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Visuospatial Processing Deficits Linked to Posterior Brain Regions in Premanifest and Early Stage Huntington’s Disease

Published online by Cambridge University Press:  23 May 2016

Izelle Labuschagne ,
Amy Mulick Cassidy ,
Rachael I. Scahill ,
Eileanoir B. Johnson ,
Elin Rees ,
Alison O’Regan ,
Sarah Queller ,
Chris Frost ,
Blair R. Leavitt  and
Alexandra Dürr
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Izelle Labuschagne
Affiliation:
School of Psychological Sciences, Monash University, Clayton, Victoria, Australia School of Psychology, Australian Catholic University, Melbourne, Victoria, Australia
Amy Mulick Cassidy
Affiliation:
Department of Medical Statistics, London School of Hygiene & Tropical Medicine, London, United Kingdom
Rachael I. Scahill
Affiliation:
UCL Institute of Neurology, University College London, United Kingdom
Eileanoir B. Johnson
Affiliation:
UCL Institute of Neurology, University College London, United Kingdom
Elin Rees
Affiliation:
UCL Institute of Neurology, University College London, United Kingdom
Alison O’Regan
Affiliation:
School of Psychological Sciences, Monash University, Clayton, Victoria, Australia
Sarah Queller
Affiliation:
Queller Consulting, Dunedin, Florida
Chris Frost
Affiliation:
Department of Medical Statistics, London School of Hygiene & Tropical Medicine, London, United Kingdom
Blair R. Leavitt
Affiliation:
Centre for Molecular Medicine and Therapeutics, Department of Medical Genetics, University of British Columbia, Vancouver, BC, Canada
Alexandra Dürr
Affiliation:
Department of Genetics and Cytogenetics, and INSERMUMR S679, APHP, ICM Institute, Hôpital de la Salpêtrière, Paris, France
Raymond Roos
Affiliation:
Department of Neurology, Leiden University Medical Centre, Leiden, Netherlands
Gail Owen
Affiliation:
UCL Institute of Neurology, University College London, United Kingdom
Beth Borowsky
Affiliation:
CHDI Management/CHDI Foundation, Princeton, New Jersey
Sarah J. Tabrizi
Affiliation:
UCL Institute of Neurology, University College London, United Kingdom
Julie C. Stout*
Affiliation:
School of Psychological Sciences, Monash University, Clayton, Victoria, Australia Monash Institute of Cognitive and Clinical Neurosciences, Monash University, Clayton, Victoria, Australia
*
Correspondence and reprint requests to: Julie C. Stout, School of Psychological Sciences, Faculty of Medicine, Nursing and Health Sciences, Monash University, Melbourne, Victoria, Australia 3800. E-mail: julie.stout@monash.edu
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Abstract

Objectives: Visuospatial processing deficits have been reported in Huntington’s disease (HD). To date, no study has examined associations between visuospatial cognition and posterior brain findings in HD. Methods: We compared 119 premanifest (55> and 64<10.8 years to expected disease onset) and 104 early symptomatic (59 stage-1 and 45 stage-2) gene carriers, with 110 controls on visual search and mental rotation performance at baseline and 12 months. In the disease groups, we also examined associations between task performance and disease severity, functional capacity and structural brain measures. Results: Cross-sectionally, there were strong differences between all disease groups and controls on visual search, and between diagnosed groups and controls on mental rotation accuracy. Only the premanifest participants close to onset took longer than controls to respond correctly to mental rotation. Visual search negatively correlated with disease burden and motor symptoms in diagnosed individuals, and positively correlated with functional capacity. Mental rotation (“same”) was negatively correlated with motor symptoms in stage-2 individuals, and positively correlated with functional capacity. Visual search and mental rotation were associated with parieto-occipital (pre-/cuneus, calcarine, lingual) and temporal (posterior fusiform) volume and cortical thickness. Longitudinally, visual search deteriorated over 12 months in stage-2 individuals, with no evidence of declines in mental rotation. Conclusions: Our findings provide evidence linking early visuospatial deficits to functioning and posterior cortical dysfunction in HD. The findings are important since large research efforts have focused on fronto-striatal mediated cognitive changes, with little attention given to aspects of cognition outside of these areas. (JINS, 2016, 22, 595–608)

Keywords

Neurodegenerative diseaseOccipital lobeParietal lobeCognitionBasal gangliaVoxel-based morphometryCortical thicknessMRI
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 22 , Issue 6 , July 2016 , pp. 595 - 608
Copyright
Copyright © The International Neuropsychological Society 2016 

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References

Baizer, J.S., Desimone, R., & Ungerleider, L.G. (1993). Comparison of subcortical connections of inferior temporal and posterior parietal cortex in monkeys. Visual Neuroscience, 10, 59–72.Google Scholar
Baron-Cohen, S., Wheelwright, S., Hill, J., Raste, Y., & Plumb, I. (2001). The “Reading the Mind in the Eyes” Test revised version: A study with normal adults, and adults with Asperger syndrome or high-functioning autism. Journal of Child Psychology and Psychiatry, and Allied Disciplines, 42, 241–251.CrossRefGoogle ScholarPubMed
Beiser, D.G., Hua, S.E., & Houk, J.C. (1997). Network models of the basal ganglia. Current Opinion in Neurobiology, 7, 185–190.Google Scholar
Bethel-Fox, C.E., & Shepard, R. (1988). Mental rotation: Effects of stimulus complexity and familiarity. Journal of Experimental Psychology: Human Perception and Performance, 14, 12–23.Google Scholar
Blankenburg, F., Ruff, C.C., Bestmann, S., Bjoertomt, O., Josephs, O., Deichmann, R., & Driver, J. (2010). Studying the role of human parietal cortex in visuospatial attention with concurrent TMS-fMRI. Cerebral Cortex, 20, 2702–2711.Google Scholar
Bogousslavsky, J., Miklossy, J., Deruaz, J.P., Assal, G., & Regli, F. (1987). Lingual and fusiform gyri in visual processing: A clinico-pathologic study of superior altitudinal hemianopia. Journal of Neurology, Neurosurgery, and Psychiatry, 50, 607–614.Google Scholar
Deboer, L.B., Medina, J.L., Davis, M.L., Presnell, K.E., Powers, M.B., & Smits, J.A. (2013). Associations between fear of negative evaluation and eating pathology during intervention and 12-month follow-up. Cognitive Therapy and Research, 37, doi:10.1007/s10608-013-9547-y Google Scholar
Donner, T.H., Kettermann, A., Diesch, E., Villringer, A., & Brandt, S.A. (2003). Parietal activation during visual search in the absence of multiple distractors. Neuroreport, 14, 2257–2261.Google Scholar
Duff, K., Beglinger, L.J., Theriault, D., Allison, J., & Paulsen, J.S. (2010). Cognitive deficits in Huntington’s disease on the Repeatable Battery for the Assessment of Neuropsychological Status. Journal of Clinical and Experimental Neuropsychology, 32, 231–238.CrossRefGoogle ScholarPubMed
Duff, K., Paulsen, J., Mills, J., Beglinger, L.J., Moser, D.J., & Smith, M.M., . . . Coordinators of the Huntington Study Group. (2010). Mild cognitive impairment in prediagnosed Huntington disease. Neurology, 75, 500–507.Google Scholar
Evans, D., & Rothbart, M.K. (2007). Developing a model for adult temperament. Journal of Research in Personality, 41, 868–888.Google Scholar
Fischl, B., & Dale, A.M. (2000). Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proceedings of the National Academy of Sciences of the United States of America, 97, 11050–11055.CrossRefGoogle ScholarPubMed
Fischl, B., Salat, D.H., Busa, E., Albert, M., Dieterich, M., Haselgrove, C.,&Dale, A.M. (2002). Whole brain segmentation: Automated labeling of neuroanatomical structures in the human brain. Neuron, 33, 341–355.Google Scholar
Fischl, B., van der Kouwe, A., Destrieux, C., Halgren, E., Segonne, F., Salat, D.H., & Dale, A.M. (2004). Automatically parcellating the human cerebral cortex. Cerebral Cortex, 14, 11–22.CrossRefGoogle ScholarPubMed
Gomez-Tortosa, E., del Barrio, A., Barroso, T., & Garcia Ruiz, P.J. (1996). Visual processing disorders in patients with Huntington’s disease and asymptomatic carriers. Journal of Neurology, 243, 286–292.CrossRefGoogle ScholarPubMed
Goodale, M.A., & Milner, A.D. (1992). Separate visual pathways for perception and action. Trends in Neurosciences, 15, 20–25.CrossRefGoogle ScholarPubMed
Hagler, D.J. Jr., Saygin, A.P., & Sereno, M. (2006). Smoothing and cluster thresholding for cortical surface-based group analysis of fMRI data. Neuroimage, 33, 1093–1103.Google Scholar
Harris, I.M., Egan, G.F., Sonkkila, C., Tochon-Danguy, H.J., Paxinos, G., & Watson, J.D. (2000). Selective right parietal lobe activation during mental rotation: A parametric PET study. Brain, 123(Pt 1), 65–73.Google Scholar
Harris, I.M., Harris, J.A., & Caine, D. (2002). Mental-rotation deficits following damage to the right basal ganglia. Neuropsychology, 16, 524–537.Google Scholar
Huber, P.J. (1967). The behavior of maximum likelihood estimates under nonstandard conditions, Proceedings of the Fith Berkeley Symposium on Mathematical Statistics and Probability (pp. 221–233). Berkeley, CA: University of California Press.Google Scholar
Huntington Study Group. (1999). Unified Huntington’s Disease Rating Scale-99. Rochester, NY: Huntington Study Group.Google Scholar
Jacobs, H.I., Van Boxtel, M.P., Heinecke, A., Gronenschild, E.H., Backes, W.H., Ramakers, I.H.,&Verhey, F.R. (2012). Functional integration of parietal lobe activity in early Alzheimer disease. Neurology, 78, 352–360.Google Scholar
Johnson, E.B., Rees, E.M., Labuschagne, I., Durr, A., Leavitt, B.R., Roos, R.A., & Scahill, R.I. (2015). The impact of occipital lobe cortical thickness on cognitive task performance: An investigation in Huntington’s Disease. Neuropsychologia, 79, 138–146.Google Scholar
Klöppel, S., Gregory, S., Scheller, E., Minkova, L., Razi, A., & Durr, A., ...Track-On Investigators. (2015). Compensation in preclinical Huntington’s disease: Evidence from the Track-On study. EBioMedicine, 2, 1420–1429.CrossRefGoogle ScholarPubMed
Kravitz, D.J., Saleem, K.S., Baker, C.I., & Mishkin, M. (2011). A new neural framework for visuospatial processing. Nature Reviews. Neuroscience, 12, 217–230.Google Scholar
Labuschagne, I., Jones, R., Callaghan, J., Whitehead, D., Dumas, E.M., & Say, M.J., ...TRACK-HD Investigators. (2013). Emotional face recognition deficits and medication effects in pre-manifest through stage-II Huntington’s disease. Psychiatry Research, 207, 118–126.Google Scholar
Lawrence, A.D., Watkins, L.H., Sahakian, B.J., Hodges, J.R., & Robbins, T.W. (2000). Visual object and visuospatial cognition in Huntington’s disease: Implications for information processing in corticostriatal circuits. Brain, 123, 1349–1364.CrossRefGoogle ScholarPubMed
Lineweaver, T.T., Salmon, D.P., Bondi, M.W., & Corey-Bloom, J. (2005). Differential effects of Alzheimer’s disease and Huntington’s disease on the performance of mental rotation. Journal of the International Neuropsychological Society, 11, 30–39.Google Scholar
Mandal, P.K., Joshi, J., & Saharan, S. (2012). Visuospatial perception: An emerging biomarker for Alzheimer’s disease. Journal of Alzheimers Disease, 31(Suppl 3), S117–S135.Google Scholar
Mohr, E., Brouwers, P., Claus, J.J., Mann, U.M., Fedio, P., & Chase, T.N. (1991). Visuospatial cognition in Huntington’s disease. Movement Disorders, 6, 127–132.Google Scholar
Muller, C.J., & MacLehose, R.F. (2014). Estimating predicted probabilities from logistic regression: Different methods correspond to different target populations. International Journal of Epidemiology, 43, 962–970.Google Scholar
Murray, L.L., & Stout, J.C. (1999). Discourse comprehension in Huntington’s and Parkinson’s diseases. American Journal of Speech-Language Pathology, 8, 137–148.Google Scholar
Oehlert, G.W. (1992). A note on the delta method. The American Statistician, 46, 27–29.Google Scholar
Penney, J.B. Jr., Vonsattel, J.P., MacDonald, M.E., Gusella, J.F., & Myers, R.H. (1997). CAG repeat number governs the development rate of pathology in Huntington’s disease. Annals of Neurology, 41, 689–692.Google Scholar
Perry, R.J., & Hodges, J.R. (2000). Relationship between functional and neuropsychological performance in early Alzheimer disease. Alzheimer Disease and Associated Disorders, 14, 1–10.Google Scholar
Peters, M., & Battista, C. (2008). Applications of mental rotation figures of the Shepard and Metzler type and description of a mental rotation stimulus library. Brain and Cognition, 66, 260–264.Google Scholar
Prvulovic, D., Hubl, D., Sack, A.T., Melillo, L., Maurer, K., Frolich, L., & Dierks, T. (2002). Functional imaging of visuospatial processing in Alzheimer’s disease. Neuroimage, 17, 1403–1414.Google Scholar
Robertson, I.H., Ward, T., Ridgeway, V., & Nimmo-Smith, I. (1994). The test of everday attention. Bury St. Edmunds: Thames Valley Test Company.Google Scholar
Robins Wahlin, T.B., Lundin, A., & Dear, K. (2007). Early cognitive deficits in Swedish gene carriers of Huntington’s disease. Neuropsychology, 21, 31–44.Google Scholar
Rothman, K.J. (1990). No adjustments are needed for multiple comparisons. Epidemiology, 1, 43–46.Google Scholar
Rubin, L.H., Carter, C.S., Bishop, J.R., Pournajafi-Nazarloo, H., Harris, M.S., Hill, S.K., & Sweeney, J. A. (2013). Peripheral vasopressin but not oxytocin relates to severity of acute psychosis in women with acutely-ill untreated first-episode psychosis. Schizophrenia Research, 146, 138–143.Google Scholar
Shepard, R., & Metzler, J. (1971). Mental rotation of three dimensional objects. Science, 171, 701–703.Google Scholar
Shoulson, I., & Fahn, S. (1979). Huntington disease: Clinical care and evaluation. Neurology, 29, 1–3.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, 1–14.Google Scholar
Tabrizi, S.J., Langbehn, D.R., Leavitt, B.R., Roos, R.A., Durr, A., & Craufurd, D., . . . TRACK-HD Investigators. (2009). Biological and clinical manifestations of Huntington’s disease in the longitudinal TRACK-HD study: Cross-sectional analysis of baseline data. Lancet Neurology, 8, 791–801.Google Scholar
Unschuld, P.G., Edden, R.A., Carass, A., Liu, X., Shanahan, M., Wang, X., & Ross, C.A. (2012). Brain metabolite alterations and cognitive dysfunction in early Huntington’s disease. Movement Disorders, 27, 895–902.Google Scholar
Vonsattel, J.P., & DiFiglia, M. (1998). Huntington disease. Journal of Neuropathology and Experimental Neurology, 57, 369–384.CrossRefGoogle ScholarPubMed
Yeterian, E.H., & Pandya, D.N. (1995). Corticostriatal connections of extrastriate visual areas in rhesus monkeys. The Journal of Comparitive Neurology, 352, 436–457.Google Scholar
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