grant (716321), and the Wellcome Institutional Strategic Support Fund.</funders><projectreference/><lastEdited>2022-10-03T15:05:34.8673625</lastEdited><Created>2022-09-13T13:52:55.5675076</Created><path><level id="1">Faculty of Science and Engineering</level><level id="2">School of Mathematics and Computer Science - Computer Science</level></path><authors><author><firstname>Carl J.</firstname><surname>Hodgetts</surname><order>1</order></author><author><firstname>Martina</firstname><surname>Stefani</surname><order>2</order></author><author><firstname>Angharad N.</firstname><surname>Williams</surname><order>3</order></author><author><firstname>Branden S.</firstname><surname>Kolarik</surname><order>4</order></author><author><firstname>Andrew P.</firstname><surname>Yonelinas</surname><order>5</order></author><author><firstname>Arne D.</firstname><surname>Ekstrom</surname><order>6</order></author><author><firstname>Andrew D.</firstname><surname>Lawrence</surname><order>7</order></author><author><firstname>Jiaxiang</firstname><surname>Zhang</surname><orcid>0000-0002-4758-0394</orcid><order>8</order></author><author><firstname>Kim S.</firstname><surname>Graham</surname><order>9</order></author></authors><documents><document><filename>61205__25289__3305e9c6a43245918d747bd7012a79ab.pdf</filename><originalFilename>61205_VoR.pdf</originalFilename><uploaded>2022-10-03T15:04:39.0794669</uploaded><type>Output</type><contentLength>1817746</contentLength><contentType>application/pdf</contentType><version>Version of Record</version><cronfaStatus>true</cronfaStatus><documentNotes>&#xA9; 2019 The Authors. 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spelling 2022-10-03T15:05:34.8673625 v2 61205 2022-09-13 The role of the fornix in human navigational learning 555e06e0ed9a87608f2d035b3bde3a87 0000-0002-4758-0394 Jiaxiang Zhang Jiaxiang Zhang true false 2022-09-13 SCS Experiments on rodents have demonstrated that transecting the white matter fibre pathway linking the hippocampus with an array of cortical and subcortical structures - the fornix - impairs flexible navigational learning in the Morris Water Maze (MWM), as well as similar spatial learning tasks. While diffusion magnetic resonance imaging (dMRI) studies in humans have linked inter-individual differences in fornix microstructure to episodic memory abilities, its role in human spatial learning is currently unknown. We used high-angular resolution diffusion MRI combined with constrained spherical deconvolution-based tractography, to ask whether inter-individual differences in fornix microstructure in healthy young adults would be associated with spatial learning in a virtual reality navigation task. To efficiently capture individual learning across trials, we adopted a novel curve fitting approach to estimate a single index of learning rate. We found a statistically significant correlation between learning rate and the microstructure (mean diffusivity) of the fornix, but not that of a comparison tract linking occipital and anterior temporal cortices (the inferior longitudinal fasciculus, ILF). Further, this correlation remained significant when controlling for both hippocampal volume and participant gender. These findings extend previous animal studies by demonstrating the functional relevance of the fornix for human spatial learning in a virtual reality environment, and highlight the importance of a distributed neuroanatomical network, underpinned by key white matter pathways, such as the fornix, in complex spatial behaviour. Journal Article Cortex 124 97 110 Elsevier BV 0010-9452 Hippocampus; Spatial navigation; Spatial learning; Episodic memory; Diffusion MRI 1 3 2020 2020-03-01 10.1016/j.cortex.2019.10.017 COLLEGE NANME Computer Science COLLEGE CODE SCS Swansea University This work was supported by funds from the Medical Research Council (G1002149; MR/N01233X/1), a Wellcome Strategic Award (104943/Z/14/Z), the National Institutes of Health (R01EY025999; R01NS076856), the National Institute of Neurological Disorders and Stroke (NSF BCS-1630296), the European Research Council ERC starting grant (716321), and the Wellcome Institutional Strategic Support Fund. 2022-10-03T15:05:34.8673625 2022-09-13T13:52:55.5675076 Faculty of Science and Engineering School of Mathematics and Computer Science - Computer Science Carl J. Hodgetts 1 Martina Stefani 2 Angharad N. Williams 3 Branden S. Kolarik 4 Andrew P. Yonelinas 5 Arne D. Ekstrom 6 Andrew D. Lawrence 7 Jiaxiang Zhang 0000-0002-4758-0394 8 Kim S. Graham 9 61205__25289__3305e9c6a43245918d747bd7012a79ab.pdf 61205_VoR.pdf 2022-10-03T15:04:39.0794669 Output 1817746 application/pdf Version of Record true © 2019 The Authors. This is an open access article under the CC BY license true eng http://creativecommons.org/licenses/by/4.0/
title The role of the fornix in human navigational learning
spellingShingle The role of the fornix in human navigational learning
Jiaxiang Zhang
title_short The role of the fornix in human navigational learning
title_full The role of the fornix in human navigational learning
title_fullStr The role of the fornix in human navigational learning
title_full_unstemmed The role of the fornix in human navigational learning
title_sort The role of the fornix in human navigational learning
author_id_str_mv 555e06e0ed9a87608f2d035b3bde3a87
author_id_fullname_str_mv 555e06e0ed9a87608f2d035b3bde3a87_***_Jiaxiang Zhang
author Jiaxiang Zhang
author2 Carl J. Hodgetts
Martina Stefani
Angharad N. Williams
Branden S. Kolarik
Andrew P. Yonelinas
Arne D. Ekstrom
Andrew D. Lawrence
Jiaxiang Zhang
Kim S. Graham
format Journal article
container_title Cortex
container_volume 124
container_start_page 97
publishDate 2020
institution Swansea University
issn 0010-9452
doi_str_mv 10.1016/j.cortex.2019.10.017
publisher Elsevier BV
college_str Faculty of Science and Engineering
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hierarchy_top_id facultyofscienceandengineering
hierarchy_top_title Faculty of Science and Engineering
hierarchy_parent_id facultyofscienceandengineering
hierarchy_parent_title Faculty of Science and Engineering
department_str School of Mathematics and Computer Science - Computer Science{{{_:::_}}}Faculty of Science and Engineering{{{_:::_}}}School of Mathematics and Computer Science - Computer Science
document_store_str 1
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description Experiments on rodents have demonstrated that transecting the white matter fibre pathway linking the hippocampus with an array of cortical and subcortical structures - the fornix - impairs flexible navigational learning in the Morris Water Maze (MWM), as well as similar spatial learning tasks. While diffusion magnetic resonance imaging (dMRI) studies in humans have linked inter-individual differences in fornix microstructure to episodic memory abilities, its role in human spatial learning is currently unknown. We used high-angular resolution diffusion MRI combined with constrained spherical deconvolution-based tractography, to ask whether inter-individual differences in fornix microstructure in healthy young adults would be associated with spatial learning in a virtual reality navigation task. To efficiently capture individual learning across trials, we adopted a novel curve fitting approach to estimate a single index of learning rate. We found a statistically significant correlation between learning rate and the microstructure (mean diffusivity) of the fornix, but not that of a comparison tract linking occipital and anterior temporal cortices (the inferior longitudinal fasciculus, ILF). Further, this correlation remained significant when controlling for both hippocampal volume and participant gender. These findings extend previous animal studies by demonstrating the functional relevance of the fornix for human spatial learning in a virtual reality environment, and highlight the importance of a distributed neuroanatomical network, underpinned by key white matter pathways, such as the fornix, in complex spatial behaviour.
published_date 2020-03-01T04:19:52Z
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