Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-21T17:08:10.902Z Has data issue: false hasContentIssue false
  • English
  • Français

Gray matter correlates of set-shifting among neurodegenerative disease, mild cognitive impairment, and healthy older adults

Published online by Cambridge University Press:  07 April 2010

JUDY PA ,
KATHERINE L. POSSIN ,
STEPHEN M. WILSON ,
LOVINGLY C. QUITANIA ,
JOEL H. KRAMER ,
ADAM L. BOXER ,
MICHAEL W. WEINER  and
JULENE K. JOHNSON
JUDY PA*
Affiliation:
Alzheimer Disease Research Center, Dept of Neurology, University of California, San Francisco, California
KATHERINE L. POSSIN
Affiliation:
Alzheimer Disease Research Center, Dept of Neurology, University of California, San Francisco, California
STEPHEN M. WILSON
Affiliation:
Alzheimer Disease Research Center, Dept of Neurology, University of California, San Francisco, California
LOVINGLY C. QUITANIA
Affiliation:
Alzheimer Disease Center, Dept of Neurology, University of California, Davis, California
JOEL H. KRAMER
Affiliation:
Alzheimer Disease Research Center, Dept of Neurology, University of California, San Francisco, California
ADAM L. BOXER
Affiliation:
Alzheimer Disease Research Center, Dept of Neurology, University of California, San Francisco, California
MICHAEL W. WEINER
Affiliation:
Center for Imaging of Neurodegenerative Diseases, San Francisco VA Medical Center, San Francisco, California
JULENE K. JOHNSON
Affiliation:
Alzheimer Disease Research Center, Dept of Neurology, University of California, San Francisco, California Institute for Health and Aging, University of California, San Francisco, California
*
*Correspondence and reprint requests to: Judy Pa, UCSF Mission Bay, Genentech Hall, Room N474, 600 16th Street, San Francisco, CA 94158. E-mail: judy.pa@ucsf.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

There is increasing recognition that set-shifting, a form of cognitive control, is mediated by different neural structures. However, these regions have not yet been carefully identified as many studies do not account for the influence of component processes (e.g., motor speed). We investigated gray matter correlates of set-shifting while controlling for component processes. Using the Design Fluency (DF), Trail Making Test (TMT), and Color Word Interference (CWI) subtests from the Delis-Kaplan Executive Function System (D-KEFS), we investigated the correlation between set-shifting performance and gray matter volume in 160 subjects with neurodegenerative disease, mild cognitive impairment, and healthy older adults using voxel-based morphometry. All three set-shifting tasks correlated with multiple, widespread gray matter regions. After controlling for the component processes, set-shifting performance correlated with focal regions in prefrontal and posterior parietal cortices. We also identified bilateral prefrontal cortex and the right posterior parietal lobe as common sites for set-shifting across the three tasks. There was a high degree of multicollinearity between the set-shifting conditions and the component processes of TMT and CWI, suggesting DF may better isolate set-shifting regions. Overall, these findings highlight the neuroanatomical correlates of set-shifting and the importance of controlling for component processes when investigating complex cognitive tasks. (JINS, 2010, 16, 640–650.)

Keywords

D-KEFSDesign fluencyTrail making testColor word interferenceExecutive functionVoxel-based morphometry
Type
Research Articles
Information
Journal of the International Neuropsychological Society , Volume 16 , Issue 4 , July 2010 , pp. 640 - 650
Copyright
Copyright © The International Neuropsychological Society 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Anderson, S.W., Damasio, H., Jones, R.D., & Tranel, D. (1991). Wisconsin Card Sorting Test performance as a measure of frontal lobe damage. Journal of Clinical and Experimental Neuropsychology, 13, 909–922.CrossRefGoogle ScholarPubMed
APA. (1994). Diagnostic and statistical manual of mental disorders - (DSM-IV) (Vol. 4). Washington, DC: American Psychiatric Association.Google Scholar
Army Individual Test Battery Manual of Directions and Scoring. (1944).Google Scholar
Aron, A.R., Monsell, S., Sahakian, B.J., & Robbins, T.W. (2004). A componential analysis of task-switching deficits associated with lesions of left and right frontal cortex. Brain, 127(Pt 7), 1561–1573.CrossRefGoogle ScholarPubMed
Aron, A.R., Watkins, L., Sahakian, B.J., Monsell, S., Barker, R.A., & Robbins, T.W. (2003). Task-set switching deficits in early-stage Huntington’s disease: Implications for basal ganglia function. Journal of Cognitive Neuroscience, 15, 629–642.CrossRefGoogle ScholarPubMed
Asari, T., Konishi, S., Jimura, K., & Miyashita, Y. (2005). Multiple components of lateral posterior parietal activation associated with cognitive set shifting. Neuroimage, 26, 694–702.CrossRefGoogle ScholarPubMed
Ashburner, J. (2007). A fast diffeomorphic image registration algorithm. Neuroimage, 38, 95–113.CrossRefGoogle ScholarPubMed
Barber, A.D., & Carter, C.S. (2005). Cognitive control involved in overcoming prepotent response tendencies and switching between tasks. Cerebral Cortex, 15, 899–912.CrossRefGoogle ScholarPubMed
Barcelo, F., & Santome-Calleja, A. (2000). [A critical review of the specificity of the Wisconsin card sorting test for the assessment of prefrontal function]. Revista de Neurologica, 30, 855–864.Google ScholarPubMed
Brass, M., Ullsperger, M., Knoesche, T.R., von Cramon, D.Y., & Phillips, N.A. (2005). Who comes first? The role of the prefrontal and parietal cortex in cognitive control. Journal of Cognitive Neuroscience, 17, 1367–1375.CrossRefGoogle ScholarPubMed
Brooks, B.R. (1994). El Escorial World Federation of Neurology criteria for the diagnosis of amyotrophic lateral sclerosis. Subcommittee on Motor Neuron Diseases/Amyotrophic Lateral Sclerosis of the World Federation of Neurology Research Group on Neuromuscular Diseases and the El Escorial “Clinical limits of amyotrophic lateral sclerosis” workshop contributors. Journal of the Neurological Sciences, 160, S25–S29.Google Scholar
Cools, R., Barker, R.A., Sahakian, B.J., & Robbins, T.W. (2001). Mechanisms of cognitive set flexibility in Parkinson’s disease. Brain, 124(Pt 12), 2503–2512.CrossRefGoogle ScholarPubMed
Corcoran, R., & Upton, D. (1993). A role for the hippocampus in card sorting? Cortex, 29, 293–304.CrossRefGoogle ScholarPubMed
Crone, E.A., Wendelken, C., Donohue, S.E., & Bunge, S.A. (2006). Neural evidence for dissociable components of task-switching. Cerebral Cortex, 16, 475–486.CrossRefGoogle ScholarPubMed
Cummings, J.L. (1997). The neuropsychiatric inventory: Assessing psychopathology in dementia patients. Neurology, 48(Suppl. 6), S10–S16.CrossRefGoogle ScholarPubMed
Delis, D., Kaplan, E.B., & Kramer, J. (2001). The Delis-Kaplan Executive Function System. San Antonio, TX: The Psychological Corporation.Google Scholar
Derrfuss, J., Brass, M., & von Cramon, D.Y. (2004). Cognitive control in the posterior frontolateral cortex: Evidence from common activations in task coordination, interference control, and working memory. Neuroimage, 23, 604–612.CrossRefGoogle ScholarPubMed
Eslinger, P.J., & Grattan, L.M. (1993). Frontal lobe and frontal-striatal substrates for different forms of human cognitive flexibility. Neuropsychologia, 31, 17–28.CrossRefGoogle ScholarPubMed
Folstein, M.F., Folstein, S.E., & McHugh, P.R. (1975). “Mini-mental state”. A practical method for grading the mental state of patients for the clinician. Journal of Psychiatric Research, 12, 189–198.CrossRefGoogle ScholarPubMed
Garbutt, S., Matlin, A., Hellmuth, J., Schenk, A.K., Johnson, J.K., Rosen, H., et al. . (2008). Oculomotor function in frontotemporal lobar degeneration, related disorders and Alzheimer’s disease. Brain, 131, 1268–1281.CrossRefGoogle ScholarPubMed
Heaton, R.K., Chelune, G.J., Talley, J.L., Kay, G.G., & Curtis, G. (1993). Wisconsin Card Sorting Test (WCST) Manual: Revised and expanded. Odessa, FL: Psychological Assessment Resources.Google Scholar
Horacek, J., Dockery, C., Kopecek, M., Spaniel, F., Novak, T., Tislerova, B., et al. . (2006). Regional brain metabolism as the predictor of performance on the Trail Making Test in schizophrenia. A 18FDG PET covariation study. Neuro Endocrinology Letters, 27, 587–594.Google ScholarPubMed
Huey, E.D., Goveia, E.N., Paviol, S., Pardini, M., Krueger, F., Zamboni, G., et al. . (2009). Executive dysfunction in frontotemporal dementia and corticobasal syndrome. Neurology, 72, 453–459.CrossRefGoogle ScholarPubMed
Jazbec, S., Pantelis, C., Robbins, T., Weickert, T., Weinberger, D.R., & Goldberg, T.E. (2007). Intra-dimensional/extra-dimensional set-shifting performance in schizophrenia: Impact of distractors. Schizophrenia Research, 89, 339–349.CrossRefGoogle ScholarPubMed
Kaplan, E., Goodglass, H., & Wintraub, S. (1983). The Boston Naming Test. Philadelphia: Lea and Febiger.Google Scholar
Kertesz, A., & Munoz, G. (2004). Relationship between frontotemporal dementia and corticobasal degeneration/progressive supranuclear palsy. Dementia and Geriatric Cognitive Disorders, 17, 282–286.CrossRefGoogle ScholarPubMed
Konishi, S., Hayashi, T., Uchida, I., Kikyo, H., Takahashi, E., & Miyashita, Y. (2002). Hemispheric asymmetry in human lateral prefrontal cortex during cognitive set shifting. Proceedings of the National Academy of Sciences of the United States of America, 99, 7803–7808.CrossRefGoogle ScholarPubMed
Kramer, J.H., Jurik, J., Sha, S.J., Rankin, K.P., Rosen, H.J., Johnson, J.K., et al. . (2003). Distinctive neuropsychological patterns in frontotemporal dementia, semantic dementia, and Alzheimer disease. Cognitive and Behavioral Neurology, 16, 211–218.CrossRefGoogle ScholarPubMed
Kramer, J.H., Quitania, L., Dean, D., Neuhaus, J., Rosen, H.J., Halabi, C., et al. . (2007). Magnetic resonance imaging correlates of set shifting. Journal of the International Neuropsychological Society, 13, 386–392.CrossRefGoogle ScholarPubMed
Lawrence, A.D., Hodges, J.R., Rosser, A.E., Kershaw, A., ffrench-Constant, C., Rubinsztein, D.C., et al. . (1998). Evidence for specific cognitive deficits in preclinical Huntington’s disease. Brain, 121(Pt 7), 1329–1341.CrossRefGoogle ScholarPubMed
Lie, C.H., Specht, K., Marshall, J.C., & Fink, G.R. (2006). Using fMRI to decompose the neural processes underlying the Wisconsin Card Sorting Test. Neuroimage, 30, 1038–1049.CrossRefGoogle ScholarPubMed
Marshall, G.A., Hendrickson, R., Kaufer, D.I., Ivanco, L.S., & Bohnen, N.I. (2006). Cognitive correlates of brain MRI subcortical signal hyperintensities in non-demented elderly. International Journal of Geriatric Psychiatry, 21, 32–35.CrossRefGoogle ScholarPubMed
Mayr, U., Diedrichsen, J., Ivry, R., & Keele, S.W. (2006). Dissociating task-set selection from task-set inhibition in the prefrontal cortex. Journal of Cognitive Neuroscience, 18, 14–21.CrossRefGoogle ScholarPubMed
McDonald, C.R., Delis, D.C., Norman, M.A., Tecoma, E.S., & Iragui-Madozi, V.I. (2005). Is impairment in set-shifting specific to frontal-lobe dysfunction? Evidence from patients with frontal-lobe or temporal-lobe epilepsy. Journal of the International Neuropsychological Society, 11, 477–481.CrossRefGoogle ScholarPubMed
McDonald, C.R., Delis, D.C., Norman, M.A., Wetter, S.R., Tecoma, E.S., & Iragui, V.J. (2005). Response inhibition and set shifting in patients with frontal lobe epilepsy or temporal lobe epilepsy. Epilepsy & Behavior, 7, 438–446.CrossRefGoogle ScholarPubMed
McKeith, I.G., Dickson, D.W., Lowe, J., Emre, M., O’Brien, J.T., Feldman, H., et al. . (2005). Diagnosis and management of dementia with Lewy bodies: Third report of the DLB Consortium. Neurology, 65, 1863–1872.CrossRefGoogle ScholarPubMed
McKhann, G., Drachman, D., Folstein, M., Katzman, R., Price, D., & Stadlan, E.M. (1984). Clinical diagnosis of Alzheimer’s disease: Report of the NINCDS-ADRDA Work Group under the auspices of Department of Health and Human Services Task Force on Alzheimer’s Disease. Neurology, 34, 939–944.CrossRefGoogle ScholarPubMed
McKirdy, J., Sussmann, J.E., Hall, J., Lawrie, S.M., Johnstone, E.C., & McIntosh, A.M. (2009). Set shifting and reversal learning in patients with bipolar disorder or schizophrenia. Psychological Medicine, 39, 1289–1293.CrossRefGoogle ScholarPubMed
Moll, J., de Oliveira-Souza, R., Moll, F.T., Bramati, I.E., & Andreiuolo, P.A. (2002). The cerebral correlates of set-shifting: An fMRI study of the trail making test. Arquivos de Neuro-psiquiatria, 60, 900–905.CrossRefGoogle ScholarPubMed
Monchi, O., Petrides, M., Petre, V., Worsley, K., & Dagher, A. (2001). Wisconsin Card Sorting revisited: Distinct neural circuits participating in different stages of the task identified by event-related functional magnetic resonance imaging. Journal of Neuroscience, 21, 7733–7741.CrossRefGoogle ScholarPubMed
Monchi, O., Petrides, M., Strafella, A.P., Worsley, K.J., & Doyon, J. (2006). Functional role of the basal ganglia in the planning and execution of actions. Annals of Neurology, 59, 257–264.CrossRefGoogle ScholarPubMed
Morris, J.C. (1993). The Clinical Dementia Rating (CDR): Current version and scoring rules [see comments]. Neurology, 43, 2412–2414.CrossRefGoogle ScholarPubMed
Nagano-Saito, A., Leyton, M., Monchi, O., Goldberg, Y.K., He, Y., & Dagher, A. (2008). Dopamine depletion impairs frontostriatal functional connectivity during a set-shifting task. Journal of Neuroscience, 28, 3697–3706.CrossRefGoogle ScholarPubMed
Neary, D., Snowden, J.S., Gustafson, L., Passant, U., Stuss, D., Black, S., et al. . (1998). Frontotemporal lobar degeneration: A consensus on clinical diagnostic criteria. Neurology, 51, 1546–1554.CrossRefGoogle ScholarPubMed
Newman, L.M., Trivedi, M.A., Bendlin, B.B., Ries, M.L., & Johnson, S.C. (2007). The relationship between gray matter morphometry and neuropsychological performance in a large sample of cognitively healthy adults. Brain Imaging and Behavior, 1, 3–10.CrossRefGoogle Scholar
Owen, A.M., Roberts, A.C., Polkey, C.E., Sahakian, B.J., & Robbins, T.W. (1991). Extra-dimensional versus intra-dimensional set shifting performance following frontal lobe excisions, temporal lobe excisions or amygdalo-hippocampectomy in man. Neuropsychologia, 29, 993–1006.CrossRefGoogle ScholarPubMed
Pa, J., Boxer, A.L., Freeman, K., Kramer, J., Miller, B.L., Chao, L.L., et al. . (2009). Clinical-Neuroimaging Characteristics of Dysexecutive Mild Cognitive Impairment. Annals of Neurology, 65, 414–423.Google ScholarPubMed
Pantelis, C., Barber, F.Z., Barnes, T.R., Nelson, H.E., Owen, A.M., & Robbins, T.W. (1999). Comparison of set-shifting ability in patients with chronic schizophrenia and frontal lobe damage. Schizophrenia Research, 37, 251–270.CrossRefGoogle ScholarPubMed
Pereira, J.M.S., Xiong, L., Acosta-Cabronero, J., Pengas, G., Williams, G.B., & Nestor, P.J. (2009). Registration accuracy for VBM studies varies according to region and degenerative disease grouping. Neuroimage, 49, 2205–2215.CrossRefGoogle ScholarPubMed
Perry, M.E., McDonald, C.R., Hagler, D.J. Jr., Gharapetian, L., Kuperman, J.M., Koyama, A.K., et al. . (2009). White matter tracts associated with set-shifting in healthy aging. Neuropsychologia, 47, 2835–2842.CrossRefGoogle ScholarPubMed
Posner, M.I., Walker, J.A., Friedrich, F.J., & Rafal, R.D. (1984). Effects of parietal injury on covert orienting of attention. Journal of Neuroscience, 4, 1863–1874.CrossRefGoogle ScholarPubMed
Ravizza, S.M., & Ciranni, M.A. (2002). Contributions of the prefrontal cortex and basal ganglia to set shifting. Journal of Cognitive Neuroscience, 14, 472–483.CrossRefGoogle ScholarPubMed
Reitan, R.M., & Wolfson, D. (1985). The Halstead-Reitan Neuropsychological Test Battery. Tucson: Neuropsychology Press.Google Scholar
Rushworth, M.F., Hadland, K.A., Paus, T., & Sipila, P.K. (2002). Role of the human medial frontal cortex in task switching: A combined fMRI and TMS study. Journal of Neurophysiology, 87, 2577–2592.CrossRefGoogle ScholarPubMed
Rushworth, M.F., Paus, T., & Sipila, P.K. (2001). Attention systems and the organization of the human parietal cortex. Journal of Neuroscience, 21, 5262–5271.CrossRefGoogle ScholarPubMed
Salmond, C.H., Ashburner, J., Vargha-Khadem, F., Connelly, A., Gadian, D.G., & Friston, K.J. (2002). Distributional assumptions in voxel-based morphometry. Neuroimage, 17, 1027–1030.CrossRefGoogle ScholarPubMed
Schmahmann, J.D., & Sherman, J.C. (1998). The cerebellar cognitive affective syndrome. Brain, 121(Pt 4), 561–579.CrossRefGoogle ScholarPubMed
Smith, A.B., Taylor, E., Brammer, M., & Rubia, K. (2004). Neural correlates of switching set as measured in fast, event-related functional magnetic resonance imaging. Human Brain Mapping, 21, 247–256.CrossRefGoogle ScholarPubMed
Strauss, E., Hunter, M., & Wada, J. (1993). Wisconsin Card Sorting Performance: Effects of age of onset of damage and laterality of dysfunction. Journal of Clinical and Experimental Neuropsychology, 15, 896–902.CrossRefGoogle ScholarPubMed
Stroop, J. (1935). Studies of interferences in serial verbal reactions. Journal of Experimental Psychology, 18, 643–662.CrossRefGoogle Scholar
Stuss, D.T., Bisschop, S.M., Alexander, M.P., Levine, B., Katz, D., & Izukawa, D. (2001). The Trail Making Test: A study in focal lesion patients. Psychological Assessment, 13, 230–239.CrossRefGoogle ScholarPubMed
Tamura, I., Kikuchi, S., Otsuki, M., Kitagawa, M., & Tashiro, K. (2003). Deficits of working memory during mental calculation in patients with Parkinson’s disease. Journal of the Neurological Sciences, 209, 19–23.CrossRefGoogle ScholarPubMed
Wager, T.D., Jonides, J., & Reading, S. (2004). Neuroimaging studies of shifting attention: A meta-analysis. Neuroimage, 22, 1679–1693.CrossRefGoogle ScholarPubMed
Warrington, E.K., & James, M. (1991). The Visual object and space perception battery. Bury St Edmunds: Thames Valley Test Company.Google Scholar
Wechsler, D. (1997). Wechsler adult intelligence scale (3rd ed.). San Antonio, TX: The Psychological Corporation.Google Scholar
Winblad, B., Palmer, K., Kivipelto, M., Jelic, V., Fratiglioni, L., Wahlund, L.O., et al. . (2004). Mild cognitive impairment–beyond controversies, towards a consensus: Report of the International Working Group on Mild Cognitive Impairment. Journal of Internal Medicine, 256, 240–246.CrossRefGoogle Scholar
Woodward, T.S., Bub, D.N., & Hunter, M.A. (2002). Task switching deficits associated with Parkinson’s disease reflect depleted attentional resources. Neuropsychologia, 40, 1948–1955.CrossRefGoogle ScholarPubMed
Yesavage, J.A., Brink, T.L., Rolse, T.L., Lum, O., Huang, V., Adey, M., et al. . (1983). Development and validity of a geriatric depression scale: A preliminary report. Journal of Psychiatric Research, 17, 37–49.CrossRefGoogle Scholar
Yochim, B., Baldo, J., Nelson, A., & Delis, D.C. (2007). D-KEFS Trail Making Test performance in patients with lateral prefrontal cortex lesions. Journal of the International Neuropsychological Soceity, 13, 704–709.Google ScholarPubMed
Zakzanis, K.K., Mraz, R., & Graham, S.J. (2005). An fMRI study of the Trail Making Test. Neuropsychologia, 43, 1878–1886.CrossRefGoogle ScholarPubMed
Zimmerman, M.E., Brickman, A.M., Paul, R.H., Grieve, S.M., Tate, D.F., Gunstad, J., et al. . (2006). The relationship between frontal gray matter volume and cognition varies across the healthy adult lifespan. American Journal of Geriatric Psychiatry, 14, 823–833.CrossRefGoogle ScholarPubMed