White matter predicts functional connectivity in premanifest Huntington's disease

Journal article


McColgan, Peter, Gregory, Sarah, Razi, Adeel, Seunarine, Kiran K., Gargouri, Fatma, Durr, Alexandra, Roos, Raymund A. C., Leavitt, Blair R., Scahill, Rachael I., Clark, Chris A., Tabrizi, Sarah J., Rees, Geraint, Coleman, Allison J., Decolongon, J., Fan, M., Petkau, T., Jauffret, Céline, Justo, Damian, Lehericy, S., ... Johnson, H.. (2017) White matter predicts functional connectivity in premanifest Huntington's disease. Annals of Clinical and Translational Neurology. 4(2), pp. 106 - 118. https://doi.org/10.1002/acn3.384
AuthorsMcColgan, Peter, Gregory, Sarah, Razi, Adeel, Seunarine, Kiran K., Gargouri, Fatma, Durr, Alexandra, Roos, Raymund A. C., Leavitt, Blair R., Scahill, Rachael I., Clark, Chris A., Tabrizi, Sarah J., Rees, Geraint, Coleman, Allison J., Decolongon, J., Fan, M., Petkau, T., Jauffret, Céline, Justo, Damian, Lehericy, S., Nigaud, Kevin, Valabregue, R., Schoonderbeek, A., Hart, Ellen P., Moss, D. J. Hensman, Crawford, H., Johnson, Eileanoir, Papoutsi, Marina, Berna, C., Reilmann, R., Weber, N., Stout, J., Labuschagne, I., Landwehrmeyer, B., Orth, M. and Johnson, H.
Abstract

Objectives The distribution of pathology in neurodegenerative disease can be predicted by the organizational characteristics of white matter in healthy brains. However, we have very little evidence for the impact these pathological changes have on brain function. Understanding any such link between structure and function is critical for understanding how underlying brain pathology influences the progressive behavioral changes associated with neurodegeneration. Here, we demonstrate such a link between structure and function in individuals with premanifest Huntington's. Methods Using diffusion tractography and resting state functional magnetic resonance imaging to characterize white matter organization and functional connectivity, we investigate whether characteristic patterns of white matter organization in the healthy human brain shape the changes in functional coupling between brain regions in premanifest Huntington's disease. Results We find changes in functional connectivity in premanifest Huntington's disease that link directly to underlying patterns of white matter organization in healthy brains. Specifically, brain areas with strong structural connectivity show decreases in functional connectivity in premanifest Huntington's disease relative to controls, while regions with weak structural connectivity show increases in functional connectivity. Furthermore, we identify a pattern of dissociation in the strongest functional connections between anterior and posterior brain regions such that anterior functional connectivity increases in strength in premanifest Huntington's disease, while posterior functional connectivity decreases. Interpretation Our findings demonstrate that organizational principles of white matter underlie changes in functional connectivity in premanifest Huntington's disease. Furthermore, we demonstrate functional antero–posterior dissociation that is in keeping with the caudo–rostral gradient of striatal pathology in HD. The distribution of pathology in neurodegenerative disease can be predicted by the organizational characteristics of white matter in healthy brains. However, we have very little evidence for the impact these pathological changes have on brain function. Understanding any such link between structure and function is critical for understanding how underlying brain pathology influences the progressive behavioral changes associated with neurodegeneration. Here, we demonstrate such a link between structure and function in individuals with premanifest Huntington's. Methods Using diffusion tractography and resting state functional magnetic resonance imaging to characterize white matter organization and functional connectivity, we investigate whether characteristic patterns of white matter organization in the healthy human brain shape the changes in functional coupling between brain regions in premanifest Huntington's disease. Results We find changes in functional connectivity in premanifest Huntington's disease that link directly to underlying patterns of white matter organization in healthy brains. Specifically, brain areas with strong structural connectivity show decreases in functional connectivity in premanifest Huntington's disease relative to controls, while regions with weak structural connectivity show increases in functional connectivity. Furthermore, we identify a pattern of dissociation in the strongest functional connections between anterior and posterior brain regions such that anterior functional connectivity increases in strength in premanifest Huntington's disease, while posterior functional connectivity decreases. Interpretation Our findings demonstrate that organizational principles of white matter underlie changes in functional connectivity in premanifest Huntington's disease. Furthermore, we demonstrate functional antero–posterior dissociation that is in keeping with the caudo–rostral gradient of striatal pathology in HD.

Year2017
JournalAnnals of Clinical and Translational Neurology
Journal citation4 (2), pp. 106 - 118
PublisherWiley-Blackwell
ISSN2328-9503
Digital Object Identifier (DOI)https://doi.org/10.1002/acn3.384
Scopus EID2-s2.0-85027403020
Open accessOpen access
Page range106 - 118
Research GroupSchool of Philosophy
Publisher's version
License
Place of publicationUnited States of America
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Stout, Julie, Jones, Rebecca, Labuschagne, Izelle, O'Regan, Alison, Say, Miranda, Dumas, Eve, Queller, Sarah, Justo, Damian, Dar Santos, Rachelle, Coleman, Allison, Hart, Ellen, Durr, Alexandra, Leavitt, Blair, Roos, Raymund, Langbehn, Doug, Tabrizi, Sarah J. and Frost, Chris. (2012) Evaluation of longitudinal 12 and 24 month cognitive outcomes in premanifest and early Huntington's disease. Journal of Neurology, Neurosurgery and Psychiatry. 83(7), pp. 687 - 694. https://doi.org/10.1136/jnnp-2011-301940
Medial frontal hyperactivity to sad faces in generalized social anxiety disorder and modulation by oxytocin
Labuschagne, Izelle, Phan, K. Luan, Wood, Amanda, Angstadt, Mike, Chua, Phyllis, Heinrichs, Markus, Stout, Julie C., Nathan, Pradeep J. and Pradeep, . (2012) Medial frontal hyperactivity to sad faces in generalized social anxiety disorder and modulation by oxytocin. International Journal of Neuropsychopharmacology (print). 15(7), pp. 883 - 896. https://doi.org/10.1017/S1461145711001489
Evaluation of longitudinal 12 and 24 month cognitive outcomes in premanifest and early Huntington's disease
Stout, Julie, Jones, Rebecca, Labuschagne, Izelle, O'Regan, Alison, Say, Miranda, Dumas, Eve, Queller, Sarah, Justo, Damian, Dar Santos, Rachelle, Coleman, Allison, Hart, Ellen, Durr, Alexandra, Leavitt, Blair, Roos, Raymund, Langbehn, Douglas, Tabrizi, Sarah J. and Frost, Chris. (2012) Evaluation of longitudinal 12 and 24 month cognitive outcomes in premanifest and early Huntington's disease. Journal of Neurology, Neurosurgery and Psychiatry. 83(7), pp. 687 - 694. https://doi.org/10.1136/jnnp-2011-301940
What the cognitive deficits in body dysmorphic disorder tell us about the underlying neurobiology: An investigation of three cases
Labuschagne, Izelle, Castle, David and Rossell, Susan L.. (2011) What the cognitive deficits in body dysmorphic disorder tell us about the underlying neurobiology: An investigation of three cases. International Journal of Cognitive Therapy. 4(1), pp. 21 - 33. https://doi.org/10.1521/ijct.2011.4.1.21
Oxytocin attenuates amygdala reactivity to fear in generalized social anxiety disorder
Labuschagne, Izelle, Phan, K. Luan, Wood, Amanda G., Angstadt, Mike, Chua, Phyllis, Heinrichs, Markus, Stout, Julie C. and Nathan, Pradeep. (2010) Oxytocin attenuates amygdala reactivity to fear in generalized social anxiety disorder. Neuropsychopharmacology. 35(12), pp. 2403 - 2413. https://doi.org/10.1038/npp.2010.123
Augmenting serotonin neurotransmission with citalopram modulates emotional expression decoding but not structural encoding of moderate intensity sad facial emotional stimuli: An event-related potential (ERP) investigation
Labuschagne, Izelle, Croft, Rodney, Phan, K. Luan and Nathan, Pradeep. (2010) Augmenting serotonin neurotransmission with citalopram modulates emotional expression decoding but not structural encoding of moderate intensity sad facial emotional stimuli: An event-related potential (ERP) investigation. Journal of Psychopharmacology. 24(8), pp. 1153 - 1164. https://doi.org/10.1177/0269881108097878
Executive function in body dysmorphic disorder
Dunai, Judith, Labuschagne, Izelle, Castle, David J., Kyrios, Michael and Rossell, Susan. (2010) Executive function in body dysmorphic disorder. Psychological Medicine. 40(9), pp. 1541 - 1548. https://doi.org/10.1017/S003329170999198X
An examination of delusional thinking and cognitive styles in body dysmorphic disorder
Labuschagne, Izelle, Castle, David J., Dunai, Judith, Kyrios, Michael and Rossell, Susan. (2010) An examination of delusional thinking and cognitive styles in body dysmorphic disorder. Australian and New Zealand Journal of Psychiatry. 44(8), pp. 706 - 712. https://doi.org/10.3109/00048671003671007
Evidence for modulation of facial emotional processing bias during emotional expression decoding by serotonergic and noradrenergic antidepressants: An event-related potential (ERP) study
Kerestes, Rebecca, Labuschagne, Izelle, Croft, Rodney, O'Neill, Barry, Bhagwagar, Zubin M., Phan, K Luan and Nathan, Pradeep. (2009) Evidence for modulation of facial emotional processing bias during emotional expression decoding by serotonergic and noradrenergic antidepressants: An event-related potential (ERP) study. Psychopharmacology. 202(4), pp. 621 - 634. https://doi.org/10.1007/s00213-008-1340-3