Testing a longitudinal compensation model in premanifest Huntington's disease

Journal article

Gregory, Sarah, Long, Jeffrey D., Klöppel, Stefan, Razi, Adeel, Scheller, Elisa, Minkova, Lora, Johnson, Eileanoir B., Durr, Alexandra, Roos, Raymund A. C., Leavitt, Blair R., Mills, James A., Stout, Julie C., Scahill, Rachael I., Tabrizi, Sarah J., Rees, Geraint, the Track-On investigators and Labuschagne, Izelle*. (2018). Testing a longitudinal compensation model in premanifest Huntington's disease. Brain. 141(7), pp. 2156-2166. https://doi.org/10.1093/brain/awy122
AuthorsGregory, Sarah, Long, Jeffrey D., Klöppel, Stefan, Razi, Adeel, Scheller, Elisa, Minkova, Lora, Johnson, Eileanoir B., Durr, Alexandra, Roos, Raymund A. C., Leavitt, Blair R., Mills, James A., Stout, Julie C., Scahill, Rachael I., Tabrizi, Sarah J., Rees, Geraint, the Track-On investigators and Labuschagne, Izelle*
Abstract

The initial stages of neurodegeneration are commonly marked by normal levels of cognitive and motor performance despite the presence of structural brain pathology. Compensation is widely assumed to account for this preserved behaviour, but despite the apparent simplicity of such a concept, it has proven incredibly difficult to demonstrate such a phenomenon and distinguish it from disease-related pathology. Recently, we developed a model of compensation whereby brain activation, behaviour and pathology, components key to understanding compensation, have specific longitudinal trajectories over three phases of progression. Here, we empirically validate our explicit mathematical model by testing for the presence of compensation over time in neurodegeneration. Huntington’s disease is an ideal model for examining longitudinal compensation in neurodegeneration as it is both monogenic and fully penetrant, so disease progression and potential compensation can be monitored many years prior to diagnosis. We defined our conditions for compensation as non-linear longitudinal trajectories of brain activity and performance in the presence of linear neuronal degeneration and applied our model of compensation to a large longitudinal cohort of premanifest and early-stage Huntington’s disease patients from the multisite Track-On HD study. Focusing on cognitive and motor networks, we integrated progressive volume loss, task and resting state functional MRI and cognitive and motor behaviour across three sequential phases of neurodegenerative disease progression, adjusted for genetic disease load. Multivariate linear mixed models were fitted and trajectories for each variable tested. Our conceptualization of compensation was partially realized across certain motor and cognitive networks at differing levels. We found several significant network trends that were more complex than that hypothesized in our model. These trends suggest changes to our theoretical model where the network effects are delayed relative to performance effects. There was evidence of compensation primarily in the prefrontal component of the cognitive network, with increased effective connectivity between the left and right dorsolateral prefrontal cortex. Having developed an operational model for the explicit testing of longitudinal compensation in neurodegeneration, it appears that general patterns of our framework are consistent with the empirical data. With the proposed modifications, our operational model of compensation can be used to test for both cross-sectional and longitudinal compensation in neurodegenerative disease with similar patterns to Huntington’s disease.

Keywordscompensation; neurodegeneration; Huntington’s disease; functional MRI
Year2018
JournalBrain
Journal citation141 (7), pp. 2156-2166
PublisherOxford University Press
ISSN0006-8950
Digital Object Identifier (DOI)https://doi.org/10.1093/brain/awy122
PubMed ID29788038
Scopus EID2-s2.0-85050817034
PubMed Central IDPMC6022638
Open accessPublished as ‘gold’ (paid) open access
Research or scholarlyResearch
Page range2156-2166
Publisher's version
License
File Access Level
Open
Output statusPublished
Publication dates
Online17 May 2018
Publication process dates
Accepted10 Mar 2018
Deposited11 Jan 2022
Additional information

Izelle Labuschagne is a member of the Track-On investigators.

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A comparison of executive function in Body Dysmorphic Disorder (BDD) and Obsessive-Compulsive Disorder (OCD)
Labuschagne, Izelle, Rossell, Susan, Dunai, Judith, Castle, David and Kyrios, Michael. (2013). A comparison of executive function in Body Dysmorphic Disorder (BDD) and Obsessive-Compulsive Disorder (OCD). Journal of Obsessive-Compulsive and Related Disorders. 2(3), pp. 257 - 262. https://doi.org/10.1016/j.jocrd.2013.05.003
Oxytocin enhances resting-state connectivity between amygdala and medial frontal cortex
Sripada, Chandra, Phan, Kinhluan, Labuschagne, Izelle, Welsh, Robert, Nathan, Pradeep and Wood, Amanda. (2013). Oxytocin enhances resting-state connectivity between amygdala and medial frontal cortex. International Journal of Neuropsychopharmacology (print). 16(2), pp. 255 - 260. https://doi.org/10.1017/S1461145712000533
Emotional face recognition deficits and medication effects in pre-manifest through stage-II Huntington's disease
Labuschagne, Izelle, Jones, Rebecca, Callaghan, Jenny, Whitehead, Daisy, Dumas, Eve, Say, Miranda, Hart, Ellen, Justo, Damian, Coleman, Allison, Dar Santos, Rachelle, Frost, Chris, Craufurd, David, Trabrizi, Sarah and Stout, Julie. (2013). Emotional face recognition deficits and medication effects in pre-manifest through stage-II Huntington's disease. Psychiatry Research. 207(1-2), pp. 118 - 126. https://doi.org/10.1016/j.psychres.2012.09.022
Emotional face recognition deficits and medication effects in pre-manifest through stage-II Huntington's disease
Labuschagne, Izelle, Jones, Rebecca, Callaghan, Jenny, Whitehead, Daisy, Dumas, Eve, Say, Miranda, Hart, Ellen, Justo, Damian, Coleman, Allison, Dar Santos, Rachelle, Frost, Chris, Craufurd, David, Tabrizi, Sarah and Stout, Julie. (2013). Emotional face recognition deficits and medication effects in pre-manifest through stage-II Huntington's disease. Psychiatry Research. 207(1-2), pp. 118 - 126. https://doi.org/10.1016/j.psychres.2012.09.022
Oxytocin enhances resting-state connectivity between amygdala and medial frontal cortex
Sripada, Chandra, Phan, Kinhluan, Labuschagne, Izelle, Welsh, Robert, Nathan, Pradeep and Wood, Amanda. (2013). Oxytocin enhances resting-state connectivity between amygdala and medial frontal cortex. International Journal of Neuropsychopharmacology. 16(2), pp. 255 - 260. https://doi.org/10.1017/S1461145712000533
Visual working memory impairment in premanifest gene-carriers and early Huntington's Disease
Dumas, Eve M., Say, Miranda Julia, Jones, Rebecca D., Labuschagne, Izelle, O'Regan, Alison M., Hart, Ellen P., van den Bogaard, Simon J. A., Queller, Sarah, Justo, Damian, Coleman, Allison J., dar Santos, Rachelle C., Durr, Alexandra, Leavitt, Blair R., Tabrizi, Sarah J., Roos, Raymund A. C. and Stout, Julie C.. (2012). Visual working memory impairment in premanifest gene-carriers and early Huntington's Disease. Journal of Huntington's Disease. 1(1), pp. 97 - 106. https://doi.org/10.3233/JHD-2012-120010
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, 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