Age-Related Differences in Functional and Structural Connectivity in the Spatial Navigation Brain Network

Spatial navigation involves multiple cognitive processes including multisensory integration, visuospatial coding, memory, and decision-making. These functions are mediated by the interplay of cerebral structures that can be broadly separated into a posterior network (subserving visual and spatial pr...

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Main Authors: Stephen Ramanoël, Elizabeth York, Marine Le Petit, Karine Lagrené, Christophe Habas, Angelo Arleo
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-10-01
Series:Frontiers in Neural Circuits
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fncir.2019.00069/full
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author Stephen Ramanoël
Elizabeth York
Elizabeth York
Marine Le Petit
Marine Le Petit
Karine Lagrené
Christophe Habas
Angelo Arleo
author_facet Stephen Ramanoël
Elizabeth York
Elizabeth York
Marine Le Petit
Marine Le Petit
Karine Lagrené
Christophe Habas
Angelo Arleo
author_sort Stephen Ramanoël
collection DOAJ
description Spatial navigation involves multiple cognitive processes including multisensory integration, visuospatial coding, memory, and decision-making. These functions are mediated by the interplay of cerebral structures that can be broadly separated into a posterior network (subserving visual and spatial processing) and an anterior network (dedicated to memory and navigation planning). Within these networks, areas such as the hippocampus (HC) are known to be affected by aging and to be associated with cognitive decline and navigation impairments. However, age-related changes in brain connectivity within the spatial navigation network remain to be investigated. For this purpose, we performed a neuroimaging study combining functional and structural connectivity analyses between cerebral regions involved in spatial navigation. Nineteen young (μ = 27 years, σ = 4.3; 10 F) and 22 older (μ = 73 years, σ = 4.1; 10 F) participants were examined in this study. Our analyses focused on the parahippocampal place area (PPA), the retrosplenial cortex (RSC), the occipital place area (OPA), and the projections into the visual cortex of central and peripheral visual fields, delineated from independent functional localizers. In addition, we segmented the HC and the medial prefrontal cortex (mPFC) from anatomical images. Our results show an age-related decrease in functional connectivity between low-visual areas and the HC, associated with an increase in functional connectivity between OPA and PPA in older participants compared to young subjects. Concerning the structural connectivity, we found age-related differences in white matter integrity within the navigation brain network, with the exception of the OPA. The OPA is known to be involved in egocentric navigation, as opposed to allocentric strategies which are more related to the hippocampal region. The increase in functional connectivity between the OPA and PPA may thus reflect a compensatory mechanism for the age-related alterations around the HC, favoring the use of the preserved structural network mediating egocentric navigation. Overall, these findings on age-related differences of functional and structural connectivity may help to elucidate the cerebral bases of spatial navigation deficits in healthy and pathological aging.
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spelling doaj.art-7cd08e7976ad40d38f9085720b4129422022-12-22T03:19:08ZengFrontiers Media S.A.Frontiers in Neural Circuits1662-51102019-10-011310.3389/fncir.2019.00069475288Age-Related Differences in Functional and Structural Connectivity in the Spatial Navigation Brain NetworkStephen Ramanoël0Elizabeth York1Elizabeth York2Marine Le Petit3Marine Le Petit4Karine Lagrené5Christophe Habas6Angelo Arleo7Sorbonne Universités, INSERM, CNRS, Institut de la Vision, Paris, FranceSorbonne Universités, INSERM, CNRS, Institut de la Vision, Paris, FranceCentre for Clinical Brain Sciences, University of Edinburgh, Edinburgh, United KingdomSorbonne Universités, INSERM, CNRS, Institut de la Vision, Paris, FranceNormandie Université, UNICAEN, PSL Université Paris, EPHE, INSERM, U1077, CHU de Caen, Neuropsychologie et Imagerie de la Mémoire Humaine, Caen, FranceSorbonne Universités, INSERM, CNRS, Institut de la Vision, Paris, FranceCHNO des Quinze-Vingts, INSERM-DHOS CIC 1423, Paris, FranceSorbonne Universités, INSERM, CNRS, Institut de la Vision, Paris, FranceSpatial navigation involves multiple cognitive processes including multisensory integration, visuospatial coding, memory, and decision-making. These functions are mediated by the interplay of cerebral structures that can be broadly separated into a posterior network (subserving visual and spatial processing) and an anterior network (dedicated to memory and navigation planning). Within these networks, areas such as the hippocampus (HC) are known to be affected by aging and to be associated with cognitive decline and navigation impairments. However, age-related changes in brain connectivity within the spatial navigation network remain to be investigated. For this purpose, we performed a neuroimaging study combining functional and structural connectivity analyses between cerebral regions involved in spatial navigation. Nineteen young (μ = 27 years, σ = 4.3; 10 F) and 22 older (μ = 73 years, σ = 4.1; 10 F) participants were examined in this study. Our analyses focused on the parahippocampal place area (PPA), the retrosplenial cortex (RSC), the occipital place area (OPA), and the projections into the visual cortex of central and peripheral visual fields, delineated from independent functional localizers. In addition, we segmented the HC and the medial prefrontal cortex (mPFC) from anatomical images. Our results show an age-related decrease in functional connectivity between low-visual areas and the HC, associated with an increase in functional connectivity between OPA and PPA in older participants compared to young subjects. Concerning the structural connectivity, we found age-related differences in white matter integrity within the navigation brain network, with the exception of the OPA. The OPA is known to be involved in egocentric navigation, as opposed to allocentric strategies which are more related to the hippocampal region. The increase in functional connectivity between the OPA and PPA may thus reflect a compensatory mechanism for the age-related alterations around the HC, favoring the use of the preserved structural network mediating egocentric navigation. Overall, these findings on age-related differences of functional and structural connectivity may help to elucidate the cerebral bases of spatial navigation deficits in healthy and pathological aging.https://www.frontiersin.org/article/10.3389/fncir.2019.00069/fullhealthy agingMRIresting-statediffusionconnectivityspatial navigation
spellingShingle Stephen Ramanoël
Elizabeth York
Elizabeth York
Marine Le Petit
Marine Le Petit
Karine Lagrené
Christophe Habas
Angelo Arleo
Age-Related Differences in Functional and Structural Connectivity in the Spatial Navigation Brain Network
Frontiers in Neural Circuits
healthy aging
MRI
resting-state
diffusion
connectivity
spatial navigation
title Age-Related Differences in Functional and Structural Connectivity in the Spatial Navigation Brain Network
title_full Age-Related Differences in Functional and Structural Connectivity in the Spatial Navigation Brain Network
title_fullStr Age-Related Differences in Functional and Structural Connectivity in the Spatial Navigation Brain Network
title_full_unstemmed Age-Related Differences in Functional and Structural Connectivity in the Spatial Navigation Brain Network
title_short Age-Related Differences in Functional and Structural Connectivity in the Spatial Navigation Brain Network
title_sort age related differences in functional and structural connectivity in the spatial navigation brain network
topic healthy aging
MRI
resting-state
diffusion
connectivity
spatial navigation
url https://www.frontiersin.org/article/10.3389/fncir.2019.00069/full
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