Episodic Learning and Memory in Prodromal Huntington’s Disease: The Role of Multimodal Encoding and Selective Reminding
Affiliation(s)
1 Department of Neurobiology, Care Sciences and Society, Karolinska Institute, Stockholm, Sweden. 2 School of Medicine, The University of Queensland, Brisbane, Australia. 3 School of Health and Welfare, Jönköping University, Jönköping, Sweden.
1 Department of Neurobiology, Care Sciences and Society, Karolinska Institute, Stockholm, Sweden. 2 School of Medicine, The University of Queensland, Brisbane, Australia. 3 School of Health and Welfare, Jönköping University, Jönköping, Sweden.
ABSTRACT
This study investigated episodic memory in prodromal HD. Three groups were compared (N = 70): mutation carriers with less than 12.5 years to disease onset (n = 16), mutation carriers with 12.5 or more years to disease onset (n = 16), and noncarriers (n = 38). Episodic memory was assessed using the Fuld Object Memory Evaluation, which included multimodal presentation and selective reminding, and the Claeson-Dahl Learning Test which included verbal repeated presentation and recall trials. Both carrier groups demonstrated deficient episodic memory compared to noncarriers. The results suggest deficient episodic memory in prodromal HD, and that inconsistent retrieval contributes to these deficits. Multimodal presentation attenuates the deficits.
This study investigated episodic memory in prodromal HD. Three groups were compared (N = 70): mutation carriers with less than 12.5 years to disease onset (n = 16), mutation carriers with 12.5 or more years to disease onset (n = 16), and noncarriers (n = 38). Episodic memory was assessed using the Fuld Object Memory Evaluation, which included multimodal presentation and selective reminding, and the Claeson-Dahl Learning Test which included verbal repeated presentation and recall trials. Both carrier groups demonstrated deficient episodic memory compared to noncarriers. The results suggest deficient episodic memory in prodromal HD, and that inconsistent retrieval contributes to these deficits. Multimodal presentation attenuates the deficits.
KEYWORDS
Prodromal Huntington’s Disease, Fuld Object Memory Evaluation, Episodic Memory, Short-Term Memory, Neurodegenerative Diseases
Prodromal Huntington’s Disease, Fuld Object Memory Evaluation, Episodic Memory, Short-Term Memory, Neurodegenerative Diseases
Cite this paper
Robins Wahlin, T. , Wahlin, Å. and J. Byrne, G. (2015) Episodic Learning and Memory in Prodromal Huntington’s Disease: The Role of Multimodal Encoding and Selective Reminding. International Journal of Clinical Medicine, 6, 876-886. doi: 10.4236/ijcm.2015.611115.
Robins Wahlin, T. , Wahlin, Å. and J. Byrne, G. (2015) Episodic Learning and Memory in Prodromal Huntington’s Disease: The Role of Multimodal Encoding and Selective Reminding. International Journal of Clinical Medicine, 6, 876-886. doi: 10.4236/ijcm.2015.611115.
References
[1] Huntington’s Disease Collaborative Research Group (1993) A Novel Gene Containing a Trinucleotide Repeat That Is Expanded and Unstable on Huntington’s Disease Chromosomes. Cell, 72, 971-983.
http://dx.doi.org/10.1016/0092-8674(93)90585-E [2] Rubinsztein, D.C., Leggo, J., Coles, R., Almqvist, E., Biancalana, V., Cassiman, J.J., Chotai, K., Connarty, M., Crauford, D., Curtis, A., Curtis, D., Davidson, M.J., Differ, A.M., Dode, C., Dodge, A., Frontali, M., Ranen, N.G., Stine, O.C., Sherr, M., Abbott, M.H., Franz, M.L., Graham, C.A., Harper, P.S., Hedreen, J.C. and Hayden, M.R. (1996) Phenotypic Characterization of Individuals with 30-40 CAG Repeats in the Huntington Disease (HD) Gene Reveals HD Cases with 36 Repeats and Apparently Normal Elderly Individuals with 36-39 Repeats. American Journal of Human Genetics, 59, 16-22. [3] Bates, G., Harper, P.S. and Jones, L. (2002) Huntington’s Disease. 3rd Edition, Oxford University Press, Oxford. [4] Langbehn, D.R., Brinkman, R.R., Falush, D., Paulsen, J.S. and Hayden, M.R. (2004) A New Model for Prediction of the Age of Onset and Penetrance for Huntington’s Disease Based on CAG Length. Clinical Genetics, 65, 267-277.
http://10.1111/j.1399-0004.2004.00241.x [5] Roos, R.A., Vegtervan der Vlis, M., Hermans, J., Elshove, H.M., Moll, A.C., van de Kamp, J.J. and Bruyn, G.W. (1991) Age at Onset in Huntington’s Disease: Effect of Line of Inheritance and Patient’s Sex. Journal of Medical Genetics, 28, 515-519.
http://jmg.bmj.com
http://dx.doi.org/10.1136/jmg.28.8.515 [6] Gusella, J.F., Wexler, N.S., Conneally, P.M., Naylor, S.L., Anderson, M.A., Tanzi, R.E., Watkins, P.C., Ottina, K., Wallace, M.R., Sakaguchi, A.Y., Young, A.B., Shoulson, I., Bonilla, E. and Martin, J.B. (1983) A Polymorphic DNA Marker Genetically Linked to Huntington’s Disease. Nature, 306, 234-238.
http://dx.doi.org/10.1038/306234a0 [7] Brandt, J., Shpritz, B., Codori, A.-M., Margolis, R. and Rosenblatt, A. (2002) Neuropsychological Manifestations of the Genetic Mutation for Huntington’s Disease in Presymptomatic Individuals. Journal of the International Neuropsychological Society, 8, 918-924.
http://dx.doi.org/10.1017/S1355617702870060 [8] Larsson, M.U., Almkvist, O., Luszcz, M.A. and Robins Wahlin, T.-B. (2008) Phonemic Fluency Deficits in Asymptomatic Gene Carriers for Huntington’s Disease. Neuropsychology, 22, 596-605.
http://dx.doi.org/10.1037/0894-4105.22.5.596 [9] Paulsen, J.S., Langbehn, D.R., Stout, J.C., Aylward, E., Ross, C.A., Nance, M., Guttman, M., Johnson, S., MacDonald, M., Beglinger, L.J., Duff, K., Kayson, E., Biglan, K., Shoulson, I., Oakes, D. and Hayden, M. (2008) Detection of Huntington’s Disease Decades before Diagnosis: The Predict-HD Study. Journal of Neurology, Neurosurgery, and Psychiatry, 79, 874-880.
http://dx.doi.org/10.1136/jnnp.2007.128728 [10] Robins Wahlin, T.-B., Larsson, M. and Luszcz, M. (2010) WAIS-R Features of Preclinical Huntington’s Disease: Implications for Early Detection. Dementia and Geriatric Cognitive Disorders, 29, 342-350.
http://dx.doi.org/10.1159/000288775 [11] Robins Wahlin, T.-B., Lundin, A. and Dear, K. (2007) Early Cognitive Deficits in Swedish Gene Carriers of Huntington’s Disease. Neuropsychology, 21, 31-44.
http://dx.doi.org/10.1037/0894-4105.21.1.31 [12] Stout, J.C., Paulsen, J.S., Queller, S., Solomon, A.C., Whitlock, K.B., Campbell, J.C., Carlozzi, N., Duff, K., Beglinger, L.J., Langbehn, D.R., Johnson, S.A., Biglan, K.M. and Aylward, E.H. (2011) Neurocognitive Signs in Prodromal Huntington Disease. Neuropsychology, 25, 1-14.
http://dx.doi.org/10.1037/a0020937
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3017660/pdf/nihms224607.pdf [13] Harrington, D.L., Smith, M.M., Zhang, Y., Carlozzi, N.E. and Paulsen, J.S. (2012) Cognitive Domains That Predict Time to Diagnosis in Prodromal Huntington Disease. Journal of Neurology, Neurosurgery and Psychiatry, 83, 612-619.
http://jnnp.bmj.com/content/83/6/612.full.pdf
http://dx.doi.org/10.1136/jnnp-2011-301732 [14] Solomon, A.C., Stout, J.C., Johnson, S.A., Langbehn, D.R., Aylward, E.H., Brandt, J., Ross, C.A., Beglinger, L., Hayden, M.R., Kieburtz, K., Kayson, E., Julian-Baros, E., Duff, K., Guttman, M., Nance, M., Oakes, D., Shoulson, I., Penziner, E. and Paulsen, J.S. (2007) Verbal Episodic Memory Declines Prior to Diagnosis in Huntington’s Disease. Neuropsychologia, 45, 1767-1776.
http://dx.doi.org/10.1016/j.neuropsychologia.2006.12.015 [15] Butters, N., Sax, D., Montgomery, K. and Tarlow, S. (1978) Comparison of the Neuropsychological Deficits Associated with Early and Advanced Huntington’s Disease. Archives of Neurology, 35, 585-589.
http://search.ebscohost.com/login.aspx?direct=true&db=cmedm&AN=150836&site=ehost-live
http://dx.doi.org/10.1001/archneur.1978.00500330033006 [16] Montoya, A., Pelletier, M., Menear, M., Duplessis, E., Richer, F. and Lepage, M. (2006) Episodic Memory Impairment in Huntington’s Disease: A Meta-Analysis. Neuropsychologia, 44, 1984-1994.
http://dx.doi.org/10.1016/j.neuropsychologia.2006.01.015 [17] Caine, E.D., Hunt, R.D., Weingartner, H. and Ebert, M.H. (1978) Huntington’s Dementia. Clinical and Neuropsychological Features. Archives of General Psychiatry, 35, 377-384.
http://dx.doi.org/10.1001/archpsyc.1978.01770270127013 [18] Beglinger, L.J., O’Rourke, J.J., Wang, C., Langbehn, D.R., Duff, K. and Paulsen, J.S. (2010) Earliest Functional Declines in Huntington Disease. Psychiatry Research, 178, 414-418.
http://dx.doi.org/10.1016/j.psychres.2010.04.030
http://ac.els-cdn.com/S0165178110001897/1-s2.0-S0165178110001897-main.pdf?_tid=15748d52-cf18-11e4-89b8-00000aab0f02&acdnat=1426866487_8f95e4d5d9b7c9e335bdc65bc9ebbcfe [19] Dorsey, E.R., Beck, C.A., Darwin, K., Nichols, P., Brocht, A.F., Biglan, K.M. and Shoulson, I. (2013) Natural History of Huntington Disease. JAMA Neurology, 70, 1520-1530.
http://archneur.jamanetwork.com/data/Journals/NEUR/929441/noi130064.pdf [20] Williams, J.K., Hamilton, R., Nehl, C., McGonigal-Kenney, M., Schutte, D.L., Sparbel, K., Birrer, E., Tripp-Reimer, T., Friedrich, R., Penziner, E., Jarmon, L. and Paulsen, J. (2007) No One Else Sees the Difference: “Family Members” Perceptions of Changes in Persons with Preclinical Huntington Disease. American Journal of Medical Genetics B Neuropsychiatric Genetics, 144, 636-641.
http://dx.doi.org/10.1002/ajmg.b.30479 [21] Zakzanis, K.K. (1998) The Subcortical Dementia of Huntington’s Disease. Journal of Clinical and Experimental Neuropsychology, 20, 565-578.
http://dx.doi.org/10.1076/jcen.20.4.565.1468 [22] Pillon, B., Deweer, B., Agid, Y. and Dubois, B. (1993) Explicit Memory in Alzheimer’s, Huntington’s, and Parkinson’s Diseases. Archives of Neurology, 50, 374-379.
http://dx.doi.org/10.1001/archneur.1993.00540040036010 [23] Fuld, P.A. (1980) Guaranteed Stimulus-Processing in the Evaluation of Memory and Learning. Cortex, 16, 255-271.
http://dx.doi.org/10.1016/S0010-9452(80)80061-X [24] Hill, R.D., Neely, A.S. and Backman, L. (1997) Predictors of Change on the Fuld Object Memory Evaluation in a Two-Year Longitudinal Study of Optimally Healthy Very Old Adults. Aging and Mental Health, 1, 140-148.
http://dx.doi.org/10.1080/13607869757236 [25] Wall, J.R., Deshpande, S.A., MacNei, S.E. and Lichtenberg, P.A. (1998) The Fuld Object Memory Evaluation, a Useful Tool in the Assessment of Urban Geriatric Patients. Clinical Gerontologist, 19, 39-49.
http://dx.doi.org/10.1300/J018v19n01_04 [26] Mastroberardino, S., Santangelo, V., Botta, F., Marucci, F. and Olivetti Belardinelli, M. (2008) Guaranteed Stimulus-Processing in the Evaluation of Memory and Learning. Cognitive Processing, 9, 69-76.
http://dx.doi.org/10.1007/s10339-007-0195-6 [27] Buschke, H. (1973) Selective Reminding for Analysis of Memory and Learning. Journal of Verbal Learning and Verbal Behavior, 12, 543-550.
http://dx.doi.org/10.1016/S0022-5371(73)80034-9 [28] Claeson, L.E., Esbjörnsson, E., Carlé, B.M. and Wahlbin, M. (1971) Claeson-Dahls inlärningstest för kliniskt bruk (Claeson-Dahl’s Learning Test). Psykologiförlaget AB, Stockholm. [29] Folstein, S.E., Jensen, B., Leigh, R.J. and Folstein, M.F. (1983) The Measurement of Abnormal Movement: Methods Developed for Huntington’s Disease. Neurobehavioral Toxicology and Teratology, 5, 605-609. [30] Robins Wahlin, T.-B., Bäckman, L., Lundin, A., Haegermark, A., Winblad, B. and Anvret, M. (2000) High Suicidal Ideation in Persons Testing for Huntington’s Disease. Acta Neurologica Scandinavica, 102, 150-161.
http://dx.doi.org/10.1034/j.1600-0404.2000.102003150.x [31] Langbehn, D.R., Hayden, M.R. and Paulsen, J.S. (2010) CAG-Repeat Length and the Age of Onset in Huntington Disease (HD): A Review and Validation Study of Statistical Approaches. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 9999B, 397-408.
http://dx.doi.org/10.1002/ajmg.b.30992 [32] Lezak, M.D., Howieson, D.B. and Loring, D.W. (2004) Neuropsychological Assessment. 4th Edition, Oxford University Press, New York. [33] Beck, A.T., Ward, C.H., Mendelson, M., Mock, J. and Erbaugh, J. (1961) An Inventory for Measuring Depression. Archives of General Psychiatry, 4, 561-571.
http://dx.doi.org/10.1001/archpsyc.1961.01710120031004 [34] Paulsen, J.S., Salmon, D.P., Monsch, A.U., Butters, N., Swenson, M.R. and Bondi, M.W. (1995) Discrimination of Cortical from Subcortical Dementias on the Basis of Memory and Problem-Solving Tests. Journal of Clinical Psychology, 51, 48-58.
http://dx.doi.org/10.1002/1097-4679(199501)51:1<48::AID-JCLP2270510109>3.0.CO;2-E [35] Butters, N., Wolfe, J., Martone, M., Granholm, E. and Cermak, L.S. (1985) Memory Disorders Associated with Huntington’s Disease: Verbal Recall, Verbal Recognition and Procedural Memory. Neuropsychologia, 23, 729-743.
http://dx.doi.org/10.1016/0028-3932(85)90080-6 [36] Lundervold, A.J. (1994) Characteristic Pattern of Verbal Memory Function in Patients with Huntington’s Disease. Scandinavian Journal of Psychology, 35, 38-47.
http://dx.doi.org/10.1111/j.1467-9450.1994.tb00931.x [37] Perry, R.J. and Hodges, J.R. (1996) Spectrum of Memory Dysfunction in Degenerative Disease. Current Opinion in Neurology, 9, 281-285.
http://dx.doi.org/10.1097/00019052-199608000-00007 [38] Bäckman, L. and Nilsson, L. (1985) Prerequisites for Lack of Age Differences in Memory Performance. Experimental Aging Research, 11, 67-73.
http://dx.doi.org/10.1080/03610738508259282 [39] Baddeley, A. (2003) Working Memory: Looking Back and Looking Forward. Nature Reviews Neuroscience, 4, 829-839.
http://dx.doi.org/10.1038/nrn1201 [40] Weible, J., Nuest, B., Welty, J., Pate, W. and Turner, M. (2002) Demonstrating the Effects of Presentation Rate on Aging Memory Using the California Verbal Learning Test (CVLT). Aging, Neuropsychology, and Cognition (Neuropsychology, Development and Cognition), 9, 38-47.
http://dx.doi.org/10.1076/anec.9.1.38.834 [41] Aylward, E.H., Sparks, B.F., Field, K.M., Yallapragada, V., Shpritz, B.D., Rosenblatt, A., Brandt, J., Gourley, L.M., Liang, K., Zhou, H., Margolis, R.L. and Ross, C.A. (2004) Onset and Rate of Striatal Atrophy in Preclinical Huntington Disease. Neurology, 63, 66-72.
http://dx.doi.org/10.1212/01.WNL.0000132965.14653.D1 [42] Bonner-Jackson, A., Long, J.D., Westervelt, H., Tremont, G., Aylward, E. and Paulsen, J.S. (2013) Cognitive Reserve and Brain Reserve in Prodromal Huntington’s Disease. Journal of the International Neuropsychological Society, 19, 739-750.
http://dx.doi.org/10.1017/S1355617713000507
http://journals.cambridge.org/download.php?file=%2FINS%2FINS19_07%2FS1355617713000507a.pdf&code=
0a2ccdf33aa4a88250aadfcbedad50cd [43] Aylward, E.H., Harrington, D.L., Mills, J.A., Nopoulos, P.C., Ross, C.A., Long, J.D., Liu, D., Westervelt, H.K. and Paulsen, J.S. (2013) Regional Atrophy Associated with Cognitive and Motor Function in Prodromal Huntington Disease. Journal of Huntingtons Disease, 2, 477-489.
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4412155/pdf/nihms640985.pdf [44] Montoya, A., Price, B.H., Menear, M. and Lepage, M. (2006) Brain Imaging and Cognitive Dysfunctions in Huntington’s Disease. Journal of Psychiatry & Neuroscience, 31, 21-29.
Copyright 2015, 8872147 Canada Inc. [45] Paulsen, J.S. (2009) Functional Imaging in Huntington’s Disease. Experimental Neurology, 216, 272-277.
http://www.sciencedirect.com/science/article/B6WFG-4V94X1C-1/2/46f187d39554216f33bec0cc0f9d2d04
http://dx.doi.org/10.1016/j.expneurol.2008.12.015 [46] Rosas, H.D., Hevelone, N.D., Zaleta, A.K., Greve, D.N., Salat, D.H. and Fischl, B. (2005) Regional Cortical Thinning in Preclinical Huntington Disease and Its Relationship to Cognition. Neurology, 65, 745-747.
http://dx.doi.org/10.1212/01.wnl.0000174432.87383.87 [47] Wolf, R.C., Vasic, N., Schonfeldt-Lecuona, C., Landwehrmeyer, G.B. and Ecker, D. (2007) Dorsolateral Prefrontal Cortex Dysfunction in Presymptomatic Huntington’s Disease: Evidence from Event-Related fMRI. Brain, 130, 2845.
http://dx.doi.org/10.1093/brain/awm210 [48] Wolf, R.C., Sambataro, F., Vasic, N., Schönfeldt-Lecuona, C., Ecker, D. and Landwehrmeyer, B. (2008) Aberrant Connectivity of Lateral Prefrontal Networks in Presymptomatic Huntington’s Disease. Experimental Neurology, 213, 137-144.
http://dx.doi.org/10.1016/j.expneurol.2008.05.017 [49] Wolf, R.C., Thomann, P.A., Thomann, A.K., Vasic, N., Wolf, N.D., Landwehrmeyer, G.B. and Orth, M. (2013) Brain Structure in Preclinical Huntington’s Disease: A Multi-Method Approach. Neuro-Degenerative Diseases, 12, 13-22.
http://www.karger.com/Article/Pdf/338635
http://dx.doi.org/10.1159/000338635 [50] Wolf, R.C., Sambataro, F., Vasic, N., Wolf, N.D., Thomann, P.A., Landwehrmeyer, G.B. and Orth, M. (2014) Longitudinal Task-Negative Network Analyses in Preclinical Huntington’s Disease. European Archives of Psychiatry and Clinical Neuroscience, 264, 493-505.
http://www.ncbi.nlm.nih.gov/pubmed/24071913
http://dx.doi.org/10.1007/s00406-013-0447-7 [51] Dogan, I., Eickhoff, S.B., Schulz, J.B., Shah, N.J., Laird, A.R., Fox, P.T. and Reetz, K. (2013) Consistent Neurodegeneration and Its Association with Clinical Progression in Huntington’s Disease: A Coordinate-Based Meta-Analysis. Neuro-Degenerative Diseases, 12, 23-35.
http://www.karger.com/Article/Pdf/339528
http://dx.doi.org/10.1159/000339528 [52] Paulsen, J.S., Long, J.D., Johnson, H.J., Aylward, E.H., Ross, C.A., Williams, J.K., Nance, M.A., Erwin, C.J., Westervelt, H.J., Harrington, D.L., Bockholt, H.J., Zhang, Y., McCusker, E.A., Chiu, E.M. and Panegyres, P.K. (2014) Clinical and Biomarker Changes in Premanifest Huntington Disease Show Trial Feasibility: A Decade of the PREDICT-HD Study. Frontiers in Aging Neuroscience, 6, 78.
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4000999/pdf/fnagi-06-00078.pdf
http://dx.doi.org/10.3389/fnagi.2014.00078 [53] Robins Wahlin, T.-B. and Byrne, G.J. (2012) Cognition in Huntington’s Disease. In: Tunali, N.E., Ed., Huntington’s Disease—Core Concepts and Current Advances, InTech, Rijeka, 175-200.
http://www.intechopen.com/articles/show/title/cognition-in-huntington-s-disease [54] Beatty, W.W., Krull, K.R., Wilbanks, S.L., Blanco, C.R., Hames, K.A. and Paul, R.H. (1996) Further Validation of Constructs from the Selective Reminding Test. Journal of Clinical and Experimental Neuropsychology, 18, 52-55.
http://dx.doi.org/10.1080/01688639608408261 [55] Biringer, E., Rongve, A. and Lund, A. (2009) A Review of Modern Antidepressants Effects on Neurocognitive Function. Current Psychiatry Reviews, 5, 164-174.
http://dx.doi.org/10.2174/157340009788971137 [56] Kremer, B., Almqvist, E., Theilmann, J., Spence, N., Telenius, H., Goldberg, Y.P. and Hayden, M.R. (1995) Sex-Dependent Mechanisms for Expansions and Contractions of the CAG Repeat on Affected Huntington Disease Chromosomes. American Journal of Human Genetics, 57, 343-350.
http://www.ncbi.nlm.nih.gov
[1] Huntington’s Disease Collaborative Research Group (1993) A Novel Gene Containing a Trinucleotide Repeat That Is Expanded and Unstable on Huntington’s Disease Chromosomes. Cell, 72, 971-983.
http://dx.doi.org/10.1016/0092-8674(93)90585-E [2] Rubinsztein, D.C., Leggo, J., Coles, R., Almqvist, E., Biancalana, V., Cassiman, J.J., Chotai, K., Connarty, M., Crauford, D., Curtis, A., Curtis, D., Davidson, M.J., Differ, A.M., Dode, C., Dodge, A., Frontali, M., Ranen, N.G., Stine, O.C., Sherr, M., Abbott, M.H., Franz, M.L., Graham, C.A., Harper, P.S., Hedreen, J.C. and Hayden, M.R. (1996) Phenotypic Characterization of Individuals with 30-40 CAG Repeats in the Huntington Disease (HD) Gene Reveals HD Cases with 36 Repeats and Apparently Normal Elderly Individuals with 36-39 Repeats. American Journal of Human Genetics, 59, 16-22. [3] Bates, G., Harper, P.S. and Jones, L. (2002) Huntington’s Disease. 3rd Edition, Oxford University Press, Oxford. [4] Langbehn, D.R., Brinkman, R.R., Falush, D., Paulsen, J.S. and Hayden, M.R. (2004) A New Model for Prediction of the Age of Onset and Penetrance for Huntington’s Disease Based on CAG Length. Clinical Genetics, 65, 267-277.
http://10.1111/j.1399-0004.2004.00241.x [5] Roos, R.A., Vegtervan der Vlis, M., Hermans, J., Elshove, H.M., Moll, A.C., van de Kamp, J.J. and Bruyn, G.W. (1991) Age at Onset in Huntington’s Disease: Effect of Line of Inheritance and Patient’s Sex. Journal of Medical Genetics, 28, 515-519.
http://jmg.bmj.com
http://dx.doi.org/10.1136/jmg.28.8.515 [6] Gusella, J.F., Wexler, N.S., Conneally, P.M., Naylor, S.L., Anderson, M.A., Tanzi, R.E., Watkins, P.C., Ottina, K., Wallace, M.R., Sakaguchi, A.Y., Young, A.B., Shoulson, I., Bonilla, E. and Martin, J.B. (1983) A Polymorphic DNA Marker Genetically Linked to Huntington’s Disease. Nature, 306, 234-238.
http://dx.doi.org/10.1038/306234a0 [7] Brandt, J., Shpritz, B., Codori, A.-M., Margolis, R. and Rosenblatt, A. (2002) Neuropsychological Manifestations of the Genetic Mutation for Huntington’s Disease in Presymptomatic Individuals. Journal of the International Neuropsychological Society, 8, 918-924.
http://dx.doi.org/10.1017/S1355617702870060 [8] Larsson, M.U., Almkvist, O., Luszcz, M.A. and Robins Wahlin, T.-B. (2008) Phonemic Fluency Deficits in Asymptomatic Gene Carriers for Huntington’s Disease. Neuropsychology, 22, 596-605.
http://dx.doi.org/10.1037/0894-4105.22.5.596 [9] Paulsen, J.S., Langbehn, D.R., Stout, J.C., Aylward, E., Ross, C.A., Nance, M., Guttman, M., Johnson, S., MacDonald, M., Beglinger, L.J., Duff, K., Kayson, E., Biglan, K., Shoulson, I., Oakes, D. and Hayden, M. (2008) Detection of Huntington’s Disease Decades before Diagnosis: The Predict-HD Study. Journal of Neurology, Neurosurgery, and Psychiatry, 79, 874-880.
http://dx.doi.org/10.1136/jnnp.2007.128728 [10] Robins Wahlin, T.-B., Larsson, M. and Luszcz, M. (2010) WAIS-R Features of Preclinical Huntington’s Disease: Implications for Early Detection. Dementia and Geriatric Cognitive Disorders, 29, 342-350.
http://dx.doi.org/10.1159/000288775 [11] Robins Wahlin, T.-B., Lundin, A. and Dear, K. (2007) Early Cognitive Deficits in Swedish Gene Carriers of Huntington’s Disease. Neuropsychology, 21, 31-44.
http://dx.doi.org/10.1037/0894-4105.21.1.31 [12] Stout, J.C., Paulsen, J.S., Queller, S., Solomon, A.C., Whitlock, K.B., Campbell, J.C., Carlozzi, N., Duff, K., Beglinger, L.J., Langbehn, D.R., Johnson, S.A., Biglan, K.M. and Aylward, E.H. (2011) Neurocognitive Signs in Prodromal Huntington Disease. Neuropsychology, 25, 1-14.
http://dx.doi.org/10.1037/a0020937
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3017660/pdf/nihms224607.pdf [13] Harrington, D.L., Smith, M.M., Zhang, Y., Carlozzi, N.E. and Paulsen, J.S. (2012) Cognitive Domains That Predict Time to Diagnosis in Prodromal Huntington Disease. Journal of Neurology, Neurosurgery and Psychiatry, 83, 612-619.
http://jnnp.bmj.com/content/83/6/612.full.pdf
http://dx.doi.org/10.1136/jnnp-2011-301732 [14] Solomon, A.C., Stout, J.C., Johnson, S.A., Langbehn, D.R., Aylward, E.H., Brandt, J., Ross, C.A., Beglinger, L., Hayden, M.R., Kieburtz, K., Kayson, E., Julian-Baros, E., Duff, K., Guttman, M., Nance, M., Oakes, D., Shoulson, I., Penziner, E. and Paulsen, J.S. (2007) Verbal Episodic Memory Declines Prior to Diagnosis in Huntington’s Disease. Neuropsychologia, 45, 1767-1776.
http://dx.doi.org/10.1016/j.neuropsychologia.2006.12.015 [15] Butters, N., Sax, D., Montgomery, K. and Tarlow, S. (1978) Comparison of the Neuropsychological Deficits Associated with Early and Advanced Huntington’s Disease. Archives of Neurology, 35, 585-589.
http://search.ebscohost.com/login.aspx?direct=true&db=cmedm&AN=150836&site=ehost-live
http://dx.doi.org/10.1001/archneur.1978.00500330033006 [16] Montoya, A., Pelletier, M., Menear, M., Duplessis, E., Richer, F. and Lepage, M. (2006) Episodic Memory Impairment in Huntington’s Disease: A Meta-Analysis. Neuropsychologia, 44, 1984-1994.
http://dx.doi.org/10.1016/j.neuropsychologia.2006.01.015 [17] Caine, E.D., Hunt, R.D., Weingartner, H. and Ebert, M.H. (1978) Huntington’s Dementia. Clinical and Neuropsychological Features. Archives of General Psychiatry, 35, 377-384.
http://dx.doi.org/10.1001/archpsyc.1978.01770270127013 [18] Beglinger, L.J., O’Rourke, J.J., Wang, C., Langbehn, D.R., Duff, K. and Paulsen, J.S. (2010) Earliest Functional Declines in Huntington Disease. Psychiatry Research, 178, 414-418.
http://dx.doi.org/10.1016/j.psychres.2010.04.030
http://ac.els-cdn.com/S0165178110001897/1-s2.0-S0165178110001897-main.pdf?_tid=15748d52-cf18-11e4-89b8-00000aab0f02&acdnat=1426866487_8f95e4d5d9b7c9e335bdc65bc9ebbcfe [19] Dorsey, E.R., Beck, C.A., Darwin, K., Nichols, P., Brocht, A.F., Biglan, K.M. and Shoulson, I. (2013) Natural History of Huntington Disease. JAMA Neurology, 70, 1520-1530.
http://archneur.jamanetwork.com/data/Journals/NEUR/929441/noi130064.pdf [20] Williams, J.K., Hamilton, R., Nehl, C., McGonigal-Kenney, M., Schutte, D.L., Sparbel, K., Birrer, E., Tripp-Reimer, T., Friedrich, R., Penziner, E., Jarmon, L. and Paulsen, J. (2007) No One Else Sees the Difference: “Family Members” Perceptions of Changes in Persons with Preclinical Huntington Disease. American Journal of Medical Genetics B Neuropsychiatric Genetics, 144, 636-641.
http://dx.doi.org/10.1002/ajmg.b.30479 [21] Zakzanis, K.K. (1998) The Subcortical Dementia of Huntington’s Disease. Journal of Clinical and Experimental Neuropsychology, 20, 565-578.
http://dx.doi.org/10.1076/jcen.20.4.565.1468 [22] Pillon, B., Deweer, B., Agid, Y. and Dubois, B. (1993) Explicit Memory in Alzheimer’s, Huntington’s, and Parkinson’s Diseases. Archives of Neurology, 50, 374-379.
http://dx.doi.org/10.1001/archneur.1993.00540040036010 [23] Fuld, P.A. (1980) Guaranteed Stimulus-Processing in the Evaluation of Memory and Learning. Cortex, 16, 255-271.
http://dx.doi.org/10.1016/S0010-9452(80)80061-X [24] Hill, R.D., Neely, A.S. and Backman, L. (1997) Predictors of Change on the Fuld Object Memory Evaluation in a Two-Year Longitudinal Study of Optimally Healthy Very Old Adults. Aging and Mental Health, 1, 140-148.
http://dx.doi.org/10.1080/13607869757236 [25] Wall, J.R., Deshpande, S.A., MacNei, S.E. and Lichtenberg, P.A. (1998) The Fuld Object Memory Evaluation, a Useful Tool in the Assessment of Urban Geriatric Patients. Clinical Gerontologist, 19, 39-49.
http://dx.doi.org/10.1300/J018v19n01_04 [26] Mastroberardino, S., Santangelo, V., Botta, F., Marucci, F. and Olivetti Belardinelli, M. (2008) Guaranteed Stimulus-Processing in the Evaluation of Memory and Learning. Cognitive Processing, 9, 69-76.
http://dx.doi.org/10.1007/s10339-007-0195-6 [27] Buschke, H. (1973) Selective Reminding for Analysis of Memory and Learning. Journal of Verbal Learning and Verbal Behavior, 12, 543-550.
http://dx.doi.org/10.1016/S0022-5371(73)80034-9 [28] Claeson, L.E., Esbjörnsson, E., Carlé, B.M. and Wahlbin, M. (1971) Claeson-Dahls inlärningstest för kliniskt bruk (Claeson-Dahl’s Learning Test). Psykologiförlaget AB, Stockholm. [29] Folstein, S.E., Jensen, B., Leigh, R.J. and Folstein, M.F. (1983) The Measurement of Abnormal Movement: Methods Developed for Huntington’s Disease. Neurobehavioral Toxicology and Teratology, 5, 605-609. [30] Robins Wahlin, T.-B., Bäckman, L., Lundin, A., Haegermark, A., Winblad, B. and Anvret, M. (2000) High Suicidal Ideation in Persons Testing for Huntington’s Disease. Acta Neurologica Scandinavica, 102, 150-161.
http://dx.doi.org/10.1034/j.1600-0404.2000.102003150.x [31] Langbehn, D.R., Hayden, M.R. and Paulsen, J.S. (2010) CAG-Repeat Length and the Age of Onset in Huntington Disease (HD): A Review and Validation Study of Statistical Approaches. American Journal of Medical Genetics Part B: Neuropsychiatric Genetics, 9999B, 397-408.
http://dx.doi.org/10.1002/ajmg.b.30992 [32] Lezak, M.D., Howieson, D.B. and Loring, D.W. (2004) Neuropsychological Assessment. 4th Edition, Oxford University Press, New York. [33] Beck, A.T., Ward, C.H., Mendelson, M., Mock, J. and Erbaugh, J. (1961) An Inventory for Measuring Depression. Archives of General Psychiatry, 4, 561-571.
http://dx.doi.org/10.1001/archpsyc.1961.01710120031004 [34] Paulsen, J.S., Salmon, D.P., Monsch, A.U., Butters, N., Swenson, M.R. and Bondi, M.W. (1995) Discrimination of Cortical from Subcortical Dementias on the Basis of Memory and Problem-Solving Tests. Journal of Clinical Psychology, 51, 48-58.
http://dx.doi.org/10.1002/1097-4679(199501)51:1<48::AID-JCLP2270510109>3.0.CO;2-E [35] Butters, N., Wolfe, J., Martone, M., Granholm, E. and Cermak, L.S. (1985) Memory Disorders Associated with Huntington’s Disease: Verbal Recall, Verbal Recognition and Procedural Memory. Neuropsychologia, 23, 729-743.
http://dx.doi.org/10.1016/0028-3932(85)90080-6 [36] Lundervold, A.J. (1994) Characteristic Pattern of Verbal Memory Function in Patients with Huntington’s Disease. Scandinavian Journal of Psychology, 35, 38-47.
http://dx.doi.org/10.1111/j.1467-9450.1994.tb00931.x [37] Perry, R.J. and Hodges, J.R. (1996) Spectrum of Memory Dysfunction in Degenerative Disease. Current Opinion in Neurology, 9, 281-285.
http://dx.doi.org/10.1097/00019052-199608000-00007 [38] Bäckman, L. and Nilsson, L. (1985) Prerequisites for Lack of Age Differences in Memory Performance. Experimental Aging Research, 11, 67-73.
http://dx.doi.org/10.1080/03610738508259282 [39] Baddeley, A. (2003) Working Memory: Looking Back and Looking Forward. Nature Reviews Neuroscience, 4, 829-839.
http://dx.doi.org/10.1038/nrn1201 [40] Weible, J., Nuest, B., Welty, J., Pate, W. and Turner, M. (2002) Demonstrating the Effects of Presentation Rate on Aging Memory Using the California Verbal Learning Test (CVLT). Aging, Neuropsychology, and Cognition (Neuropsychology, Development and Cognition), 9, 38-47.
http://dx.doi.org/10.1076/anec.9.1.38.834 [41] Aylward, E.H., Sparks, B.F., Field, K.M., Yallapragada, V., Shpritz, B.D., Rosenblatt, A., Brandt, J., Gourley, L.M., Liang, K., Zhou, H., Margolis, R.L. and Ross, C.A. (2004) Onset and Rate of Striatal Atrophy in Preclinical Huntington Disease. Neurology, 63, 66-72.
http://dx.doi.org/10.1212/01.WNL.0000132965.14653.D1 [42] Bonner-Jackson, A., Long, J.D., Westervelt, H., Tremont, G., Aylward, E. and Paulsen, J.S. (2013) Cognitive Reserve and Brain Reserve in Prodromal Huntington’s Disease. Journal of the International Neuropsychological Society, 19, 739-750.
http://dx.doi.org/10.1017/S1355617713000507
http://journals.cambridge.org/download.php?file=%2FINS%2FINS19_07%2FS1355617713000507a.pdf&code=
0a2ccdf33aa4a88250aadfcbedad50cd [43] Aylward, E.H., Harrington, D.L., Mills, J.A., Nopoulos, P.C., Ross, C.A., Long, J.D., Liu, D., Westervelt, H.K. and Paulsen, J.S. (2013) Regional Atrophy Associated with Cognitive and Motor Function in Prodromal Huntington Disease. Journal of Huntingtons Disease, 2, 477-489.
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4412155/pdf/nihms640985.pdf [44] Montoya, A., Price, B.H., Menear, M. and Lepage, M. (2006) Brain Imaging and Cognitive Dysfunctions in Huntington’s Disease. Journal of Psychiatry & Neuroscience, 31, 21-29.
Copyright 2015, 8872147 Canada Inc. [45] Paulsen, J.S. (2009) Functional Imaging in Huntington’s Disease. Experimental Neurology, 216, 272-277.
http://www.sciencedirect.com/science/article/B6WFG-4V94X1C-1/2/46f187d39554216f33bec0cc0f9d2d04
http://dx.doi.org/10.1016/j.expneurol.2008.12.015 [46] Rosas, H.D., Hevelone, N.D., Zaleta, A.K., Greve, D.N., Salat, D.H. and Fischl, B. (2005) Regional Cortical Thinning in Preclinical Huntington Disease and Its Relationship to Cognition. Neurology, 65, 745-747.
http://dx.doi.org/10.1212/01.wnl.0000174432.87383.87 [47] Wolf, R.C., Vasic, N., Schonfeldt-Lecuona, C., Landwehrmeyer, G.B. and Ecker, D. (2007) Dorsolateral Prefrontal Cortex Dysfunction in Presymptomatic Huntington’s Disease: Evidence from Event-Related fMRI. Brain, 130, 2845.
http://dx.doi.org/10.1093/brain/awm210 [48] Wolf, R.C., Sambataro, F., Vasic, N., Schönfeldt-Lecuona, C., Ecker, D. and Landwehrmeyer, B. (2008) Aberrant Connectivity of Lateral Prefrontal Networks in Presymptomatic Huntington’s Disease. Experimental Neurology, 213, 137-144.
http://dx.doi.org/10.1016/j.expneurol.2008.05.017 [49] Wolf, R.C., Thomann, P.A., Thomann, A.K., Vasic, N., Wolf, N.D., Landwehrmeyer, G.B. and Orth, M. (2013) Brain Structure in Preclinical Huntington’s Disease: A Multi-Method Approach. Neuro-Degenerative Diseases, 12, 13-22.
http://www.karger.com/Article/Pdf/338635
http://dx.doi.org/10.1159/000338635 [50] Wolf, R.C., Sambataro, F., Vasic, N., Wolf, N.D., Thomann, P.A., Landwehrmeyer, G.B. and Orth, M. (2014) Longitudinal Task-Negative Network Analyses in Preclinical Huntington’s Disease. European Archives of Psychiatry and Clinical Neuroscience, 264, 493-505.
http://www.ncbi.nlm.nih.gov/pubmed/24071913
http://dx.doi.org/10.1007/s00406-013-0447-7 [51] Dogan, I., Eickhoff, S.B., Schulz, J.B., Shah, N.J., Laird, A.R., Fox, P.T. and Reetz, K. (2013) Consistent Neurodegeneration and Its Association with Clinical Progression in Huntington’s Disease: A Coordinate-Based Meta-Analysis. Neuro-Degenerative Diseases, 12, 23-35.
http://www.karger.com/Article/Pdf/339528
http://dx.doi.org/10.1159/000339528 [52] Paulsen, J.S., Long, J.D., Johnson, H.J., Aylward, E.H., Ross, C.A., Williams, J.K., Nance, M.A., Erwin, C.J., Westervelt, H.J., Harrington, D.L., Bockholt, H.J., Zhang, Y., McCusker, E.A., Chiu, E.M. and Panegyres, P.K. (2014) Clinical and Biomarker Changes in Premanifest Huntington Disease Show Trial Feasibility: A Decade of the PREDICT-HD Study. Frontiers in Aging Neuroscience, 6, 78.
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4000999/pdf/fnagi-06-00078.pdf
http://dx.doi.org/10.3389/fnagi.2014.00078 [53] Robins Wahlin, T.-B. and Byrne, G.J. (2012) Cognition in Huntington’s Disease. In: Tunali, N.E., Ed., Huntington’s Disease—Core Concepts and Current Advances, InTech, Rijeka, 175-200.
http://www.intechopen.com/articles/show/title/cognition-in-huntington-s-disease [54] Beatty, W.W., Krull, K.R., Wilbanks, S.L., Blanco, C.R., Hames, K.A. and Paul, R.H. (1996) Further Validation of Constructs from the Selective Reminding Test. Journal of Clinical and Experimental Neuropsychology, 18, 52-55.
http://dx.doi.org/10.1080/01688639608408261 [55] Biringer, E., Rongve, A. and Lund, A. (2009) A Review of Modern Antidepressants Effects on Neurocognitive Function. Current Psychiatry Reviews, 5, 164-174.
http://dx.doi.org/10.2174/157340009788971137 [56] Kremer, B., Almqvist, E., Theilmann, J., Spence, N., Telenius, H., Goldberg, Y.P. and Hayden, M.R. (1995) Sex-Dependent Mechanisms for Expansions and Contractions of the CAG Repeat on Affected Huntington Disease Chromosomes. American Journal of Human Genetics, 57, 343-350.
http://www.ncbi.nlm.nih.gov