Selective perforant-pathway atrophy in Huntington disease : MRI analysis of hippocampal subfields

Journal article

Wibawa, Pierre, Walterfang, Mark, Malpas, Charles B., Glikmann-Johnston, Yifat, Poudel, Govinda, Razi, Adeel, Hannan, Anthony J., Velakoulis, Dennis and Georgiou-Karistianis, Nellie. (2023). Selective perforant-pathway atrophy in Huntington disease : MRI analysis of hippocampal subfields. European Journal of Neurology. 30(9), pp. 2650-2660. https://doi.org/10.1111/ene.15918
AuthorsWibawa, Pierre, Walterfang, Mark, Malpas, Charles B., Glikmann-Johnston, Yifat, Poudel, Govinda, Razi, Adeel, Hannan, Anthony J., Velakoulis, Dennis and Georgiou-Karistianis, Nellie
Abstract

Introduction
While individuals with Huntington disease (HD) show memory impairment that indicates hippocampal dysfunction, the available literature does not consistently identify structural evidence for involvement of the whole hippocampus but rather suggests that hippocampal atrophy may be confined to certain hippocampal subregions.

Methods
We processed T1-weighted MRI from IMAGE-HD study using FreeSurfer 7.0 and compared the volumes of the hippocampal subfields among 36 early motor symptomatic (symp-HD), 40 pre-symptomatic (pre-HD), and 36 healthy control individuals across three timepoints over 36 months.

Results
Mixed-model analyses revealed significantly lower subfield volumes in symp-HD, compared with pre-HD and control groups, in the subicular regions of the perforant-pathway: presubiculum, subiculum, dentate gyrus, tail, and right molecular layer. These adjoining subfields aggregated into a single principal component, which demonstrated an accelerated rate of atrophy in the symp-HD. Volumes between pre-HD and controls did not show any significant difference. In the combined HD groups, CAG repeat length and disease burden score were associated with presubiculum, molecular layer, tail, and perforant-pathway subfield volumes. Hippocampal left tail and perforant-pathway subfields were associated with motor onset in the pre-HD group.

Conclusions
Hippocampal subfields atrophy in early symptomatic HD affects key regions of the perforant-pathway, which may implicate the distinctive memory impairment at this stage of illness. Their volumetric associations with genetic and clinical markers suggest the selective susceptibility of these subfields to mutant Huntingtin and disease progression.

Keywordshippocampal subfields; hippocampus; Huntington disease; memory; MRI
Year2023
JournalEuropean Journal of Neurology
Journal citation30 (9), pp. 2650-2660
PublisherJohn Wiley & Sons Ltd
ISSN1351-5101
Digital Object Identifier (DOI)https://doi.org/10.1111/ene.15918
PubMed ID37306313
Scopus EID2-s2.0-85163026548
PubMed Central IDPMC10946817
Open accessPublished as ‘gold’ (paid) open access
Page range2650-2660
FunderCHDI Foundation
National Health and Medical Research Council (NHMRC)
Publisher's version
License
File Access Level
Open
Output statusPublished
Publication dates
Online23 Jun 2023
Publication process dates
Accepted08 Jun 2023
Deposited31 Mar 2025
Grant IDA—3433
606650].
Additional information

© 2023 The Authors. European Journal of Neurology published by John Wiley & Sons Ltd on behalf of European Academy of Neurology.

This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License (http://creativecommons.org/licenses/by-nc-nd/4.0/), which permits use and distribution in any medium, provided the original work is properly cited, the use is non-commercial and no modifications or adaptations are made.

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Multimodal imaging biomarkers in premanifest and early Huntington's disease: 30-month IMAGE-HD data
Dominguez, Juan, Stout, Julie C., Poudel, Govinda, Churchyard, Andrew, Chua, Phyllis, Egan, Gary F. and Georgiou-Karistianis, Nellie. (2016). Multimodal imaging biomarkers in premanifest and early Huntington's disease: 30-month IMAGE-HD data. British Journal of Psychiatry. 208(6), pp. 571 - 578. https://doi.org/10.1192/bjp.bp.114.156588
Time-varying effective connectivity of the cortical neuroelectric activity associated with behavioural microsleeps
Toppi, Jlenia, Astolfi, Laura, Poudel, Govinda, H., Babiloni, Fabio, Jones, Richard and Innes, Carrie R. H.. (2016). Time-varying effective connectivity of the cortical neuroelectric activity associated with behavioural microsleeps. NeuroImage. 124, pp. 421 - 432. https://doi.org/10.1016/j.neuroimage.2015.08.059
Characterising upper limb movements in Huntington's Disease and the impact of restricted visual cues
Despard, Jessica, Ternes, Anne-Marie, Dimech-Betancourt, Bleydy, Poudel, Govinda, Churchyard, Andrew and Georgiou-Karistianis, Nellie. (2015). Characterising upper limb movements in Huntington's Disease and the impact of restricted visual cues. PLoS ONE. 10(8), pp. 1 - 18. https://doi.org/10.1371/journal.pone.0133709
Comparison of beamformers for EEG source signal reconstruction
Jonmohamadi, Yaqub, Poudel, Govinda, Innes, Carrie, Weiss, Daniel, Krueger, Rejko and Jones, Richard. (2014). Comparison of beamformers for EEG source signal reconstruction. Biomedical Signal Processing and Control. 14(1), pp. 175 - 188. https://doi.org/10.1016/j.bspc.2014.07.014
Source-space ICA for EEG source separation, localization, and time-course reconstruction
Jonmohamadi, Yaqub, Poudel, Govinda, Innes, Carrie and Jones, Richard. (2014). Source-space ICA for EEG source separation, localization, and time-course reconstruction. NeuroImage. 101(November), pp. 720 - 737. https://doi.org/10.1016/j.neuroimage.2014.07.052
The Multi-modal Australian ScienceS Imaging and Visualization Environment (MASSIVE) high performance computing infrastructure: Applications in neuroscience and neuroinformatics research
Goscinski, Wojtek J., McIntosh, Paul, Felzmann, Ulrich, Maksimenko, Anton, Hall, Christopher J., Gureyev, Timur, Thompson, Darren, Janke, Andrew, Galloway, Graham, Killeen, Neil E. B., Raniga, Parnesh, Kaluza, Owen, Ng, Amanda, Poudel, Govinda, Barnes, David G., Nguyen, Toan, Bonnington, Paul and Egan, Gary F.. (2014). The Multi-modal Australian ScienceS Imaging and Visualization Environment (MASSIVE) high performance computing infrastructure: Applications in neuroscience and neuroinformatics research. Frontiers in Neuroinformatics. 8(March), pp. 1 - 13. https://doi.org/10.3389/fninf.2014.00030
Functional magnetic resonance imaging of working memory in Huntington's disease: Cross-sectional data from the IMAGE-HD study
Georgiou-Karistianis, Nellie, Stout, Julie C., Domínguez, Juan F., Carron, Sarah P., Ando, Ayaka, Churchyard, Andrew, Chua, Phyllis, Bohanna, India, Dymowski, Alicia R., Poudel, Govinda and Egan, Gary F.. (2014). Functional magnetic resonance imaging of working memory in Huntington's disease: Cross-sectional data from the IMAGE-HD study. Human Brain Mapping. 35(5), pp. 1847 - 1864. https://doi.org/10.1002/hbm.22296
Voxel-ICA for reconstruction of source signal time-series and orientation in EEG and MEG
Jonmohamadi, Yaqub, Poudel, Govinda, Innes, Carrie and Jones, Richard. (2014). Voxel-ICA for reconstruction of source signal time-series and orientation in EEG and MEG. Australasian Physical and Engineering Sciences in Medicine. 37(2), pp. 457 - 464. https://doi.org/10.1007/s13246-014-0265-x
Multi-modal neuroimaging in premanifest and early Huntington's disease : 18 month longitudinal data from the IMAGE-HD study
Domínguez D, Juan F., Egan, Gary F., Gray, Marcus A., Poudel, Govinda R., Churchyard, Andrew, Chua, Phyllis, Stout, Julie C. and Georgiou-Karistianis, Nellie. (2013). Multi-modal neuroimaging in premanifest and early Huntington's disease : 18 month longitudinal data from the IMAGE-HD study. PLoS ONE. 8(9), pp. 1-10. https://doi.org/10.1371/journal.pone.0074131
Functional and connectivity changes during working memory in Huntington's disease : 18 month longitudinal data from the IMAGE-HD study
Georgiou-Karistianis, Nellie, Poudel, Govinda R., Domínguez D, Juan F., Langmaid, Rebecca, Gray, Marcus A., Churchyard, Andrew, Chua, Phyllis, Borowsky, Beth, Egan, Gary F. and Stout, Julie C.. (2013). Functional and connectivity changes during working memory in Huntington's disease : 18 month longitudinal data from the IMAGE-HD study. Brain and Cognition. 83(1), pp. 80-91. https://doi.org/10.1016/j.bandc.2013.07.004
Efficient and regular patterns of nighttime sleep are related to increased vulnerability to microsleeps following a single night of sleep restriction
Innes, Carrie R. H., Poudel, Govinda R. and Jones, Richard D.. (2013). Efficient and regular patterns of nighttime sleep are related to increased vulnerability to microsleeps following a single night of sleep restriction. Chronobiology International. 30(9), pp. 1187-1196. https://doi.org/10.3109/07420528.2013.810222
Distinct neural correlates of time-on-task and transient errors during a visuomotor tracking task after sleep restriction
Poudel, Govinda R., Innes, Carrie R. H. and Jones, Richard D.. (2013). Distinct neural correlates of time-on-task and transient errors during a visuomotor tracking task after sleep restriction. NeuroImage. 77, pp. 105-113. https://doi.org/10.1016/j.neuroimage.2013.03.054
Time-Varying Functional Connectivity for Understanding the Neural Basis of Behavioral Microsleeps
J Toppi, L Astolfi, GR Poudel, F Babiloni, L Macchiusi, D Mattia, S Salinari and RD Jones. (2012). Time-Varying Functional Connectivity for Understanding the Neural Basis of Behavioral Microsleeps. 34th Annual International Conference of the IEEE EMBS. IEEE, Institute of Electrical and Electronics Engineers. pp. 4708-4711 https://doi.org/10.1109/EMBC.2012.6347018
Performance of Beamformers on EEG Source Reconstruction
Yaqub Jon Mohamadi, Govinda Poudel, Carrie R H Innes and Richard Jones. (2012). Performance of Beamformers on EEG Source Reconstruction. 34th Annual International Conference of the IEEE EMBS. IEEE, Institute of Electrical and Electronics Engineers. https://doi.org/10.1109/EMBC.2012.6346476
Cerebral perfusion differences between drowsy and nondrowsy individuals after acute sleep restriction
Poudel, Govinda R., Innes, Carrie R. H. and Jones, Richard D.. (2012). Cerebral perfusion differences between drowsy and nondrowsy individuals after acute sleep restriction. Sleep. 35(8), pp. 1085-1096. https://doi.org/10.5665/sleep.1994