Theoretical exploration of the neural bases of behavioural disinhibition, apathy and executive dysfunction in preclinical Alzheimer's disease in people with Down's syndrome: Potential involvement of multiple frontal-subcortical neuronal circuits

Journal article


Ball, S., Holland, Anne, Watson, P. and Huppert, Felicia. (2010) Theoretical exploration of the neural bases of behavioural disinhibition, apathy and executive dysfunction in preclinical Alzheimer's disease in people with Down's syndrome: Potential involvement of multiple frontal-subcortical neuronal circuits. Journal of Intellectual Disability Research. 54(4), pp. 320 - 336. https://doi.org/10.1111/j.1365-2788.2010.01261.x
AuthorsBall, S., Holland, Anne, Watson, P. and Huppert, Felicia
Abstract

Background:  Recent research has suggested a specific impairment in frontal‐lobe functioning in the preclinical stages of Alzheimer's disease (AD) in people with Down's syndrome (DS), characterised by prominent changes in personality or behaviour. The aim of the current paper is to explore whether particular kinds of change (namely executive dysfunction (EDF), disinhibition and apathy), associated in the literature with disruption of different underlying frontal‐subcortical circuits, are a) more or less frequently reported than others and b) related to poor performance on tasks involving different cognitive processes.

Method:  Seventy‐eight participants (mean age 47 years, range 36–72) with DS and mild to moderate intellectual disability (based on ICD‐10 criteria), without a diagnosis of dementia of Alzheimer's type (DAT) or other psychiatric disorders, were selected from a larger sample of older adults with DS (n = 122). Dementia diagnosis was based on the CAMDEX informant interview, conducted with each participant's main carer. Informant‐reported changes in personality/behaviour and memory were recorded. Participants were scored based on symptoms falling into three behavioural domains and completed five executive function (EF) tasks, six memory tasks (two of which also had a strong executive component) and the BPVS (as a measure of general intellectual ability). Multiple regression analyses were conducted to determine the degree to which the behavioural variables of ‘EDF’, ‘disinhibition’ and ‘apathy’, along with informant‐reported memory decline and antidepressant medication use, predicted performance on the cognitive tasks (whilst controlling for the effects of age and general intellectual ability).

Results:  Strikingly, disinhibited behaviour was reported for 95.7% of participants with one or more behavioural change (n = 47) compared to 57.4% with reported apathy and 36.2% with reported EDF. ‘Disinhibition’ score significantly predicted performance on three EF tasks (designed to measure planning, response inhibition and working memory) and an object memory task, (also thought to place high demands on working memory), while ‘apathy’ score significantly predicted performance on two different tasks, those measuring spatial reversal and prospective memory (p < 0.05). Informant reported memory decline was associated only with performance on a delayed recall task while antidepressant medication use was associated with better performance on a working memory task (p < 0.05).

Conclusion:  Observed dissociation between performance on cognitive tasks associated with reported apathy and disinhibition is in keeping with proposed differences underlying neural circuitry and supports the involvement of multiple frontal‐subcortical circuits in the early stages of DAT in DS. However, the prominence of disinhibition in the behavioural profile (which more closely resembles that of disinhibited subtype of DFT than that of AD in the general population) leads us to postulate that the serotonergically mediated orbitofrontal circuit may be disproportionately affected. A speculative theory is developed regarding the biological basis for observed changes and discussion is focused on how this understanding may aid us in the development of treatments directly targeting underlying abnormalities.

Year2010
JournalJournal of Intellectual Disability Research
Journal citation54 (4), pp. 320 - 336
PublisherWiley-Blackwell Publishing Ltd.
ISSN0964-2633
Digital Object Identifier (DOI)https://doi.org/10.1111/j.1365-2788.2010.01261.x
Scopus EID2-s2.0-77952487837
Page range320 - 336
Place of publicationUnited Kingdom
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Ramachandra, Pranathi, Booth, Sara, Pieters, Thirza, Vrotsou, Kalliopi and Huppert, Felicia. (2009) A brief self-administered psychological intervention to improve well-being in patients with cancer: Results from a feasibility study. Psycho-Oncology: journal of the psychological, social and behavioral dimensions of cancer. 18(12), pp. 1323 - 1326. https://doi.org/10.1002/pon.1516
Hormone replacement therapy to maintain cognitive function in women with dementia
Hogervorst, E., Yaffe, K., Richards, Marcus and Huppert, Felicia. (2009) Hormone replacement therapy to maintain cognitive function in women with dementia. Cochrane Database of Systematic Reviews. https://doi.org/10.1002/14651858.CD003799.pub2
Information communication technology as a means of enhancing the well-being of older people
Johnson, Daniel and Huppert, Felicia. (2009) Information communication technology as a means of enhancing the well-being of older people. In Behaviour monitoring and interpretation: BMI pp. 11 - 25 IOS Press.
Neuropathological correlates of dementia in over-80-year-old brain donors from the population-based Cambridge city over-75s cohort (CC75C) study
Brayne, Carol, Richardson, Kathryn, Matthews, Fiona E., Fleming, Jane, Hunter, Sally, Xuereb, John H., Paykel, Eugene S., Mukaetova-Ladinska, Elizabeta B., Huppert, Felicia, O'Sullivan, Angela and Dening, Tom. (2009) Neuropathological correlates of dementia in over-80-year-old brain donors from the population-based Cambridge city over-75s cohort (CC75C) study. Journal of Alzheimer's Disease. 18(3), pp. 645 - 658. https://doi.org/10.3233/JAD-2009-1182
A new approach to reducing disorder and improving well-being
Huppert, Felicia. (2009) A new approach to reducing disorder and improving well-being. Perspectives on Psychological Science. 4(1), pp. 108 - 111. https://doi.org/10.1111/j.1745-6924.2009.01100.x
Education and trajectories of cognitive decline over 9 years in very old people: Methods and risk analysis
Muniz-Terrera, Graciela, Matthews, Fiona E., Dening, Tom, Huppert, Felicia A. and Brayne, Carol. (2009) Education and trajectories of cognitive decline over 9 years in very old people: Methods and risk analysis. Age and Ageing. 38(3), pp. 277 - 282. https://doi.org/10.1093/ageing/afp004
Psychological well-being: Evidence regarding its causes and consequences
Huppert, Felicia. (2009) Psychological well-being: Evidence regarding its causes and consequences. Applied Psychology: Health and Well-Being. 1(2), pp. 137 - 164. https://doi.org/10.1111/j.1758-0854.2009.01008.x
Cognitive health among older adults in the United States and in England
Langa, Kenneth M., Llewellyn, David J., Lang, Iain A., Weir, David R., Wallace, Robert B., Kabeto, Mohammed U. and Huppert, Felicia A.. (2009) Cognitive health among older adults in the United States and in England. BMC Geriatrics. 9(1), pp. 1 - 11. https://doi.org/10.1186/1471-2318-9-23
Measuring well-being across Europe: Description of the ESS Well-being Module and preliminary findings
Huppert, Felicia A., Marks, Nic, Clark, Andrew, Siegrist, Johannes, Stutzer, Alois, Vitterso, Joar and Wahrendorf, Morten. (2009) Measuring well-being across Europe: Description of the ESS Well-being Module and preliminary findings. Social Indicators Research. 91(3), pp. 301 - 315. https://doi.org/10.1007/s11205-008-9346-0
The relationship between early personality and midlife psychological well-being: Evidence from a UK birth cohort study
Abbott, Rosemary A., Croudace, Tim J., Ploubidis, George B., Kuh, Diana, Richards, Marcus and Huppert, Felicia A.. (2008) The relationship between early personality and midlife psychological well-being: Evidence from a UK birth cohort study. Social Psychiatry and Psychiatric Epidemiology. 43(9), pp. 679 - 687. https://doi.org/10.1007/s00127-008-0355-8
Ascertaining late-life depressive symptoms in Europe: An evaluation of the survey version of the EURO-D scale in 10 nations. The SHARE project
Castro-Costa, Erico, Dewey, Michael, Stewart, Robert, Banerjee, Sube, Huppert, Felicia, Mendonca-Lima, Carlos, Bula, Christophe, Reisches, Friedel, Wancata, Johannes, Ritchie, Karen, Tsolaki, Magda, Mateos, Raimundo and Prince, Martin. (2008) Ascertaining late-life depressive symptoms in Europe: An evaluation of the survey version of the EURO-D scale in 10 nations. The SHARE project. International Journal of Methods in Psychiatric Research. 17(1), pp. 12 - 29. https://doi.org/10.1002/mpr.236
Thyroid function and cognitive decline in the MRC Cognitive Function and Ageing Study
Hogervorst, Eef, Huppert, Felicia, Matthews, Fiona E. and Brayne, Carol. (2008) Thyroid function and cognitive decline in the MRC Cognitive Function and Ageing Study. Psychoneuroendocrinology. 33(7), pp. 1013 - 1022. https://doi.org/10.1016/j.psyneuen.2008.05.008
Long-term DHEA replacement in primary adrenal insufficiency: A randomized, controlled trial
Gurnell, Eleanor M., Hunt, Penelope J., Curran, Zusanne E., Conway, Catherine L., Pullenayegum, Eleanor M., Huppert, Felicia A., Compston, Juliet E., Herbert, Joseph and Chatterjee, V. Krishna K.. (2008) Long-term DHEA replacement in primary adrenal insufficiency: A randomized, controlled trial. Journal of Clinical Endocrinology and Metabolism. 93(2), pp. 400 - 409. https://doi.org/10.1210/jc.2007-1134
Executive dysfunction and its association with personality and behaviour changes in the development of Alzheimer's disease in adults with Down syndrome and mild to moderate learning disabilities
Ball, Sarah L., Holland, Anthony J., Treppner, Peter, Watson, Peter C. and Huppert, Felicia A.. (2008) Executive dysfunction and its association with personality and behaviour changes in the development of Alzheimer's disease in adults with Down syndrome and mild to moderate learning disabilities. British Journal of Clinical Psychology. 47, pp. 1 - 29. https://doi.org/10.1348/014466507X230967
The mental wealth of nations
Beddington, John, Cooper, Cary L., Field, John, Goswami, Usha, Huppert, Felicia A., Jenkins, Rachel, Jones, Hannah S., Kirkwood, Tom B. L., Sahakian, Barbara J. and Thomas, Sandy M.. (2008) The mental wealth of nations. Nature. 455(7216), pp. 1057 - 1060. https://doi.org/10.1038/4551057a
Cognitive function and psychological well-being: Findings from a population-based cohort
Llewellyn, David J., Lang, Iain A., Langa, Kenneth M. and Huppert, Felicia A.. (2008) Cognitive function and psychological well-being: Findings from a population-based cohort. Age and Ageing. 37(6), pp. 685 - 689. https://doi.org/10.1093/ageing/afn194
Neighborhood deprivation, individual socioeconimic status, and cognitive function in older people: Analyses from the English Longitudinal Study of Ageing
Lang, Iain A., Llewellyn, David J., Langa, Kenneth M., Wallace, Robert B., Huppert, Felicia A. and Melzer, David. (2008) Neighborhood deprivation, individual socioeconimic status, and cognitive function in older people: Analyses from the English Longitudinal Study of Ageing. Journal of the American Geriatrics Society. 56, pp. 191 - 198. https://doi.org/10.1111/j.1532-5415.2007.01557.x
Framingham Stroke Risk Profile and poor cognitive function: A population-based study
Llewellyn, David J., Lang, Iain A., Xie, Jing, Huppert, Felicia A., Melzer, David and Langa, Kenneth M.. (2008) Framingham Stroke Risk Profile and poor cognitive function: A population-based study. BMC Neurology. 8(12), pp. 1 - 8. https://doi.org/10.1186/1471-2377-8-12
Moderate alcohol consumption in older adults is associated with better cognition and well-being than abstinence
Lang, I. A., Wallace, R. B., Huppert, Felicia and Melzer, D. (2007) Moderate alcohol consumption in older adults is associated with better cognition and well-being than abstinence. Age and Ageing. 36(3), pp. 256 - 261. https://doi.org/10.1093/ageing/afm001
WITHDRAWN: Dehydroepiandrosterone (DHEA) supplementation for cognitive function.
Huppert, Felicia and Van Niekerk, J. K.. (2007) WITHDRAWN: Dehydroepiandrosterone (DHEA) supplementation for cognitive function. Cochrane Database of Systematic Reviews. 18(3).
Cohort differences in disease and disability in the young-old: Findings from the MRC Cognitive Function and Ageing Study (MRC-CFAS)
Jagger, Carol, Matthews, Ruth J., Matthews, F. E., Spiers, Nicola A., Nickson, Judith, Paykel, E S., Huppert, Felicia and Brayne, C. (2007) Cohort differences in disease and disability in the young-old: Findings from the MRC Cognitive Function and Ageing Study (MRC-CFAS). BMC Public Health. 7(1). https://doi.org/10.1186/1471-2458-7-156
Improvements in social functioning reported by a birth cohort in mid-adult life: A person-centred analysis of GHQ-28 social dysfunction items using latent class analysis
Ploubidis, George B., Abbott, Rosemary A., Huppert, Felicia, Kuh, Diana, Wadsworth, Michael E. J. and Croudace, Tim J.. (2007) Improvements in social functioning reported by a birth cohort in mid-adult life: A person-centred analysis of GHQ-28 social dysfunction items using latent class analysis. Personality and Individual Differences. 42(2), pp. 305 - 316. https://doi.org/10.1016/j.paid.2006.07.010
Was John Reid right? Smoking, class, and pleasure: A population-based cohort study in England
Lang, I. A., Gardener, Elizabeth A., Huppert, Felicia and Melzer, D. (2007) Was John Reid right? Smoking, class, and pleasure: A population-based cohort study in England. Public Health. 121(7), pp. 518 - 524. https://doi.org/10.1016/j.puhe.2007.01.005
The Women's International Study of Long-duration Oestrogen after Menopause (WISDOM): A randomised controlled trial
Vickers, Madge, Martin, Jeannett, Meade, Tom W., Arasaratnum, N., Collins, N., Furness, P., Ghali, M., Gordon, E., Huppert, Felicia, Islam, Z., Knott, C., Meredith, S., Prince, M., Purdon, S., Richards, Marcus, Taylor, L., Welton, A., Zhu, C. Q., Zuhrie, R., ... MacLennon, A.. (2007) The Women's International Study of Long-duration Oestrogen after Menopause (WISDOM): A randomised controlled trial. BMC Women's Health. 7(1). https://doi.org/10.1186/1472-6874-7-2
Prevalence of depressive symptoms and syndromes in later life in ten European countries: The SHARE study
Castro-Costa, E., Dewey, M., Stewart, Robert, Banerjee, S, Huppert, Felicia, Mendonca-Lima, C, Bula, C, Reisches, F, Wancata, J, Ritchie, K, Tsolaki, M, Mateos, R and Prince, M. (2007) Prevalence of depressive symptoms and syndromes in later life in ten European countries: The SHARE study. British Journal of Psychiatry. 191(NOV.), pp. 393 - 401. https://doi.org/10.1192/bjp.bp.107.036772
A randomised controlled trial investigating the effect of n-3 long-chain polyunsaturated fatty acid supplementation on cognitive and retinal function in cognitively healthy older people: The Older People and n-3 Long-chain polyunsaturated fatty acids
Alan, Dangour D., Clemens, Felicity, Elbourne, Diana, Fasey, Nicky, Fletcher, Astrid E., Hardy, Pollyanna, Holder, Graham E., Huppert, Felicia, Knight, Rosemary, Letley, Louise, Richards, Marcus, Truesdale, Ann, Vickers, Madge and Uauy, Ricardo. (2006) A randomised controlled trial investigating the effect of n-3 long-chain polyunsaturated fatty acid supplementation on cognitive and retinal function in cognitively healthy older people: The Older People and n-3 Long-chain polyunsaturated fatty acids. Nutrition Journal. 5, p. 1. https://doi.org/10.1186/1475-2891-5-20
Personality and behaviour changes mark the early stages of Alzheimer's disease in adults with Down's syndrome: Findings from a prospective population-based study
Ball, Sarah L., Holland, Anthony J., Hon, Johnny, Huppert, Felicia, Treppner, P and Watson, P C.. (2006) Personality and behaviour changes mark the early stages of Alzheimer's disease in adults with Down's syndrome: Findings from a prospective population-based study. International Journal of Geriatric Psychiatry. 21(7), pp. 661 - 673. https://doi.org/10.1002/gps.1545
Low prevalence of depression and anxiety is linked to statutory retirement ages rather than personal work exit: A national survey
Villamil, Elena, Huppert, Felicia and Melzer, D.. (2006) Low prevalence of depression and anxiety is linked to statutory retirement ages rather than personal work exit: A national survey. Psychological Medicine. 36(7), pp. 999 - 1009. https://doi.org/10.1017/S0033291706007719
Psychometric evaluation and predictive validity of Ryff's psychological well-being items in a UK birth cohort sample of women
Abbott, Rosemary A., Ploubidis, George B., Huppert, Felicia, Kuh, Diana, Wadsworth, Michael E. J. and Croudace, Tim J.. (2006) Psychometric evaluation and predictive validity of Ryff's psychological well-being items in a UK birth cohort sample of women. Health and Quality of Life Outcomes. 4(1), pp. 1 - 16. https://doi.org/10.1186/1477-7525-4-76
Middle-aged and mobility-limited: Prevalence of disability and symptom attributions in a national survey
Gardener, Elizabeth A., Huppert, Felicia, Guralnik, Jack M. and Melzer, D. (2006) Middle-aged and mobility-limited: Prevalence of disability and symptom attributions in a national survey. Journal of General Internal Medicine. 21(10), pp. 1091 - 1096. https://doi.org/10.1111/j.1525-1497.2006.00564.x
Dehydroepiandrosterone (DHEA) supplementation for cognitive function in healthy elderly people
Evans, J. Grimley, Malouf, R., Huppert, Felicia and Van Niekerk, J. K.. (2006) Dehydroepiandrosterone (DHEA) supplementation for cognitive function in healthy elderly people. Cochrane Database of Systematic Reviews. https://doi.org/10.1002/14651858.CD006221