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Journal of Neurology

, Volume 266, Issue 6, pp 1323–1331 | Cite as

Sustained attention failures on a 3-min reaction time task is a sensitive marker of dementia

  • Aurélie L. ManuelEmail author
  • David Foxe
  • Nathan Bradshaw
  • Nicholas J. Cordato
  • John R. Hodges
  • James R. Burrell
  • Olivier Piguet
Original Communication

Abstract

The objective of the study is to determine the utility of a simple reaction time task as a marker of general cognitive decline across the frontotemporal lobar degeneration (FTLD) spectrum and in Alzheimer’s disease (AD). One hundred and twelve patients presenting with AD or FTLD affecting behaviour (behavioural-variant frontotemporal dementia), language (progressive non fluent aphasia, logopenic progressive aphasia, semantic dementia) or motor function (corticobasal syndrome, progressive supranuclear palsy, frontotemporal dementia–motor neuron disease) and 25 age-matched healthy controls completed the Psychomotor Vigilance Task (PVT), a 3-min reaction time (RT) task. The proportion of lapses (RT > 500 ms) was significantly increased in dementia patients compared to healthy controls, except for semantic dementia, and correlated with all cognitive functions except language. Discrimination of individuals (dementia patients versus healthy controls) based on the proportion of lapses yielded the highest classification performance (Area Under the Curve, AUC, 0.90) compared to standard neuropsychological tests. Only the complete and lengthy neuropsychological battery had a higher predictive value (AUC 0.96). The basic ability to sustain attention is fundamental to perform any cognitive task. Lapses, interpreted as momentary shifts in goal-directed processing, can therefore, be used as a marker of general cognitive decline indicative of possible dementia.

Keywords

Sustained attention Vigilance Neurodegenerative disorders Dementia Reaction time Psychomotor vigilance task 

Notes

Acknowledgements

This work was supported in part by funding to ForeFront, a collaborative research group dedicated to the study of frontotemporal dementia and motor neuron disease, from the National Health and Medical Research Council (NHMRC) (APP1037746) and the Australian Research Council (ARC) Centre of Excellence in Cognition and its Disorders Memory Program (CE11000102). ALM is supported by the Swiss National Science Foundation (P300P1_171478), JRB was supported by an NHMRC Early Career Fellowship (1072451) and OP is supported by an NHMRC Senior Research Fellowship (APP1103258).

Compliance with ethical standards

Conflicts of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Supplementary material

415_2019_9261_MOESM1_ESM.docx (22 kb)
Supplementary material 1 (DOCX 21 KB)

References

  1. 1.
    Unsworth N, Redick TS, Lakey CE, Young DL (2010) Lapses in sustained attention and their relation to executive control and fluid abilities: an individual differences investigation. Intelligence 38:111–122CrossRefGoogle Scholar
  2. 2.
    Wilkins AJ, Shallice T, McCarthy R (1987) Frontal lesions and sustained attention. Neuropsychologia 25:359–365CrossRefGoogle Scholar
  3. 3.
    Parasuraman R, Nestor PG (1991) Attention and driving skills in aging and Alzheimer’s disease. Hum Factors 33:539–557CrossRefGoogle Scholar
  4. 4.
    Taylor ME, Lord SR, Delbaere K, Mikolaizak AS, Close JC (2012) Physiological fall risk factors in cognitively impaired older people: a one-year prospective study. Dement Geriatr Cogn Disord 34:181–189CrossRefGoogle Scholar
  5. 5.
    Bailon O, Roussel M, Boucart M, Krystkowiak P, Godefroy O (2010) Psychomotor slowing in mild cognitive impairment, Alzheimer’s disease and lewy body dementia: mechanisms and diagnostic value. Dement Geriatr Cogn Disord 29:388–396CrossRefGoogle Scholar
  6. 6.
    Park M, Hood MM, Shah RC, Fogg LF, Wyatt JK (2012) Sleepiness, parkinsonian features and sustained attention in mild Alzheimer’s disease. Age Ageing 41:765–770CrossRefGoogle Scholar
  7. 7.
    Phillips M, Rogers P, Haworth J, Bayer A, Tales A (2013) Intra-individual reaction time variability in mild cognitive impairment and Alzheimer’s disease: gender, processing load and speed factors. PLoS One 8:e65712CrossRefGoogle Scholar
  8. 8.
    Wallert J, Westman E, Ulinder J, Annerstedt M, Terzis B, Ekman U (2018) Differentiating patients at the memory clinic with simple reaction time variables: a predictive modeling approach using support vector machines and Bayesian optimization. Front Aging Neurosci 10:144CrossRefGoogle Scholar
  9. 9.
    Kochan NA, Bunce D, Pont S, Crawford JD, Brodaty H, Sachdev PS (2016) Reaction time measures predict incident dementia in community-living older adults: the Sydney Memory and Ageing Study. Am J Geriatr Psychiatry 24:221–231CrossRefGoogle Scholar
  10. 10.
    Tales A, Leonards U, Bompas A, Snowden RJ, Philips M, Porter G, Haworth J, Wilcock G, Bayer A (2012) Intra-individual reaction time variability in amnestic mild cognitive impairment: a precursor to dementia? J Alzheimers Dis 32:457–466CrossRefGoogle Scholar
  11. 11.
    Hodges JR (2013) Alzheimer’s disease and the frontotemporal dementias: contributions to clinico-pathological studies, diagnosis, and cognitive neuroscience. J Alzheimers Dis 33(Suppl 1):S211–S217Google Scholar
  12. 12.
    Murtha S, Cismaru R, Waechter R, Chertkow H (2002) Increased variability accompanies frontal lobe damage in dementia. J Int Neuropsychol Soc 8:360–372CrossRefGoogle Scholar
  13. 13.
    Donders FC (1969) On the speed of mental processes. Acta Psychol (Amst) 30:412–431CrossRefGoogle Scholar
  14. 14.
    Lim J, Dinges DF (2008) Sleep deprivation and vigilant attention. Ann N Y Acad Sci 1129:305–322CrossRefGoogle Scholar
  15. 15.
    Basner M, Dinges DF (2011) Maximizing sensitivity of the psychomotor vigilance test (PVT) to sleep loss. Sleep 34:581–591CrossRefGoogle Scholar
  16. 16.
    Rascovsky K, Hodges JR, Knopman D, Mendez MF, Kramer JH, Neuhaus J, van Swieten JC, Seelaar H, Dopper EG, Onyike CU, Hillis AE, Josephs KA, Boeve BF, Kertesz A, Seeley WW, Rankin KP, Johnson JK, Gorno-Tempini ML, Rosen H, Prioleau-Latham CE, Lee A, Kipps CM, Lillo P, Piguet O, Rohrer JD, Rossor MN, Warren JD, Fox NC, Galasko D, Salmon DP, Black SE, Mesulam M, Weintraub S, Dickerson BC, Diehl-Schmid J, Pasquier F, Deramecourt V, Lebert F, Pijnenburg Y, Chow TW, Manes F, Grafman J, Cappa SF, Freedman M, Grossman M, Miller BL (2011) Sensitivity of revised diagnostic criteria for the behavioural variant of frontotemporal dementia. Brain 134:2456–2477CrossRefGoogle Scholar
  17. 17.
    McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack CR Jr, Kawas CH, Klunk WE, Koroshetz WJ, Manly JJ, Mayeux R, Mohs RC, Morris JC, Rossor MN, Scheltens P, Carrillo MC, Thies B, Weintraub S, Phelps CH (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. Alzheimers Dement 7:263–269CrossRefGoogle Scholar
  18. 18.
    Gorno-Tempini ML, Hillis AE, Weintraub S, Kertesz A, Mendez M, Cappa SF, Ogar JM, Rohrer JD, Black S, Boeve BF, Manes F, Dronkers NF, Vandenberghe R, Rascovsky K, Patterson K, Miller BL, Knopman DS, Hodges JR, Mesulam MM, Grossman M (2011) Classification of primary progressive aphasia and its variants. Neurology 76:1006–1014CrossRefGoogle Scholar
  19. 19.
    Mathew R, Bak TH, Hodges JR (2012) Diagnostic criteria for corticobasal syndrome: a comparative study. J Neurol Neurosurg Psychiatry 83:405–410CrossRefGoogle Scholar
  20. 20.
    Litvan I, Agid Y, Calne D, Campbell G, Dubois B, Duvoisin RC, Goetz CG, Golbe LI, Grafman J, Growdon JH, Hallett M, Jankovic J, Quinn NP, Tolosa E, Zee DS (1996) Clinical research criteria for the diagnosis of progressive supranuclear palsy (Steele-Richardson-Olszewski syndrome): report of the NINDS-SPSP international workshop. Neurology 47:1–9CrossRefGoogle Scholar
  21. 21.
    Strong MJ, Grace GM, Freedman M, Lomen-Hoerth C, Woolley S, Goldstein LH, Murphy J, Shoesmith C, Rosenfeld J, Leigh PN, Bruijn L, Ince P, Figlewicz D (2009) Consensus criteria for the diagnosis of frontotemporal cognitive and behavioural syndromes in amyotrophic lateral sclerosis. Amyotroph Lateral Scler 10:131–146CrossRefGoogle Scholar
  22. 22.
    Hsieh S, Schubert S, Hoon C, Mioshi E, Hodges JR (2013) Validation of the Addenbrooke’s Cognitive Examination III in frontotemporal dementia and Alzheimer’s disease. Dement Geriatr Cogn Disord 36:242–250CrossRefGoogle Scholar
  23. 23.
    Wechsler D (1997) Wechsler adult intelligence scale—Third Edition (WAIS-III). The Psychological Corporation., San AntonioGoogle Scholar
  24. 24.
    Tombaugh TN (2004) Trail Making Test A and B: normative data stratified by age and education. Arch Clin Neuropsychol 19:203–214CrossRefGoogle Scholar
  25. 25.
    Meyers J, Meyers K (1995) The Meyers scoring system for the Rey complex figure and the recognition trial: professional manual. Psychological Assessment Resourses, OdessaGoogle Scholar
  26. 26.
    Spreen O, Strauss E, A (1998) A compendium of neuropsychological tests: administration, norms and commentary. Oxford University Press, New YorkGoogle Scholar
  27. 27.
    Savage S, Hsieh S, Leslie F, Foxe D, Piguet O, Hodges JR (2013) Distinguishing subtypes in primary progressive aphasia: application of the Sydney language battery. Dement Geriatr Cogn Disord 35:208–218CrossRefGoogle Scholar
  28. 28.
    Knopman DS, Kramer JH, Boeve BF, Caselli RJ, Graff-Radford NR, Mendez MF, Miller BL, Mercaldo N (2008) Development of methodology for conducting clinical trials in frontotemporal lobar degeneration. Brain 131:2957–2968CrossRefGoogle Scholar
  29. 29.
    Wear HJ, Wedderburn CJ, Mioshi E, Williams-Gray CH, Mason SL, Barker RA, Hodges JR (2008) The Cambridge behavioural inventory revised. Dement Neuropsychol 2:102–107CrossRefGoogle Scholar
  30. 30.
    Swets JA (1996) Signal detection theory and ROC analysis in psychology and diagnostics: Collected papers. Lawrence Erlbaum Associates, Inc, HillsdaleGoogle Scholar
  31. 31.
    Langner R, Kellermann T, Eickhoff SB, Boers F, Chatterjee A, Willmes K, Sturm W (2012) Staying responsive to the world: modality-specific and -nonspecific contributions to speeded auditory, tactile, and visual stimulus detection. Hum Brain Mapp 33:398–418CrossRefGoogle Scholar
  32. 32.
    Czeisler CA, Walsh JK, Roth T, Hughes RJ, Wright KP, Kingsbury L, Arora S, Schwartz JR, Niebler GE, Dinges DF, Group USMiSWSDS (2005) Modafinil for excessive sleepiness associated with shift-work sleep disorder. N Engl J Med 353:476–486CrossRefGoogle Scholar
  33. 33.
    Robertson IH (2003) The absent mind: attention and error. Psychologist 16:476–758Google Scholar
  34. 34.
    Sinclair KL, Ponsford JL, Rajaratnam SM, Anderson C (2013) Sustained attention following traumatic brain injury: use of the Psychomotor Vigilance Task. J Clin Exp Neuropsychol 35:210–224CrossRefGoogle Scholar
  35. 35.
    Castellanos FX, Sonuga-Barke EJ, Scheres A, Di Martino A, Hyde C, Walters JR (2005) Varieties of attention-deficit/hyperactivity disorder-related intra-individual variability. Biol Psychiatry 57:1416–1423CrossRefGoogle Scholar
  36. 36.
    Jongman SR, Meyer AS, Roelofs A (2015) The role of sustained attention in the production of conjoined noun phrases: an individual differences study. PLoS One 10:e0137557CrossRefGoogle Scholar
  37. 37.
    Weissman DH, Roberts KC, Visscher KM, Woldorff MG (2006) The neural bases of momentary lapses in attention. Nat Neurosci 9:971–978CrossRefGoogle Scholar
  38. 38.
    Raichle ME, MacLeod AM, Snyder AZ, Powers WJ, Gusnard DA, Shulman GL (2001) A default mode of brain function. Proc Natl Acad Sci USA 98:676–682CrossRefGoogle Scholar
  39. 39.
    Stuss DT, Murphy KJ, Binns MA, Alexander MP (2003) Staying on the job: the frontal lobes control individual performance variability. Brain 126:2363–2380CrossRefGoogle Scholar
  40. 40.
    Wolfers T, Onnink AM, Zwiers MP, Arias-Vasquez A, Hoogman M, Mostert JC, Kan CC, Slaats-Willemse D, Buitelaar JK, Franke B (2015) Lower white matter microstructure in the superior longitudinal fasciculus is associated with increased response time variability in adults with attention-deficit/ hyperactivity disorder. J Psychiatry Neurosci 40:344–351CrossRefGoogle Scholar
  41. 41.
    Ahmed RM, Devenney EM, Irish M, Ittner A, Naismith S, Ittner LM, Rohrer JD, Halliday GM, Eisen A, Hodges JR, Kiernan MC (2016) Neuronal network disintegration: common pathways linking neurodegenerative diseases. J Neurol Neurosurg Psychiatry 87:1234–1241CrossRefGoogle Scholar
  42. 42.
    Michely J, Barbe MT, Hoffstaedter F, Timmermann L, Eickhoff SB, Fink GR, Grefkes C (2012) Differential effects of dopaminergic medication on basic motor performance and executive functions in Parkinson’s disease. Neuropsychologia 50:2506–2514CrossRefGoogle Scholar
  43. 43.
    Putzhammer A, Perfahl M, Pfeiff L, Ibach B, Johann M, Zitzelsberger U, Hajak G (2005) Performance of diadochokinetic movements in schizophrenic patients. Schizophr Res 79:271–280CrossRefGoogle Scholar
  44. 44.
    Sharma K, Davis T, Coulthard E (2016) Enhancing attention in neurodegenerative diseases: current therapies and future directions. Transl Neurosci 7:98–109CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of PsychologyThe University of SydneySydneyAustralia
  2. 2.Brain and Mind CentreThe University of SydneySydneyAustralia
  3. 3.ARC Centre of Excellence in Cognition and its DisordersSydneyAustralia
  4. 4.The Department of Aged CareSt George HospitalKogarahAustralia
  5. 5.Calvary Health Care SydneyKogarahAustralia
  6. 6.Faculty of MedicineUniversity of New South WalesSydneyAustralia
  7. 7.Clinical Medical SchoolThe University of SydneySydneyAustralia
  8. 8.Concord General HospitalSydneyAustralia

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