Functional and connectivity changes during working memory in Huntington's disease : 18 month longitudinal data from the IMAGE-HD study

Journal article

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
AuthorsGeorgiou-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.
Abstract

Background
This study aimed to characterize, for the first time, 18 month longitudinal changes in both functional activation and functional connectivity during working memory in premanifest Huntington’s disease (pre-HD) and symptomatic HD (symp-HD).

Methods
Functional magnetic resonance imaging (fMRI) was used to investigate longitudinal changes in neuronal activity during working memory performance via an N-BACK task (0-BACK and 1-BACK) in 27 pre-HD, 17 symp-HD, and 23 control participants. Whole-brain analysis of activation and region-of-interest analysis of functional connectivity was applied to longitudinal fMRI data collected at baseline and 18 months follow-up.

Results
Compared with controls, the pre-HD group showed significantly increased activation longitudinally during 1-BACK versus 0-BACK in the lateral and medial prefrontal, anterior cingulate, primary motor, and temporal areas cortically, and caudate and putamen subcortically. Pre-HD far from onset, compared with controls, showed further longitudinal increases in the right and left dorsolateral prefrontal cortex (DLPFC). Longitudinal increased activation in anterior cingulate and medial primary motor areas were associated with disease burden in the pre-HD group. Moreover, in pre-HD increased activation over time in primary motor and putamen regions were associated with average response time during 1-BACK performance. During 1-BACK, functional connectivity between the right DLPFC and posterior parietal, anterior cingulate, and caudate was significantly reduced over 18 months only in the pre-HD group.

Conclusions
Longitudinal reductions in connectivity over 18 months may represent an early signature of cortico-cortical and cortico-striatal functional disconnectivity in pre-HD, whereas the concomitant increased cortical and subcortical activation may reflect a compensatory response to the demands for cognitive resources required during task performance. Our findings demonstrate that functional imaging modalities have the potential to serve as sensitive methods for the assessment of cortical and subcortical responses to future treatment measures.

KeywordsHuntington’s disease; functional connectivity; functional MRI; longitudinal; working memory
Year2013
JournalBrain and Cognition
Journal citation83 (1), pp. 80-91
PublisherAcademic Press
ISSN0278-2626
Digital Object Identifier (DOI)https://doi.org/10.1016/j.bandc.2013.07.004
Scopus EID2-s2.0-84882255988
Research or scholarlyResearch
Page range80-91
FunderNational Health and Medical Research Council (NHMRC)
Publisher's version
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All rights reserved
File Access Level
Controlled
Output statusPublished
Publication dates
Online09 Aug 2013
Publication process dates
Accepted16 Jul 2013
Deposited27 Apr 2021
Grant IDNHMRC/606650
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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
Longitudinal change in white matter microstructure in Huntington's disease: The IMAGE-HD study
Poudel, Govinda R., Stout, Julie C., Dominguez, Juan F., Churchyard, Andrew, Chua, Phyllis, Egan, Gary F. and Georgiou-Karistianis, Nellie. (2015). Longitudinal change in white matter microstructure in Huntington's disease: The IMAGE-HD study. Neurobiology of Disease. 74(1), pp. 406 - 412. https://doi.org/10.1016/j.nbd.2014.12.009
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
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