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Disinhibition in Frontotemporal Dementia and Alzheimer’s Disease: A Neuropsychological and Behavioural Investigation

Published online by Cambridge University Press:  23 September 2019

Luciano I. Mariano Open the ORCID record for Luciano I. Mariano [Opens in a new window] ,
Claire O’Callaghan ,
Henrique C. Guimarães ,
Leandro B. Gambogi ,
Thaís B.L. da Silva ,
Mônica S. Yassuda Open the ORCID record for Mônica S. Yassuda [Opens in a new window] ,
Juliana S. Amaral ,
Paulo Caramelli ,
Michael Hornberger  and
Antônio L. Teixeira
...Show all authors
Luciano I. Mariano
Affiliation:
Programa de Pós-Graduação em Neurociências, Universidade Federal de Minas Gerais (UFMG), Belo Horizonte, Minas Gerais (MG) 31270-901, Brazil Laboratório Interdisciplinar de Investigação Médica, Faculdade de Medicina da UFMG, Belo Horizonte, MG 30130-100, Brazil
Claire O’Callaghan
Affiliation:
Brain and Mind Research Institute, University of Sydney, Sydney 2050, Australia Department of Psychiatry, University of Cambridge, Cambridge CB2 0SZ, UK
Henrique C. Guimarães
Affiliation:
Programa de Pós-Graduação em Neurociências, Universidade Federal de Minas Gerais (UFMG), Belo Horizonte, Minas Gerais (MG) 31270-901, Brazil
Leandro B. Gambogi
Affiliation:
Programa de Pós-Graduação em Neurociências, Universidade Federal de Minas Gerais (UFMG), Belo Horizonte, Minas Gerais (MG) 31270-901, Brazil
Thaís B.L. da Silva
Affiliation:
Cognitive Behavior Neurology Group (GNCC), Neurology Department, University of São Paulo, São Paulo 05403-000, Brazil Gerontology, School of Arts, Sciences and Humanities, University of São Paulo, São Paulo 03828-000, Brazil
Mônica S. Yassuda
Affiliation:
Cognitive Behavior Neurology Group (GNCC), Neurology Department, University of São Paulo, São Paulo 05403-000, Brazil Gerontology, School of Arts, Sciences and Humanities, University of São Paulo, São Paulo 03828-000, Brazil
Juliana S. Amaral
Affiliation:
Laboratório Interdisciplinar de Investigação Médica, Faculdade de Medicina da UFMG, Belo Horizonte, MG 30130-100, Brazil
Paulo Caramelli
Affiliation:
Departamento de Clínica Médica, Faculdade de Medicina da UFMG, Belo Horizonte, MG 30130-100, Brazil
Michael Hornberger
Affiliation:
Norwich Medical School, University of East Anglia, Norwich NR4 7TJ, UK
Antônio L. Teixeira
Affiliation:
Laboratório Interdisciplinar de Investigação Médica, Faculdade de Medicina da UFMG, Belo Horizonte, MG 30130-100, Brazil Neuropsychiatry Program, Department of Psychiatry & Behavioral Sciences, UTHealth Houston, Houston, TX 77030, USA
Leonardo C. de Souza*
Affiliation:
Programa de Pós-Graduação em Neurociências, Universidade Federal de Minas Gerais (UFMG), Belo Horizonte, Minas Gerais (MG) 31270-901, Brazil Laboratório Interdisciplinar de Investigação Médica, Faculdade de Medicina da UFMG, Belo Horizonte, MG 30130-100, Brazil Departamento de Clínica Médica, Faculdade de Medicina da UFMG, Belo Horizonte, MG 30130-100, Brazil
*
Correspondence and reprint requests to: Leonardo Cruz de Souza, Laboratório Interdisciplinar de Investigação Médica, Faculdade de Medicina, Universidade Federal de Minas Gerais, Avenida Professor Alfredo Balena, no. 190/sl 281, Santa Efigênia, Belo Horizonte, MG 30130-100, Brazil. E-mail: [email protected]
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Abstract

Objective:

Cognitive tests of inhibitory control show variable results for the differential diagnosis between behavioural variant of Frontotemporal Dementia (bvFTD) and Alzheimer’s disease (AD). We compared the diagnostic accuracies of tests of inhibitory control and of a behavioural questionnaire, to distinguish bvFTD from AD.

Methods:

Three groups of participants were enrolled: 27 bvFTD patients, 25 AD patients, and 24 healthy controls. Groups were matched for gender, education, and socio-economic level. Participants underwent a comprehensive neuropsychological assessment of inhibitory control, including Hayling Test, Stroop, the Five Digits Test (FDT) and the Delay Discounting Task (DDT). Caregivers completed the Barratt Impulsiveness Scale 11th version (BIS-11).

Results:

bvFTD and AD groups showed no difference in the tasks of inhibitory control, while the caregiver questionnaire revealed that bvFTD patients were significantly more impulsive (BIS-11: bvFTD 76.1+9.5, AD 62.9+13, p < .001).

Conclusions:

Neuropsychological tests of inhibitory control failed to distinguish bvFTD from AD. On the contrary, impulsivity caregiver-completed questionnaire provided good distinction between bvFTD and AD. These results highlight the current limits of cognitive measures of inhibitory control for the differential diagnosis between bvFTD and AD, whereas questionnaire information appears more reliable and in line with clinical diagnostics.

Keywords

Behavioural variant Frontotemporal DementiaAlzheimer’s diseaseImpulsivityInhibitory controlDelay discountingExecutive function
Type
Regular Research
Information
Journal of the International Neuropsychological Society , Volume 26 , Issue 2 , February 2020 , pp. 163 - 171
Copyright
Copyright © INS. Published by Cambridge University Press, 2019 

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References

REFERENCES

Associação Brasileira de Empresas de Pesquisa – ABEP (2016). Critério Brasil 2015 e atualização da distribuição de classes para 2016. Critério de Classificação Econômica Brasil. Retrieved March 29, 2015, from http://www.abep.org/criterio-brasil.Google Scholar
Ballard, I.C., Kim, B., Liatsis, A., Aydogan, G., Cohen, J.D., & McClure, S.M. (2017). More is meaningful: the magnitude effect in intertemporal choice depends on self-control. Psychological Science, 28(10), 1443–1454.CrossRefGoogle ScholarPubMed
Beato, R.G., Nitrini, R., Formigoni, A.P., & Caramelli, P. (2007). Brazilian version of the Frontal Assessment Battery (FAB): Preliminary data on administration to healthy elderly. Dementia & Neuropsychologia, 1(1), 59–65.CrossRefGoogle ScholarPubMed
Bertoux, M., de Souza, L.C., Zamith, P., Dubois, B., & Bourgeois-Gironde, S. (2015). Discounting of future rewards in behavioural variant frontotemporal dementia and Alzheimer’s disease. Neuropsychology, 29(6), 933.CrossRefGoogle ScholarPubMed
Brucki, S., Nitrini, R., Caramelli, P., Bertolucci, P.H., & Okamoto, I.H. (2003). Suggestions for utilization of the mini-mental state examination in Brazil. Arquivos de neuro-psiquiatria, 61(3B), 777–781.CrossRefGoogle Scholar
Buhl, C., Stokholm, J., & Gade, A. (2013). Clinical utility of short social cognitive tests in early differentiation of behavioral variant frontotemporal dementia from Alzheimer’s disease. Dementia and Geriatric Cognitive Disorders Extra, 3(1), 376–385.CrossRefGoogle ScholarPubMed
Burgess, P.W., Alderman, N., Volle, E., Benoit, R.G., & Gilbert, S.J. (2009). Mesulam’s frontal lobe mystery re-examined. Restorative Neurology and Neuroscience, 27(5), 493–506.CrossRefGoogle ScholarPubMed
Castiglioni, S., Pelati, O., Zuffi, M., Somalvico, F., Marino, L., Tentorio, T., & Franceschi, M. (2006). The frontal assessment battery does not differentiate frontotemporal dementia from Alzheimer’s disease. Dementia and Geriatric Cognitive Disorders, 22(2), 125–131.CrossRefGoogle Scholar
Collette, F., Amieva, H., Adam, S., Hogge, M., Van der Linden, M., Fabrigoule, C., & Salmon, E. (2007). Comparison of inhibitory functioning in mild Alzheimer’s disease and frontotemporal dementia. Cortex, 43(7), 866–874.CrossRefGoogle ScholarPubMed
Dalley, J.W., Everitt, B.J., & Robbins, T.W. (2011). Impulsivity, compulsivity, and top-down cognitive control. Neuron, 69(4), 680–694.CrossRefGoogle ScholarPubMed
de Paula, J.J., Oliveira, T.D.O., Querino, E.H.G., & Malloy-Diniz, L.F. (2017). The Five Digits Test in the assessment of older adults with low formal education: Construct validity and reliability in a Brazilian clinical sample. Trends in Psychiatry and Psychotherapy, 39(3), 173–179.CrossRefGoogle Scholar
Diamond, A. (2013). Executive functions. Annual Review of Psychology, 64, 135–168.CrossRefGoogle ScholarPubMed
Ducharme, S., Price, B.H., & Dickerson, B.C. (2018). Apathy: A neurocircuitry model based on frontotemporal dementia. Journal of Neurology, Neurosurgery, and Psychiatry, 89(4), 389–396.CrossRefGoogle ScholarPubMed
Flanagan, E.C., Wong, S., Dutt, A., Tu, S., Bertoux, M., Irish, M., Piguet, O., Rao, S., Hodges, J.R., Ghosh, A., & Hornberger, M. (2016). False recognition in behavioral variant frontotemporal dementia and Alzheimer’s disease—disinhibition or amnesia? Frontiers in Aging Neuroscience, 8, 177.CrossRefGoogle ScholarPubMed
Green, L., Myerson, J., Holt, D.D., Slevin, J.R., & Estle, S.J. (2004). Discounting of delayed food rewards in pigeons and rats: Is there a magnitude effect? Journal of the Experimental Analysis of Behavior, 81(1), 39–50.CrossRefGoogle Scholar
Grochmal-Bach, B., Bidzan, L., Pachalska, M., Bidzan, M., Lukaszewska, B., & Pufal, A. (2009). Aggressive and impulsive behaviors in frontotemporal dementia and Alzheimer’s disease. Medical Science Monitor, 15(5), CR248–CR254.Google ScholarPubMed
Hampshire, A. & Sharp, D.J. (2015). Contrasting network and modular perspectives on inhibitory control. Trends in Cognitive Sciences, 19(8), 445–452.CrossRefGoogle ScholarPubMed
Heflin, L.H., Laluz, V., Jang, J., Ketelle, R., Miller, B.L., & Kramer, J.H. (2011). Let’s inhibit our excitement: The relationships between Stroop, behavioral disinhibition, and the frontal lobes. Neuropsychology, 25(5), 655.CrossRefGoogle ScholarPubMed
Hornberger, M., Savage, S., Hsieh, S., Mioshi, E., Piguet, O., & Hodges, J.R. (2010). Orbitofrontal dysfunction discriminates behavioral variant frontotemporal dementia from Alzheimer’s disease. Dementia and Geriatric Cognitive Disorders, 30(6), 547–552.CrossRefGoogle ScholarPubMed
Kertesz, A., Davidson, W., & Fox, H. (1997). Frontal behavioral inventory: Diagnostic criteria for frontal lobe dementia. Canadian Journal of Neurological Sciences, 24(1), 29–36.CrossRefGoogle ScholarPubMed
Kim, S. & Lee, D. (2011). Prefrontal cortex and impulsive decision making. Biological Psychiatry, 69(12), 1140–1146.CrossRefGoogle ScholarPubMed
Kirby, K.N., Petry, N.M., & Bickel, W.K. (1999). Heroin addicts have higher discount rates for delayed rewards than non-drug-using controls. Journal of Experimental Psychology: General, 128(1), 78.CrossRefGoogle ScholarPubMed
Lansdall, C.J., Coyle-Gilchrist, I.T., Jones, P.S., Vázquez Rodríguez, P., Wilcox, A., Wehmann, E., Dick, K.M., Robbins, T.W., & Rowe, J.B. (2017). Apathy and impulsivity in frontotemporal lobar degeneration syndromes. Brain, 140(6), 1792–1807.CrossRefGoogle ScholarPubMed
Le Ber, I., Guedj, E., Gabelle, A., Verpillat, P., Volteau, M., Thomas-Anterion, C., Decousus, M., Hannequin, D., Véra, P., Lacomblez, L., Camuzat, A., Didier, H., Puel, M., Lotterie, J., Golfier, V., Bernard, A., Vercelletto, M., Magne, C., Sellal, F., Namer, I., Michel, B., Pasquier, J., Salachas, F., Bochet, J., Brice, A., Habert, M., & Dubois, B. (2006). Demographic, neurological and behavioural characteristics and brain perfusion SPECT in frontal variant of frontotemporal dementia. Brain, 129, 3051–3065.CrossRefGoogle ScholarPubMed
Lebreton, M., Bertoux, M., Boutet, C., Lehericy, S., Dubois, B., Fossati, P., & Pessiglione, M. (2013). A critical role for the hippocampus in the valuation of imagined outcomes. PLoS Biology, 11(10), e1001684.CrossRefGoogle ScholarPubMed
Leslie, F.V.C., Foxe, D., Daveson, N., Flannagan, E., Hodges, J.R., & Piguet, O. (2016). FRONTIER Executive Screen: A brief executive battery to differentiate frontotemporal dementia and Alzheimer’s disease. Journal of Neurology, Neurosurgery, and Psychiatry, 87(8), 831–835.CrossRefGoogle ScholarPubMed
Machado, T.H., Fichman, H.C., Santos, E.L., Carvalho, V.A., Fialho, P.P., Koenig, A.M., Fernandes, C.S., Lourenço, R.A., de Paiva Paradela, E.M., & Caramelli, P. (2009). Normative data for healthy elderly on the phonemic verbal fluency task-FAS. Dementia & Neuropsychologia, 3(1), 55–60.CrossRefGoogle Scholar
Magalhães, C.A., Figueiró, M., Fraga, V.G., Mateo, E.C., Toledo, A.A., Carvalho, M.D.G., Caramelli, P., & Gomes, K.B. (2015). Cerebrospinal fluid biomarkers for the differential diagnosis of Alzheimer’s disease. Jornal Brasileiro de Patologia e Medicina Laboratorial, 51(6), 376–382.CrossRefGoogle Scholar
Malloy, P., Tremont, G., Grace, J., & Frakey, L. (2007). The Frontal Systems Behavior Scale discriminates frontotemporal dementia from Alzheimer’s disease. Alzheimer’s & Dementia, 3(3), 200–203.CrossRefGoogle ScholarPubMed
Malloy-Diniz, L.F., Mattos, P., Leite, W.B., Abreu, N., Coutinho, G., Paula, J.J.D., Tavaresv, H., Vasconcelos, A.G., & Fuentes, D. (2010). Tradução e adaptação cultural da Barratt Impulsiveness Scale (BIS-11) para aplicação em adultos brasileiros. Jornal Brasileiro de Psiquiatria, 59(2), 99–105.CrossRefGoogle Scholar
Malloy-Diniz, L.F., Paula, J.J.D., Vasconcelos, A.G., Almondes, K.M.D., Pessoa, R., Faria, L., Coutinho, G., Costa, D.S., Duran, V., Coutinho, T.V., Corrêa, H., Fuentes, D., Abreu, N., & Mattos, P. (2015). Normative data of the Barratt Impulsiveness Scale 11 (BIS-11) for Brazilian adults. Revista Brasileira de Psiquiatria, 37(3), 245–248.CrossRefGoogle ScholarPubMed
Massimo, L., Powers, C., Moore, P., Vesely, L., Avants, B., Gee, J., Libon, D.J., & Grossman, M. (2009). Neuroanatomy of apathy and disinhibition in frontotemporal lobar degeneration. Dementia and Geriatric Cognitive Disorders, 27(1), 96–104.CrossRefGoogle ScholarPubMed
Matías-Guiu, J.A., Cabrera-Martín, M.N., Valles-Salgado, M., Rognoni, T., Galán, L., Moreno-Ramos, T., Carreras, J.L., & Matías-Guiu, J. (2019). Inhibition impairment in frontotemporal dementia, amyotrophic lateral sclerosis, and Alzheimer’s disease: clinical assessment and metabolic correlates. Brain Imaging and Behavior, 13, 651–659.CrossRefGoogle ScholarPubMed
McKhann, G.M., Knopman, D.S., Chertkow, H., Hyman, B.T., Jack, C.R. Jr, Kawas, C.H., Klunk, W.E., Koroshetz, W.J., Manly, J.J., Mayeux, R., Mohs, R.C., Morris, J.C., Rossor, M.N., Scheltens, P., Carrillo, M.C., Thies, B., Weintraud, S., & Phelps, C.H. (2011). The diagnosis of dementia due to Alzheimer’s disease: Recommendations from the National Institute on Aging-Alzheimer’s Association workgroups on diagnostic guidelines for Alzheimer’s disease. Alzheimer’s & dementia, 7(3), 263–269.CrossRefGoogle Scholar
Nitrini, R., Caramelli, P., Porto, C.S., Charchat-Fichman, H., Formigoni, A.P., Carthery-Goulart, M.T., Otero, C., & Prandini, J.C. (2007). Brief cognitive battery in the diagnosis of mild Alzheimer’s disease in subjects with medium and high levels of education. Dementia & Neuropsychologia, 1(1), 32–36.CrossRefGoogle Scholar
O’Callaghan, C., Hodges, J.R., & Hornberger, M. (2013a). Inhibitory dysfunction in frontotemporal dementia: A review. Alzheimer Disease & Associated Disorders, 27(2), 102–108.CrossRefGoogle ScholarPubMed
O’Callaghan, C., Naismith, S.L., Hodges, J.R., Lewis, S.J., & Hornberger, M. (2013b). Fronto-striatal atrophy correlates of inhibitory dysfunction in Parkinson’s disease versus behavioural variant frontotemporal dementia. Cortex, 49(7), 1833–1843.CrossRefGoogle ScholarPubMed
O’Connor, C.M., Landin-Romero, R., Clemson, L., Kaizik, C., Daveson, N., Hodges, J.R., Hsieh, S., Piguet, O., & Mioshi, E. (2017). Behavioral-variant frontotemporal dementia – Distinct phenotypes with unique functional profiles. Neurology, 89(6), 570–577.CrossRefGoogle ScholarPubMed
Paholpak, P., Carr, A.R., Barsuglia, J.P., Barrows, R.J., Jimenez, E., Lee, G.J., & Mendez, M.F. (2016). Person-based versus generalized impulsivity disinhibition in frontotemporal dementia and Alzheimer disease. Journal of Geriatric Psychiatry and Neurology, 29(6), 344–351.CrossRefGoogle ScholarPubMed
Perry, R.J. & Hodges, J.R. (2000). Differentiating frontal and temporal variant frontotemporal dementia from Alzheimer’s disease. Neurology, 54(12), 2277–2284.CrossRefGoogle ScholarPubMed
Rachlin, H. (2000). The science of self-control. Cambridge: Harvard University Press.Google Scholar
Ramanan, S., Bertoux, M., Flanagan, E., Irish, M., Piguet, O., Hodges, J.R., & Hornberger, M. (2017). Longitudinal executive function and episodic memory profiles in behavioral-variant frontotemporal dementia and Alzheimer’s disease. Journal of the International Neuropsychological Society, 23(1), 34–43.CrossRefGoogle ScholarPubMed
Rascovsky, K., Hodges, J.R., Knopman, D., Mendez, M.F., Kramer, J.H., Neuhaus, J., Swieten, J.C., Seelaar, H., Dopper, E.G.P., Onyke, C.U., Hillis, A.E., Josephs, K.A., Boeve, B.F., Ketesz, A., Seeley, W.W., Rankin, K.P., Johnson, J.K., Gorno-Tempini, M., Rosen, H., Prioleau-Latham, C.E., Lee, A., Kipps, C.M., Lillo, P., Piguet, O., Rohrer, J.D., Rossor, M.N., Warren, J.D., Fox, N.C., Galasko, D., Salmon, D.P., Black, S.E., Mesulam, M., Weintraud, S., Dickerson, B.C., Diehl-Schmid, J., Pasquier, F., Deramecourt, V., Lebert, F., Pijinenburg, Y., Chow, T.W., Manes, F., Grafman, J., Cappa, S.F., Freedman, M., Grossman, M., & Miller, B.L. (2011). Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain, 134(9), 2456–2477.CrossRefGoogle ScholarPubMed
Schubert, S., Leyton, C.E., Hodges, J.R., & Piguet, O. (2016). Longitudinal memory profiles in behavioral-variant frontotemporal dementia and Alzheimer’s disease. Journal of Alzheimer’s Disease, 51(3), 775–782.CrossRefGoogle ScholarPubMed
Siqueira, L.D.S., Scherer, L.C., Reppold, C.T., & Fonseca, R.P. (2010). Hayling test-adult version: Applicability in the assessment of executive functions in children. Psychology & Neuroscience, 3(2), 189–194.CrossRefGoogle Scholar
Strauss, E., Sherman, E.M., & Spreen, O. (2006). A compendium of neuropsychological tests. Oxford: Oxford University Press.Google Scholar
Vestberg, S., Nordström, E.B., Waldö, M.L., Nilsson, K., Santillo, A.F., & Nilsson, C. (2019). Swedish version of the Hayling test: Clinical utility in frontotemporal dementia syndromes. Journal of the International Neuropsychological Society, 25(2), 195–203.CrossRefGoogle ScholarPubMed
Volle, E., Costello, A.L., Coates, L.M., McGuire, C., Towgood, K., Gilbert, S., Kinkingnehun, S., McNeil, J.E., Greenwood, R., Papps, B., den Broeck, M., & Burgess, P.W. (2011). Dissociation between verbal response initiation and suppression after prefrontal lesions. Cerebral Cortex, 22(10), 2428–2440.CrossRefGoogle ScholarPubMed
Wechsler, D. (1997). WAIS-III, Wechsler adult intelligence scale: administration and scoring manual. San Antonio, TX: Psychological Corporation.Google Scholar
Wedderburn, C., Wear, H., Brown, J., Mason, S.J., Barker, R.A., Hodges, J., & Williams-Gray, C. (2008). The utility of the Cambridge Behavioural Inventory in neurodegenerative disease. Journal of Neurology, Neurosurgery & Psychiatry, 79(5), 500–503.CrossRefGoogle ScholarPubMed
Zamboni, G., Huey, E.D., Krueger, F., Nichelli, P.F., & Grafman, J. (2008). Apathy and disinhibition in frontotemporal dementia: insights into their neural correlates. Neurology, 71(10), 736–742.CrossRefGoogle ScholarPubMed