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Papez Circuit Gray Matter and Episodic Memory in Amyotrophic Lateral Sclerosis and Behavioural Variant Frontotemporal Dementia

Abstract

Amyotrophic lateral sclerosis and behavioural variant frontotemporal dementia are two different diseases recognized to overlap at clinical, pathological and genetic characteristics. Both conditions are traditionally known for relative sparing of episodic memory. However, recent studies have disputed that with the report of patients presenting with marked episodic memory impairment. Besides that, structural and functional changes in temporal lobe regions responsible for episodic memory processing are often detected in neuroimaging studies of both conditions. In this study, we investigated the gray matter features associated with the Papez circuit in amyotrophic lateral sclerosis, behavioural variant frontotemporal dementia and healthy controls to further explore similarities and differences between the two conditions. Our non-demented amyotrophic lateral sclerosis patients showed no episodic memory deficits measured by a short-term delayed recall test while no changes in gray matter of the Papez circuit were found. Compared with the amyotrophic lateral sclerosis group, the behavioural variant frontotemporal dementia group had lower performance on the short-term delayed recall test and marked atrophy in gray matter of the Papez circuit. Bilateral atrophy of entorhinal cortex and mammillary bodies distinguished behavioural variant frontotemporal dementia from amyotrophic lateral sclerosis patients as well as atrophy in left cingulate, left hippocampus and right parahippocampal gyrus. Taken together, our results suggest that sub-regions of the Papez circuit could be differently affected in amyotrophic lateral sclerosis and behavioural variant frontotemporal dementia.

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Acknowledgements

The authors gratefully acknowledge the contribution of the patients and their families.

Funding

AB is supported by São Paulo Research Foundation (FAPESP) grant 2016/19376–9.

This study was funded by Conselho Nacional de Pesquisa Científica (CNPq), Brazil: Grant 402,853/2012. ALT, LCS and PC are supported by the Brazilian National Council for Scientific and Technological Development (CNPq – Bolsa de Produtividade em Pesquisa).

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APAB preprocessed MRI images, performed statistical analyses, drafted and edited the manuscript; LCS diagnosed the patients and performed cognitive assessments, drafted and revised the manuscript; WHLP supervised MRI preprocessing, prepared MRI figures and revised the manuscript; ALT diagnosed the patients, worked on financial support for MRI acquisition and revised the manuscript; LGRP has worked on patient selection, on financial support for MRI and revised the manuscript; PC diagnosed the patients and revised the manuscript; MH conceived the study and revised the manuscript; JRS supervised MRI preprocessing and statistical analyses, and revised the manuscript. All authors approved the final version of the manuscript.

Corresponding author

Correspondence to Ana Paula Arantes Bueno.

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The authors report no conflict of interest.

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All procedures performed in this study were in accordance with the ethical standards of national research committee, the institutional ethics committee of Universidade Federal de Minas Gerais and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

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Written informed consent was obtained from all individual participants included in the study or from a close relative.

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Bueno, A.P.A., de Souza, L.C., Pinaya, W.H.L. et al. Papez Circuit Gray Matter and Episodic Memory in Amyotrophic Lateral Sclerosis and Behavioural Variant Frontotemporal Dementia. Brain Imaging and Behavior 15, 996–1006 (2021). https://doi.org/10.1007/s11682-020-00307-5

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Keywords

  • Amyotrophic lateral sclerosis
  • Behavioural variant frontotemporal dementia
  • Episodic memory
  • Papez circuit