Scene construction impairments in frontotemporal dementia: evidence for a primary hippocampal contribution

Nikki-Anne Wilson, Siddharth Ramanan, Daniel Roquet, Zoë Lee Goldberg, John R. Hodges, Olivier Piguet, Muireann Irish*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

6 Citations (Scopus)

Abstract

The capacity to generate naturalistic three-dimensional and spatially coherent representations of the world, i.e., scene construction, is posited to lie at the heart of a wide range of complex cognitive endeavours. Clinical populations with selective damage to key nodes of a putative scene construction network of the brain have provided important insights regarding the contribution of medial temporal and prefrontal regions in this regard. Here, we explored the capacity for atemporal scene construction, and its associated neural substrates, in the behavioural-variant of frontotemporal dementia (bvFTD); a neurodegenerative brain disorder in which atrophy systematically erodes medial and lateral prefrontal cortices with variable medial temporal lobe involvement. Nineteen bvFTD patients were compared to 18 typical Alzheimer's Disease (AD), and 25 healthy older Control participants on a scene construction task. Relative to Controls, both patient groups displayed marked impairments in generating contextually detailed and spatially coherent scenes, with bvFTD indistinguishable from AD patients across the majority of task metrics. Voxel-based morphometry, based on structural brain MRI, revealed divergent neural substrates of scene construction performance in each patient group. Despite widespread medial and lateral prefrontal atrophy, the capacity to generate richly detailed and spatially coherent scenes in bvFTD was found to rely predominantly upon the integrity of right medial temporal structures, including the hippocampus and parahippocampal gyrus. Scene construction impairments in AD, by contrast, hinged upon the integrity of posterior parietal brain regions. Our findings in bvFTD resonate with a large body of work implicating the right hippocampus in the construction of spatially integrated scene imagery. How these impairments relate to changes in autobiographical memory and prospection in bvFTD will be an important question for future studies to address.

Original languageEnglish
Article number107327
Pages (from-to)1-9
Number of pages9
JournalNeuropsychologia
Volume137
DOIs
Publication statusPublished - 3 Feb 2020
Externally publishedYes

Bibliographical note

Funding Information:
The authors are grateful to the participants and their families for their continued support of our research. The authors wish to acknowledge the Sydney Informatics Hub, funded by the University of Sydney for providing access to High Performing Computing (HPC) facilities. This work was supported in part by funding to Forefront, a collaborative research group specialising in the study of frontotemporal dementia and motor neurone disease from the National Health and Medical Research Council of Australia (NHMRC; APP1037746) and the Australian Research Council (ARC) Centre of Excellence in Cognition and its Disorders Memory Program (CE110001021). N.-A.W. is supported by School of Psychology Stipend and Top Up scholarship from The University of Sydney. S.R. is supported by a Faculty of Science Ph.D. Research Scholarship from The University of Sydney. O.P. is supported by an NHMRC Senior Research Fellowship (APP1103258). D.R. is supported by an ARC Discovery Project (DP180101548). M.I. is supported by an ARC Future Fellowship (FT160100096).

Funding Information:
The authors are grateful to the participants and their families for their continued support of our research. The authors wish to acknowledge the Sydney Informatics Hub, funded by the University of Sydney for providing access to High Performing Computing (HPC) facilities. This work was supported in part by funding to Forefront, a collaborative research group specialising in the study of frontotemporal dementia and motor neurone disease from the National Health and Medical Research Council of Australia (NHMRC; APP1037746 ) and the Australian Research Council (ARC) Centre of Excellence in Cognition and its Disorders Memory Program ( CE110001021 ). N.-A.W. is supported by School of Psychology Stipend and Top Up scholarship from The University of Sydney . S.R. is supported by a Faculty of Science Ph.D. Research Scholarship from The University of Sydney. O.P. is supported by an NHMRC Senior Research Fellowship ( APP1103258 ). D.R. is supported by an ARC Discovery Project ( DP180101548 ). M.I. is supported by an ARC Future Fellowship ( FT160100096 ). Appendix A

Publisher Copyright:
© 2019 Elsevier Ltd

Copyright:
Copyright 2020 Elsevier B.V., All rights reserved.

Keywords

  • Episodic memory
  • Semantic memory
  • Imagination
  • Parietal lobe
  • Dementia
  • Medial prefrontal cortex

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