Skip to main content
×
×
Home

Rule violation errors are associated with right lateral prefrontal cortex atrophy in neurodegenerative disease

  • KATHERINE L. POSSIN (a1), SIMONA M. BRAMBATI (a2), HOWARD J. ROSEN (a1), JULENE K. JOHNSON (a1), JUDY PA (a1), MICHAEL W. WEINER (a1), BRUCE L. MILLER (a1) and JOEL H. KRAMER (a1)...
Abstract

Good cognitive performance requires adherence to rules specific to the task at hand. Patients with neurological disease often make rule violation (RV) errors, but the anatomical basis for RV during cognitive testing remains debated. The present study examined the neuroanatomical correlates of RV errors made on tests of executive functioning in 166 subjects diagnosed with neurodegenerative disease or as neurologically healthy. Specifically, RV errors were voxel-wisely correlated with gray matter volume derived from high-definition magnetic resonance images using voxel-based morphometry implemented in SPM2. Latent variable analysis showed that RV errors tapped a unitary construct separate from repetition errors. This analysis was used to generate factor scores to represent what is common among RV errors across tests. The extracted RV factor scores correlated with tissue loss in the lateral middle and inferior frontal gyri and the caudate nucleus bilaterally. When a more stringent control for global cognitive functioning was applied using Mini Mental State Exam scores, only the correlations with the right lateral prefrontal cortex (PFC) remained significant. These data underscore the importance of right lateral PFC in behavioral monitoring and highlight the potential of RV error assessment for identifying patients with damage to this region. (JINS, 2009, 15, 354–364.)

Copyright
Corresponding author
*Correspondence and reprint requests to: Katherine L. Possin, 350 Parnassus Ste. 905, San Francisco, California 94143-1207. E-mail: kpossin@memory.ucsf.edu
References
Hide All
Alexander, M.P., Stuss, D.T., Picton, T., Shallice, T., & Gillingham, S. (2007). Regional frontal injuries cause distinct impairments in cognitive control. Neurology, 68(18), 15151523.
American Psychiatric Association. (1994). Diagnostic and Statistical Manual of Mental Disorders—(DSM-IV). Washington, D.C.
Amici, S., Brambati, S.M., Wilkins, D.P., Ogar, J., Dronkers, N.L., Miller, B.L., & Gorno-Tempini, M.L. (2007). Anatomical correlates of sentence comprehension and verbal working memory in neurodegenerative disease. Journal of Neuroscience, 27(23), 62826290.
Aron, A.R., Robbins, T.W., & Poldrack, R.A. (2004). Inhibition and the right inferior frontal cortex. Trends in Cognitive Sciences, 8(4), 170177.
Ashburner, J. & Friston, K.J. (2000). Voxel-based morphometry—The methods. NeuroImage, 11(6 Pt 1), 805821.
Binetti, G., Magni, E., Padovani, A., Cappa, S.F., Bianchetti, A., & Trabucchi, M. (1996). Executive dysfunction in early Alzheimer’s disease. Journal of Neurology, Neurosurgery, and Psychiatry 60(1), 9193.
Bonelli, R.M. & Cummings, J.L. (2007). Frontal-subcortical circuitry and behavior. Dialogues in Clinical Neuroscience, 9(2), 141151.
Boxer, A.L., Geschwind, M.D., Belfor, N., Gorno-Tempini, M.L., Schauer, G.F., Miller, B.L., Weiner, M.W., & Rosen, H.J. (2006). Patterns of brain atrophy that differentiate corticobasal degeneration syndrome from progressive supranuclear palsy. Archives of Neurology, 63(1), 8186.
Brooks, B.R., Miller, R.G., Swash, M., & Munsat, T.L. (2000). El Escorial revisited: Revised criteria for the diagnosis of amyotrophic lateral sclerosis. Amyotrophic Lateral Sclerosis and Other Motor Neuron Disorders, 1(5), 293299.
Buchsbaum, B.R., Greer, S., Chang, W.L., & Berman, K.F. (2005). Meta-analysis of neuroimaging studies of the Wisconsin card-sorting task and component processes. Human Brain Mapping, 25(1), 3545.
Bunge, S.A., Ochsner, K.N., Desmond, J.E., Glover, G.H., & Gabrieli, J.D. (2001). Prefrontal regions involved in keeping information in and out of mind. Brain, 124(Pt 10), 20742086.
Cahn-Weiner, D.A., Boyle, P.A., & Malloy, P.F. (2002). Tests of executive function predict instrumental activities of daily living in community-dwelling older individuals. Applied Neuropsychology, 9(3), 187191.
Carey, C.L., Woods, S.P., Damon, J., Halabi, C., Dean, D., Delis, D.C., Miller, B.L., & Kramer, J.H. (2008). Discriminant validity and neuroanatomical correlates of rule monitoring in frontotemporal dementia and Alzheimer’s disease. Neuropsychologia, 46(4), 10811087.
Cato, M.A., Delis, D.C., Abildskov, T.J., & Bigler, E. (2004). Assessing the elusive cognitive deficits associated with ventromedial prefrontal damage: A case of a modern-day Phineas Gage. Journal of the International Neuropsychological Society, 10(3), 453465.
Chan, F., Armstrong, I.T., Pari, G., Riopelle, R.J., & Munoz, D.P. (2005). Deficits in saccadic eye-movement control in Parkinson’s disease. Neuropsychologia, 43(5), 784796.
Chang, J.L., Lomen-Hoerth, C., Murphy, J., Henry, R.G., Kramer, J.H., Miller, B.L., & Gorno-Tempini, M.L. (2005). A voxel-based morphometry study of patterns of brain atrophy in ALS and ALS/FTLD. Neurology, 65(1), 7580.
Chikazoe, J., Konishi, S., Asari, T., Jimura, K., & Miyashita, Y. (2007). Activation of right inferior frontal gyrus during response inhibition across response modalities. Journal of Cognitive Neuroscience, 19(1), 6980.
Clark, L., Blackwell, A.D., Aron, A.R., Turner, D.C., Dowson, J., Robbins, T.W., & Sahakian, B.J. (2007). Association between response inhibition and working memory in adult ADHD: A link to right frontal cortex pathology? Biological Psychiatry, 61(12), 13951401.
Comrey, A.L. & Lee, H.B. (1992). A first course in factor analysis. Hillsdale, NJ: Lawrence Erlbaum Associates.
Courtney, S.M. (2004). Attention and cognitive control as emergent properties of information representation in working memory. Cognitive, Affective & Behavioral Neuroscience, 4(4), 501516.
Culbertson, W.C., Moberg, P.J., Duda, J.E., Stern, M.B., & Weintraub, D. (2004). Assessing the executive function deficits of patients with Parkinson’s disease: Utility of the Tower of London-Drexel. Assessment, 11(1), 2739.
Dao-Castellana, M.H., Samson, Y., Legault, F., Martinot, J.L., Aubin, H.J., Crouzel, C., Feldman, L., Barraucand, D., Rancurel, G., Feline, A., & Syrota, A. (1998). Frontal dysfunction in neurologically normal chronic alcoholic subjects: Metabolic and neuropsychological findings. Psychological Medicine, 28(5), 10391048.
de Fockert, J.W., Rees, G., Frith, C.D., & Lavie, N. (2001). The role of working memory in visual selective attention. Science, 291(5509), 18031806.
Delis, D.C, Jacobson, M., Bondi, M.W., Hamilton, J.M., & Salmon, D.P. (2003). The myth of testing construct validity using factor analysis or correlations with normal or mixed clinical populations: Lessons from memory assessment. Journal of the International Neuropsychological Society, 9(6) 936946.
Delis, D., Kaplan, E.B., & Kramer, J. (2001). The Delis-Kaplan Executive Function System. San Antonio, TX: The Psychological Corporation.
Donohue, S.E., Wendelken, C., & Bunge, S.A. (2008). Neural correlates of preparation for action selection as a function of specific task demands. Journal of Cognitive Neuroscience, 20(4), 694706.
Fielding, J., Georgiou-Karistianis, N., & White, O. (2006). The role of the basal ganglia in the control of automatic visuospatial attention. Journal of the International Neuropsychological Society, 12(5), 657667.
Filoteo, J.V., Delis, D.C., Salmon, D.P., Demadura, T., Roman, M.J., & Shults, C.W.(1997). An examination of the nature of attentional deficits in patients with Parkinson’s disease: Evidence from a spatial orienting task. Journal of the International Neuropsychological Society 3(4) 337347
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, 189198.
Funahashi, S., Bruce, C.J., & Goldman-Rakic, P.S. (1993). Dorsolateral prefrontal lesions and oculomotor delayed-response performance: Evidence for mnemonic “scotomas”. Journal of Neuroscience, 13(4), 14791497.
Gazzaley, A., Cooney, J.W., Rissman, J., & D’Esposito, M. (2005). Top-down suppression deficit underlies working memory impairment in normal aging. Nature Neuroscience, 8(10), 12981300.
Gazzaley, A., Rissman, J., Cooney, J., Rutman, A., Seibert, T., Clapp, W., & D’Esposito, M. (2007). Functional interactions between prefrontal and visual association cortex contribute to top-down modulation of visual processing. Cerebral Cortex, 17(Suppl 1), i125i135.
Good, C.D., Johnsrude, I., Ashburner, J., Henson, R.N., Friston, K.J., & Frackowiak, R.S. (2001a). Cerebral asymmetry and the effects of sex and handedness on brain structure: A voxel-based morphometric analysis of 465 normal adult human brains. NeuroImage, 14(3), 685700.
Good, C.D., Johnsrude, I.S., Ashburner, J., Henson, R.N., Friston, K.J., & Frackowiak, R.S. (2001b). A voxel-based morphometric study of ageing in 465 normal adult human brains. NeuroImage, 14(1 Pt 1), 2136.
Henik, A., Singh, J., Beckley, D.J., & Rafal, R.D. (1993). Disinhibition of automatic word reading in Parkinson’s disease. Cortex, 29(4), 589599.
Hester, R., Murphy, K., & Garavan, H. (2004). Beyond common resources: The cortical basis for resolving task interference. NeuroImage, 23(1), 202212.
Jurado, M.B. & Rosselli, M. (2007). The elusive nature of executive functions: A review of our current understanding. Neuropsychology Review, 17(3), 213233.
Kaplan, E. (1988). A process approach to neuropsychological assessment. In Boll, T. & Bryant, B. (Eds.), Clinical neuropsychology and brain function: Research, measurement, and practice (pp. 129167). Washington, DC: American Psychological Association.
Kramer, J.H., Jurik, J., Sha, S.J., Rankin, K.P., Rosen, H.J., Johnson, J.K., & Miller, B.L. (2003). Distinctive neuropsychological patterns in frontotemporal dementia, semantic dementia, and Alzheimer disease. Cognitive and Behavioral Neurology, 16(4), 211218.
Kramer, J.H., Nelson, A., Johnson, J.K., Yaffe, K., Glenn, S., Rosen, H.J., & Miller, B.L. (2006). Multiple cognitive deficits in amnestic mild cognitive impairment. Dementia and Geriatric Cognitive Disorders, 22(4), 306311.
Lawrence, V., Houghton, S., Douglas, G., Durkin, K., Whiting, K., & Tannock, R. (2004). Executive function and ADHD: A comparison of children’s performance during neuropsychological testing and real-world activities. Journal of Attention Disorders, 7(3), 137149.
Lezak, M.D., Howieson, D.B., Loring, D.W., Loring, D.W., Hannay, H.J., & Fischer, J.S. (2004). Neuropsychological assessment (4th ed.). Oxford: Oxford University Press.
Litvan, I., Agid, Y., Calne, D., Campbell, G., Dubois, B., Duvoisin, R.C., Goetz, C.G., Golbe, L.I., Grafman, J., Growdon, J.H., Hallett, M., Jankovic, J., Quinn, N.P., Tolosa, E., & Zee, D.S. (1996). Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): Report of the NINDS-SPSP international workshop. Neurology, 47(1), 19.
Litvan, I., Bhatia, K.P., Burn, D.J., Goetz, C.G., Lang, A.E., McKeith, I., Quinn, N., Sethi, K.D., Shults, C., Wenning, G.K., & Movement Disorders Society Scientific Issues Committee. (2003). Movement Disorders Society Scientific Issues Committee report: SIC Task Force appraisal of clinical diagnostic criteria for Parkinsonian disorders. Movement Disorders, 18(5), 467486.
MacDonald, A.W. 3rd, Cohen, J.D., Stenger, V.A., & Carter, C.S. (2000). Dissociating the role of the dorsolateral prefrontal and anterior cingulate cortex in cognitive control. Science, 288(5472), 18351838.
McKeith, I.G. (2006). Consensus guidelines for the clinical and pathologic diagnosis of dementia with Lewy bodies (DLB): Report of the Consortium on DLB International Workshop. Journal of Alzheimer’s Disease, 9(3 Suppl), 417423.
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(7), 939944.
Miller, E.K. (2000). The prefrontal cortex and cognitive control. Nature Reviews. Neuroscience, 1(1), 5965.
Mitchell, J.P., Macrae, C.N., & Gilchrist, I.D. (2002). Working memory and the suppression of reflexive saccades. Journal of Cognitive Neuroscience, 14(1), 95103.
Morris, J.C. (1993). The Clinical Dementia Rating (CDR): Current version and scoring rules. Neurology, 43(11), 24122414.
Mychack, P., Kramer, J.H., Boone, K.B., & Miller, B.L. (2001). The influence of right frontotemporal dysfunction on social behavior in frontotemporal dementia. Neurology, 56(11 Suppl 4), S11S15.
Neary, D., Snowden, J.S., Gustafson, L., Passant, U., Stuss, D., Black, S., Freedman, M., Kertesz, A., Robert, P.H., Albert, M., Boone, K., Miller, B.L., Cummings, J., & Benson, D.F. (1998). Frontotemporal lobar degeneration: A consensus on clinical diagnostic criteria. Neurology, 51(6), 15461554.
Osher, J.E., Wicklund, A.H., Rademaker, A., Johnson, N., & Weintraub, S. (2007). The mini-mental state examination in behavioral variant frontotemporal dementia and primary progressive aphasia. American Journal of Alzheimer’s Disease and Other Dementia’s 22(6) 468-473.
Pa, J., Boxer, A.L., Freeman, K., Kramer, J.H., Miller, B.L., Chao, L.L., Gazzaley, A., Weiner, M.W., Neuhaus, J., & Johnson, J.K. (in press). Clinical-neuroimaging characteristics of dysexecutive mild cognitive impairment. Annals of Neurology.
Petersen, R.C., Smith, G.E., Waring, S.C., Ivnik, R.J., Tangalos, E.G., & Kokmen, E. (1999). Mild cognitive impairment: Clinical characterization and outcome. Archives of Neurology, 56(3), 303308.
Phukan, J., Pender, N.P., & Hardiman, O. (2007). Cognitive impairment in amyotrophic lateral sclerosis. Lancet Neurology, 6(11), 9941003.
Pierrot-Deseilligny, C., Muri, R.M., Ploner, C.J., Gaymard, B., Demeret, S., & Rivaud-Pechoux, S. (2003). Decisional role of the dorsolateral prefrontal cortex in ocular motor behaviour. Brain, 126(Pt 6), 14601473.
Pillon, B., Blin, J., Vidailhet, M., Deweer, B., Sirigu, A., Dubois, B., & Agid, Y. (1995). The neuropsychological pattern of corticobasal degeneration: Comparison with progressive supranuclear palsy and Alzheimer’s disease. Neurology, 45(8), 14771483.
Possin, K.L., Filoteo, J.V., Roesch, S.C., Zizak, V., Rilling, L.M., & Davis, J.D. (2005). Is a perseveration a perseveration? An evaluation of cognitive error types in patients with subcortical pathology. Journal of Clinical and Experimental Neuropsychology, 27(8), 953966.
Possin, K.L., Filoteo, J.V., Song, D.D., & Salmon, D.P. (2008). Spatial and object working memory deficits in Parkinson’s disease are due to impairment in different underlying processes. Neuropsychology, 22(5), 585595.
Possin, K.L., Filoteo, J.V., Song, D.D., & Salmon, D.P. (in press). Space-based but not object-based inhibition of return is impaired in Parkinson’s disease. Neuropsychologia.
Rabinovici, G.D., Seeley, W.W., Kim, E.J., Gorno-Tempini, M.L., Rascovsky, K., Pagliaro, T., Allison, S.C., Halabi, C., Kramer, J.H., Johnson, J.K., Weiner, M.W., Forman, M.S., Trojanowski, J.Q., Dearmond, S.J., Miller, B.L., & Rosen, H.J. (2007). Distinct MRI atrophy patterns in autopsy-proven Alzheimer’s disease and frontotemporal lobar degeneration. American Journal of Alzheimer’s Disease and Other Dementias, 22(6), 474488.
Rankin, K.P., Gorno-Tempini, M.L., Allison, S.C., Stanley, C.M., Glenn, S., Weiner, M.W., & Miller, B.L. (2006). Structural anatomy of empathy in neurodegenerative disease. Brain, 129(Pt 11), 29452956.
Rascovsky, K., Salmon, D.P., Lipton, A.M., Leverenz, J.B., DeCarli, C., Jagust, W.J., et al. (2005). Rate of progression differs in frontotemporal dementia and Alzheimer disease. Neurology, 65(3), 397403.
Reitan, R. (1993). The Halstead-Reitan Neuropsychological Test Battery: Theory and clinical interpretation. Tucson, AZ: Neuropsychology Press.
Rosen, H.J., Allison, S.C., Schauer, G.F., Gorno-Tempini, M.L., Weiner, M.W., & Miller, B.L. (2005). Neuroanatomical correlates of behavioural disorders in dementia. Brain, 128(Pt 11), 26122625.
Rosen, H.J., Gorno-Tempini, M.L., Goldman, W.P., Perry, R.J., Schuff, N., Weiner, M., Feiwell, R., Kramer, J.H., & Miller, B.L. (2002). Patterns of brain atrophy in frontotemporal dementia and semantic dementia. Neurology, 58(2), 198208.
Simmonds, D.J., Pekar, J.J., & Mostofsky, S.H. (2008). Meta-analysis of Go/No-go tasks demonstrating that fMRI activation associated with response inhibition is task-dependent. Neuropsychologia, 46(1), 224232.
Stokholm, J., Vogel, A., Gade, A., & Waldemar, G. (2006). Heterogeneity in executive impairment in patients with very mild Alzheimer’s disease. Dementia and Geriatric Cognitive Disorders, 22(1), 5459.
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(2), 230239.
Sullivan, E.V. & Sagar, H.J. (1991). Double dissociation of short-term and long-term memory for nonverbal material in Parkinson’s disease and global amnesia. A further analysis. Brain, 114(Pt 2), 893906.
Tabachnick, B.G. & Fidell, L.S. (2001). Using multivariate statistics (4th ed.). Needham Heights, MA: Allyn and Bacon.
Teri, L., Hughes, J.P., & Larson, E.B. (1990). Cognitive deterioration in Alzheimer’s disease: Behavioral and health factors. Journal of Gerontology, 45(2), P58P63.
Testa, C., Laakso, M.P., Sabattoli, F., Rossi, R., Beltramello, A., Soininen, H., & Frisoni, G.B. (2004). A comparison between the accuracy of voxel-based morphometry and hippocampal volumetry in Alzheimer’s disease. Journal of Magnetic Resonance Imaging, 19(3), 274282.
Tranel, D., Bechara, A., & Denburg, N.L. (2002). Asymmetric functional roles of right and left ventromedial prefrontal cortices in social conduct, decision-making, and emotional processing. Cortex, 38(4), 589612.
Viskontas, I.V., Possin, K.L., & Miller, B.L. (2007). Symptoms of frontotemporal dementia provide insights into orbitofrontal cortex function and social behavior. Annals of the New York Academy of Sciences, 1121, 528545.
Wallis, J.D., Anderson, K.C., & Miller, E.K. (2001). Single neurons in prefrontal cortex encode abstract rules. Nature, 411(6840), 953956.
Wittenberg, D., Possin, K.L., Rascovsky, K., Rankin, K.P., Miller, B.L., & Kramer, J.H. (2008). The early neuropsychological and behavioral characteristics of frontotemporal dementia. Neuropsychology Review, 18(1), 91102.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Journal of the International Neuropsychological Society
  • ISSN: 1355-6177
  • EISSN: 1469-7661
  • URL: /core/journals/journal-of-the-international-neuropsychological-society
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed