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Cognitive Reserve and Brain Reserve in Prodromal Huntington's Disease

Published online by Cambridge University Press:  23 May 2013

Aaron Bonner-Jackson ,
Jeffrey D. Long ,
Holly Westervelt ,
Geoffrey Tremont ,
Elizabeth Aylward ,
Jane S. Paulsen  and
The PREDICT-HD Investigators and Coordinators of the Huntington Study Group
Aaron Bonner-Jackson
Affiliation:
Cleveland Clinic, Cleveland, Ohio
Jeffrey D. Long
Affiliation:
University of Iowa, Iowa City, Iowa
Holly Westervelt
Affiliation:
Rhode Island Hospital, Providence, Rhode Island Alpert Medical School of Brown University, Providence, Rhode Island
Geoffrey Tremont
Affiliation:
Rhode Island Hospital, Providence, Rhode Island Alpert Medical School of Brown University, Providence, Rhode Island
Elizabeth Aylward
Affiliation:
Seattle Children's Research Institute, Seattle, Washington
Jane S. Paulsen*
Affiliation:
University of Iowa, Iowa City, Iowa
*
Correspondence and reprint requests to: Jane S. Paulsen, 500 Newton Road, 1-305 MEB, Iowa City, IA 52242. E-mail: jane-paulsen@uiowa.edu
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Abstract

Huntington disease (HD) is associated with decline in cognition and progressive morphological changes in brain structures. Cognitive reserve may represent a mechanism by which disease-related decline may be delayed or slowed. The current study examined the relationship between cognitive reserve and longitudinal change in cognitive functioning and brain volumes among prodromal (gene expansion-positive) HD individuals. Participants were genetically confirmed individuals with prodromal HD enrolled in the PREDICT-HD study. Cognitive reserve was computed as the composite of performance on a lexical task estimating premorbid intellectual level, occupational status, and years of education. Linear mixed effects regression (LMER) was used to examine longitudinal changes on four cognitive measures and three brain volumes over approximately 6 years. Higher cognitive reserve was significantly associated with a slower rate of change on one cognitive measure (Trail Making Test, Part B) and slower rate of volume loss in two brain structures (caudate, putamen) for those estimated to be closest to motor disease onset. This relationship was not observed among those estimated to be further from motor disease onset. Our findings demonstrate a relationship between cognitive reserve and both a measure of executive functioning and integrity of certain brain structures in prodromal HD individuals. (JINS, 2013, 19, 1–12).

Keywords

Huntington diseaseProdromalCognitive reserveCognitionCaudatePutamen
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 19 , Issue 7 , August 2013 , pp. 739 - 750
Copyright
Copyright © The International Neuropsychological Society 2013 

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References

Alexander, G.E., Furey, M.L., Grady, C.L., Pietrini, P., Brady, D.R., Mentis, M.J., Schapiro, M.B. (1997). Association of premorbid intellectual function with cerebral metabolism in Alzheimer's disease: Implications for the cognitive reserve hypothesis. American Journal of Psychiatry, 154(2), 165–172.Google ScholarPubMed
Arenaza-Urquijo, E.M., Bosch, B., Sala-Llonch, R., Sole-Padulles, C., Junque, C., Fernandez-Espejo, D., Bartres-Faz, D. (2011). Specific anatomic associations between white matter integrity and cognitive reserve in normal and cognitively impaired elders. American Journal Geriatric Psychiatry, 19(1), 33–42. doi:10.1097/JGP.0b013e3181e448e1CrossRefGoogle ScholarPubMed
Aylward, E.H. (2007). Change in MRI striatal volumes as a biomarker in preclinical Huntington's disease. Brain Research Bulletin, 72(2-3), 152–158. doi:S0361-9230(06)00324-8 [pii] 10.1016/j.brainresbull.2006.10.028CrossRefGoogle ScholarPubMed
Aylward, E.H., Li, Q., Stine, O.C., Ranen, N., Sherr, M., Barta, P.E., Ross, C.A. (1997). Longitudinal change in basal ganglia volume in patients with Huntington's disease. Neurology, 48(2), 394–399.CrossRefGoogle ScholarPubMed
Aylward, E.H., Nopoulos, P.C., Ross, C.A., Langbehn, D.R., Pierson, R.K., Mills, J.A., Paulsen, J.S. (2011). Longitudinal change in regional brain volumes in prodromal Huntington disease. Journal of Neurology, Neurosurgery, & Psychiatry, 82(4), 405–410. doi:jnnp.2010.208264 [pii] 10.1136/jnnp.2010.208264CrossRefGoogle ScholarPubMed
Bachoud-Levi, A.C., Maison, P., Bartolomeo, P., Boisse, M.F., Dalla Barba, G., Ergis, A.M., Peschanski, M. (2001). Retest effects and cognitive decline in longitudinal follow-up of patients with early HD. Neurology, 56(8), 1052–1058.CrossRefGoogle ScholarPubMed
Bamford, K.A., Caine, E.D., Kido, D.K., Cox, C., Shoulson, I. (1995). A prospective evaluation of cognitive decline in early Huntington's disease: Functional and radiographic correlates. Neurology, 45(10), 1867–1873.CrossRefGoogle ScholarPubMed
Bates, D.M. (2011). lme4: Mixed-effects modeling with R. New York: Springer.Google Scholar
Beck, A.T., Steer, R.A., Brown, G.K. (1996). BDI-II, Beck depression inventory: Manual (2nd ed.). Boston: Harcourt Brace.Google Scholar
Beglinger, L.J., Duff, K., Allison, J., Theriault, D., O'Rourke, J.J.F., Leserman, A., Paulsen, J.S. (2010). Cognitive change in patients with Huntington disease on the Repeatable Battery for the Assessment of Neuropsychological Status. Journal of Clinical and Experimental Neuropsychology, 32, 573–578.CrossRefGoogle ScholarPubMed
Benedict, R.H., Morrow, S.A., Weinstock Guttman, B., Cookfair, D., Schretlen, D.J. (2010). Cognitive reserve moderates decline in information processing speed in multiple sclerosis patients. Journal of International Neuropsychology Society, 16(5), 829–835. doi:S1355617710000688 [pii] 10.1017/S1355617710000688CrossRefGoogle ScholarPubMed
Brandt, J., Bylsma, F.W., Aylward, E.H., Rothlind, J., Gow, C.A. (1995). Impaired source memory in Huntington's disease and its relation to basal ganglia atrophy. Journal of Clinical Experimental Neuropsychology, 17(6), 868–877. doi:10.1080/01688639508402436CrossRefGoogle ScholarPubMed
Burnham, K.P., Anderson, D.R. (2002). Model selection and multimodal inference. New York: Springer.Google Scholar
Campodonico, J.R., Codori, A.M., Brandt, J. (1996). Neuropsychological stability over two years in asymptomatic carriers of the Huntington's disease mutation. Journal of Neurology, Neurosurgery, & Psychiatry, 61(6), 621–624.CrossRefGoogle ScholarPubMed
Carlozzi, N.E., Stout, J.C., Mills, J.A., Duff, K., Beglinger, L.J., Aylward, E.H., … the PREDICT-HD Investigators of the Huntington Study Group. (2011). Estimating premorbid IQ in the prodromal phase of a neurodegenerative disease. The Clinical Neuropsychologist, 25, 757–777.CrossRefGoogle ScholarPubMed
Del Ser, T., Gonzalez-Montalvo, J.I., Martinez-Espinosa, S., Delgado-Villapalos, C., Bermejo, F. (1997). Estimation of premorbid intelligence in Spanish people with the Word Accentuation Test and its application to the diagnosis of dementia. Brain and Cognition, 33(3), 343–356. doi:S0278-2626(97)90877-0 [pii] 10.1006/brcg.1997.0877CrossRefGoogle Scholar
Fratiglioni, L., Wang, H.X. (2007). Brain reserve hypothesis in dementia. Journal of Alzheimers Disease, 12(1), 11–22.CrossRefGoogle ScholarPubMed
Fritsch, T., McClendon, M.J., Smyth, K.A., Ogrocki, P.K. (2002). Effects of educational attainment and occupational status on cognitive and functional decline in persons with Alzheimer-type dementia. International Psychogeriatrics, 14(4), 347–363.CrossRefGoogle ScholarPubMed
Goul, W.R., Brown, M. (1970). Effects of age and intelligence on trail making test performance and validity. Perceptual and Motor Skills, 30, 319–326.CrossRefGoogle ScholarPubMed
Grober, E., Sliwinski, M. (1991). Development and validation of a model for estimating premorbid verbal intelligence in the elderly. Journal of Clinical Experimental Neuropsychology, 13(6), 933–949. doi:10.1080/01688639108405109CrossRefGoogle Scholar
Hahn-Barma, V., Deweer, B., Durr, A., Dode, C., Feingold, J., Pillon, B., Dubois, B. (1998). Are cognitive changes the first symptoms of Huntington's disease? A study of gene carriers. Journal of Neurology, Neurosurgery, and Psychiatry, 64, 172–177.CrossRefGoogle ScholarPubMed
Ho, A.K., Sahakian, B.J., Brown, R.G., Barker, R.A., Hodges, J.R., Ane, M.N., Bodner, T. (2003). Profile of cognitive progression in early Huntington's disease. Neurology, 61(12), 1702–1706.CrossRefGoogle ScholarPubMed
Hobbs, N.Z., Barnes, J., Frost, C., Henley, S.M., Wild, E.J., Macdonald, K., Tabrizi, S.J. (2010). Onset and progression of pathologic atrophy in Huntington disease: A longitudinal MR imaging study. AJNR American Journal of Neuroradiology, 31(6), 1036–1041. doi:ajnr.A2018 [pii] 10.3174/ajnr.A2018CrossRefGoogle ScholarPubMed
Jurgens, C.K., van de Wiel, L., van Es, A.C., Grimbergen, Y.M., Witjes-Ane, M.N., van der Grond, J., Roos, R.A. (2008). Basal ganglia volume and clinical correlates in ‘preclinical’ Huntington's disease. Journal of Neurology, 255(11), 1785–1791. doi:10.1007/s00415-008-0050-4CrossRefGoogle ScholarPubMed
Lawrence, A.D., Hodges, J.R., Rosser, A.E., Kershaw, A., ffrench-Constant, C., Rubinsztein, D.C., Sahakian, B.J. (1998). Evidence for specific cognitive deficits in preclinical Huntington's disease. Brain, 121, 1329–1341.CrossRefGoogle ScholarPubMed
Lemiere, J., Decruyenaere, M., Evers-Kiebooms, G., Vandenbussche, E., Dom, R. (2004). Cognitive changes in patients with Huntington's disease (HD) and asymptomatic carriers of the HD mutation--a longitudinal follow-up study. Journal of Neurology, 251(8), 935–942. doi:10.1007/s00415-004-0461-9CrossRefGoogle Scholar
Long, J.D. (2011). Longitudinal data analysis for the behavioral sciences using R. Thousand Oaks, CA: Sage Publications Inc.Google Scholar
Lopez-Sendon, J.L., Royuela, A., Trigo, P., Orth, M., Lange, H., Reilmann, R., de Yebenes, J.G. (2011). What is the impact of education on Huntington's disease? Movement Disorders, 26(8), 1489–1495. doi:10.1002/mds.23385CrossRefGoogle ScholarPubMed
Magnotta, V.A., Harris, G., Andreasen, N.C., O'Leary, D.S., Yuh, W.T., Heckel, D. (2002). Structural MR image processing using the BRAINS2 toolbox. Computerized Medical Imaging and Graphics, 26(4), 251–264. doi:S0895611102000113 [pii]CrossRefGoogle ScholarPubMed
Mazzocchi-Jones, D., Dobrossy, M., Dunnett, S.B. (2011). Environmental enrichment facilitates long-term potentiation in embryonic striatal grafts. Neurorehabilitation and Neural Repair, 25, 548–557.CrossRefGoogle ScholarPubMed
Montoya, A., Price, B.H., Menear, M., Lepage, M. (2006). Brain imaging and cognitive dysfunctions in Huntington's disease. Journal of Psychiatry and Neuroscience, 31(1), 21–29.Google ScholarPubMed
Nelson, H.E., Willison, J. (1991). The National Adult Reading Test (NART): Test manual (2nd ed.). Windsor, England: NFER Nelson.Google Scholar
Nithianantharajah, J., Barkus, C., Vijiaratnam, N., Clement, O., Hannan, A.J. (2009). Modeling brain reserve: Experience-dependent neuronal plasticity in healthy and Huntington's disease transgenic mice. American Journal of Geriaticr Psychiatry, 17(3), 196–209. doi:10.1097/JGP.0b013e318196a632 00019442-200903000-00004 [pii]CrossRefGoogle ScholarPubMed
Pang, T.Y., Stam, N.C., Nithianantharajah, J., Howard, M.L., Hannan, A.J. (2006). Differential effects of voluntary physical exercise on behavioral and brain-dervied neurotrophic factor expression deficits in Huntington's disease transgenic mice. Neuroscience, 141, 569–584.CrossRefGoogle ScholarPubMed
Paulsen, J.S., Hayden, M., Stout, J.C., Langbehn, D.R., Aylward, E., Ross, C.A., … Predict-HD Investigators of the Huntington Study Group. (2006). Preparing for preventative clinical trials: The Predict-HD study. Archives of Neurology, 63, 883–890.CrossRefGoogle ScholarPubMed
Paulsen, J.S., Langbehn, D.R., Stout, J.C., Aylward, E., Ross, C.A., Nance, M., Hayden, M. (2008). Detection of Huntington's disease decades before diagnosis: The Predict-HD study. Journal of Neurology, Neurosurgery, & Psychiatry, 79(8), 874–880. doi:jnnp.2007.128728 [pii] 10.1136/jnnp.2007.128728CrossRefGoogle ScholarPubMed
Paulsen, J.S., Zhao, H., Stout, J.C., Brinkman, R.R., Guttman, M., Ross, C.A., The Huntington Study Group. (2001). Clinical markers of early disease in persons near onset of Huntington's disease. Neurology, 57, 658–662.CrossRefGoogle ScholarPubMed
Pierson, R.K., Johnson, H.J., Harris, G., Keefe, H., Paulsen, J., Andreasen, N.C., Magnotta, V.A. (2011). Fully automated analysis using BRAINS: AutoWorkup. Neuroimage, 54, 328–336.CrossRefGoogle ScholarPubMed
Powell, S., Magnotta, V.A., Johnson, H., Jammalamadaka, V.K., Pierson, R., Andreasen, N.C. (2008). Registration and machine learning-based automated segmentation of subcortical and cerebellar brain structures. Neuroimage, 39(1), 238–247. doi:S1053-8119(07)00713-6 [pii] 10.1016/j.neuroimage.2007.05.063CrossRefGoogle ScholarPubMed
Reading, S.A., Yassa, M.A., Bakker, A., Dziorny, A.C., Gourley, L.M., Yallapragada, V., Ross, C.A. (2005). Regional white matter change in pre-symptomatic Huntington's disease: A diffusion tensor imaging study. Psychiatry Research, 140(1), 55–62. doi:S0925-4927(05)00106-X [pii] 10.1016/j.pscychresns.2005.05.011CrossRefGoogle ScholarPubMed
Reitan, R.M. (1958). Validity of the trail making test as an indicator of organic brain damage. Perceptual and Motor Skills, 8, 271–276.CrossRefGoogle Scholar
Roe, C.M., Xiong, C., Miller, J.P., Morris, J.C. (2007). Education and Alzheimer disease without dementia: Support for the cognitive reserve hypothesis. Neurology, 68(3), 223–228. doi:68/3/223 [pii] 10.1212/01.wnl.0000251303.50459.8aCrossRefGoogle ScholarPubMed
Rupp, J., Blekher, T., Jackson, J., Beristain, X., Marshall, J., Hui, S., Foroud, T. (2010). Progression in prediagnostic Huntington disease. Journal of Neurology, Neurosurgery & Psychiatry, 81(4), 379–384. doi:jnnp.2009.176982 [pii] 10.1136/jnnp.2009.176982CrossRefGoogle ScholarPubMed
Salthouse, T.A. (2011). What cognitive abilities are involved in trail-making performance? Intelligence, 39, 222–232.CrossRefGoogle ScholarPubMed
Schmidt, K., Metzler, P. (1992). Wortschatztest (WST). Weinheim: Beltz Verlag.Google Scholar
Smith, A. (1991). Symbol Digit Modalities Test. Los Angeles: Western Psychological Services.Google Scholar
Smith, M.M., Mills, J.A., Epping, E.A., Westervelt, H.J., Paulsen, J.S., …The PREDICT-HD Investigators and Coordinators of the Huntington Study Group. (2012). Depressive symptom severity is related to poorer cognitive performance in prodromal Huntington disease. Neuropsychology, 26, 664–669.CrossRefGoogle ScholarPubMed
Snowden, J.S., Craufurd, D., Thompson, J., Neary, D. (2002). Psychomotor, executive, and memory function in preclinical Huntington's disease. Journal of Clinical and Experimental Neuropsychology, 24(2), 133–145.CrossRefGoogle ScholarPubMed
Solomon, A.C., Stout, J.C., Weaver, M., Queller, S., Tomusk, A., Whitlock, K.B., Foroud, T. (2008). Ten-year rate of longitudinal change in neurocognitive and motor function in prediagnosis Huntington disease. Movement Disorders, 23(13), 1830–1836. doi:10.1002/mds.22097CrossRefGoogle ScholarPubMed
Starkstein, S.E., Brandt, J., Folstein, S., Strauss, M., Berthier, M.L., Pearlson, G.D., Folstein, M. (1988). Neuropsychological and neuroradiological correlates in Huntington's disease. Journal of Neurology, Neurosurgery, & Psychiatry, 51(10), 1259–1263.CrossRefGoogle ScholarPubMed
Stern, Y. (2009). Cognitive reserve. Neuropsychologia, 47(10), 2015–2028. doi:S0028-3932(09)00123-7 [pii] 10.1016/j.neuropsychologia.2009.03.004CrossRefGoogle ScholarPubMed
Stout, J.C., Jones, R., Labuschagne, I., O'Regan, A.M., Say, M.J., Dumas, E.M., Frost, C. (2012). Evaluation of longitudinal 12 and 24 month cognitive outcomes in premanifest and early Huntington's disease. Journal of Neurology, Neurosurgery, and Psychiatry, 83, 687–694.CrossRefGoogle ScholarPubMed
Stout, J.C., Paulsen, J.S., Queller, S., Solomon, A.C., Whitlock, K.B., Campbell, J.C., Aylward, E.H. (2011). Neurocognitive signs in prodromal Huntington disease. Neuropsychology, 25(1), 1–14. doi:2010-20839-001 [pii] 10.1037/a0020937CrossRefGoogle ScholarPubMed
Stout, J.C., Weaver, M., Solomon, A.C., Queller, S., Hui, S., Johnson, S.A., Foroud, T. (2007). Are cognitive changes progressive in prediagnostic HD? Cognitive and Behavioral Neurology, 20(4), 212–218. doi:10.1097/WNN.0b013e31815cfef8 00146965-200712000-00002 [pii]CrossRefGoogle ScholarPubMed
Stroop, J.R. (1935). Studies of interference and serial verbal reactions. Journal of Experimental Psychology, 18, 643–662.CrossRefGoogle Scholar
Sumowski, J.F., Wylie, G.R., Chiaravalloti, N., DeLuca, J. (2010). Intellectual enrichment lessens the effect of brain atrophy on learning and memory in multiple sclerosis. Neurology, 74(24), 1942–1945. doi:74/24/1942 [pii] 10.1212/WNL.0b013e3181e396beCrossRefGoogle ScholarPubMed
Tabrizi, S.J., Scahill, R.I., Durr, A., Roos, R.A., Leavitt, B.R., Jones, R., … TRACK-HD Investigators. (2011). Biological and clinical changes in premanifest and early stage Huntington's disease in the TRACK-HD study: The 12-month longitudinal analysis. Lancet Neurology, 10, 31–42.CrossRefGoogle Scholar
Teipel, S.J., Meindl, T., Wagner, M., Kohl, T., Burger, K., Reiser, M.F., Hampel, H. (2009). White matter microstructure in relation to education in aging and Alzheimer's disease. Journal of Alzheimers Disease, 17(3), 571–583. doi:J4213346J64N534X [pii] 10.3233/JAD-2009-1077CrossRefGoogle ScholarPubMed
Zhang, Y., Long, J.D., Mills, J.A., Warner, J.H., Lu, W., Paulsen, J.S. (2011). Indexing disease progression at study entry with individuals at-risk for Huntington disease. American Journal of Medical Genetetics Part B: Neuropsychiatric Genetics, 156B(7), 751–763. doi:10.1002/ajmg.b.31232CrossRefGoogle ScholarPubMed