Neurobiology of Aging
Volume 30, Issue 6 , Pages 875-889 , June 2009

Specificity of inhibitory deficits in normal aging and Alzheimer's disease

  • Fabienne Collette

      Affiliations

    • Cognitive Sciences Department, University of Liège, Liège, Belgium
    • Cyclotron Research Center, University of Liège, Liège, Belgium
    • Fonds National de la Recherche Scientifique, Belgium
    • Corresponding Author InformationCorresponding author at: Neuropsychology Unit, University of Liège, Boulevard du Rectorat 3 (B33), 4000 Liège, Belgium. Tel.: +32 4 366 22 74; fax: +32 4 366 28 75.
  • ,
  • Christina Schmidt

      Affiliations

    • Cognitive Sciences Department, University of Liège, Liège, Belgium
    • Cyclotron Research Center, University of Liège, Liège, Belgium
    • Fonds National de la Recherche Scientifique, Belgium
  • ,
  • Christine Scherrer

      Affiliations

    • Cognitive Sciences Department, University of Liège, Liège, Belgium
  • ,
  • Stéphane Adam

      Affiliations

    • Cognitive Sciences Department, University of Liège, Liège, Belgium
  • ,
  • Eric Salmon

      Affiliations

    • Cyclotron Research Center, University of Liège, Liège, Belgium
    • Neurology Department, CHU, Liège, Belgium

Received 24 January 2007 ,Revised 24 August 2007 ,Accepted 18 September 2007.

References 

  1. Adam S, Van der Linden M, Collette F, Lemauvais L, Salmon E. Further exploration of controlled and automatic processes in early Alzheimer's disease. Neuropsychologia. 2005;19:420–427
  2. Amieva H, Lafont S, Rainville C, Dartigues J-F, Fabrigoule C. Analyse of inhibitory dysfunction in patients with Alzheimer's disease and normal elderly adults in two verbal tasks. Brain Cogn. 1998;37:58–60
  3. Amieva H, Lafont S, Auriacombe S, LeCarret N, Dartigues J-F, Orgogozo J, et al. Inhibitory breakdown and dementia of the Alzheimer type: a general phenomenon?. J. Clin. Exp. Neuropsychol. 2002;24:503–516
  4. Amieva H, Phillips LH, Della Sala S, Henry JD. Inhibitory functioning in Alzheimer's disease: a review. Brain. 2004;127:949–964
  5. Amieva H, Lafont S, Rouch-Leroyer I, Rainville C, Dartigues J-F, Orgogozo J, et al. Evidencing inhibitory deficits in Alzheimer's disease through interference effects and shifting disabilities in the Stroop test. Arch. Clin. Neuropsychol. 2004;19:791–803
  6. Andrès P, Van der Linden M. Age-related differences in supervisory attentional system functions. J. Gerontol.: Psychol. Sci. 2000;55B:P373–P380
  7. Andrès P. Ageing and inhibition: distinguishing between automatic and controlled inhibition. In: Paper presented at the Annual Conference of the British Psychological Society. Blackpool. 2002;
  8. Andrès P. Further evidence for the fractionation of inhibition in ageing. In: Paper presented at the Annual Conference of the British Psychological Society. Bournemouth. 2003;
  9. Andrès P, Van der Linden M, Parmentier FB. Directed forgetting in working memory: age-related differences. Memory. 2004;12:248–256
  10. Arbuthnott K. Inhibitory mechanisms in cognition: Phenomena and models. Curr. Psychol. Cogn. 1995;14:3–45
  11. Balota DA, Faust M. Attention in dementia of the Alzheimer's type. In: second ed..  Boller F,  Grafman J editor. Handbook of Neuropsychology. 6:Amsterdam: Elsevier Science; 2001;p. 51–80
  12. Bandera L, Della Sala S, Laiacona M, Luzzatti C, Spinnler H. Generative associative naming in dementia of Alzheimer's type. Neuropsychologia. 1991;29:291–304
  13. Belleville S, Rouleau N, Van der Linden M. Use of the Hayling task to measure inhibition of prepotent responses in normal aging and Alzheimer's disease. Brain Cogn. 2006;62:113–119
  14. Bielak AA, Mansuetti L, Strauss E, Dixon RA. Performance on the Hayling and Brixton tests in older adults: norms and correlates. Arch. Clin. Neuropsychol. 2006;21:141–149
  15. Bjorklund DF, Harnishfeger KK. The evolution of inhibitionmechanisms and their role in human cognition and behavior. In:  Dempster FN,  Brainerd CJ editor. Interference and Inhibition in Cognition. San Diego: Academic Press; 1995;p. 142–173
  16. Bondi MW, Serody AB, Chan AS, Eberson-Shumate SC, Delis DC, Hansen LA, et al. Cognitive and neuropathologic correlates of Stroop color-word test performance in Alzheimer's disease. Neuropsychologia. 2002;16:335–343
  17. Burgess PW, Shallice T. Response suppression, initiation and strategy use following frontal lobe lesions. Neuropsychologia. 1996;34:263–273
  18. Butler KM, Zacks RT, Henderson JM. Suppression of reflexive saccades in younger and older adults: age comparisons on an antisaccade task. Memory Cogn. 1999;27:584–591
  19. Cahn DA, Salmon DP, Bondi MW, Butters N, Johnson SA, Wiederholt WC, et al. A population-based analysis of qualitative features of the neuropsychological test performance of individuals with dementia of the Alzheimer type: implications for individuals with questionable dementia. J. Int. Neuropsychol. Soc. 1997;3:387–393
  20. Charlot V, Feyereisen P. Aging and the deletion function of inhibition. Aging Neuropsychol. Cogn. 2004;11:12–24
  21. Charlot V, Feyereisen P. Mémoire épisodique et déficit d’inhibition au cours du vieillissement cognitif: un examen de l’hypothèse frontale. L’Année Psychologique. 2005;105:323–357
  22. Clark JM. Contributions of inhibitory mechanisms to unified theory in neuroscience and psychology. Brain Cogn. 1996;30:127–152
  23. Collette F, Van der Linden M, Salmon E. Executive dysfunction in Alzheimer's disease. Cortex. 1999;35:57–72
  24. Collette F, Van der Linden M. Attention disorders in degenerative syndromes. In:  Leclercq M,  Zimmerman P editor. Applied Neuropsychology of Attention: Theory, Diagnosis and Rehabilitation. London: Psychology Press; 2002;p. 305–338
  25. Collette F, Van der Linden M, Delrue G, Salmon E. Frontal hypometabolism does not explain inhibitory dysfunction in Alzheimer's disease. Alzheimer's Dis. Assoc. Disord. 2002;16:228–238
  26. Connelly SL, Hasher L, Zacks R. Age and reading: the impact of distraction. Psychol. Aging. 1991;6:533–541
  27. Connelly L, Hasher L. Aging and the inhibition of spatial location. J. Exp. Psychol.: Hum. Percept. Perf. 1993;19:1238–1250
  28. Content A, Mousty P, Radeau M. Brulex: une base de données lexicales informatisée pour le français écrit et parlé. L’Année Psychologique. 1990;90:551–566
  29. D’Esposito M, Postle BR, Jonides J, Smith EE. The neural substrate and temporal dynamics of interference effects in working memory as revealed by event-related functional MRI. Proc. Nat. Acad. Sci. 1999;96:7514–7519
  30. Dagenbach D, Carr TH. Inhibitory Processes in Attention, Memory and Language. San Diego: Academic Press; 1994;
  31. Danckert J, Maruff P, Crowe S, Currie J. Inhibitory processes in covert orienting in patients with Alzheimer's disease. Neuropsychologia. 1998;12:225–241
  32. Deltour, J.J., 1993. Echelle de vocabulaire Mill Hill de J.C. Raven. Braine-le-Chateau, Belgium: Editions l’Application des Techniques Modernes.
  33. Dempster FN, Brainerd CJ. Interference and Inhibition in Cognition. San Diego: Academic Press; 1995;
  34. Dempster FN, Corkill AJ. Individual differences in susceptibility to interference and general cognitive ability. Acta Psychol. 1999;101:395–416
  35. Dempster FN, Corkill AJ. Interference and inhibition in cognition and behavior: unifying themes for educational psychology. Educ. Psychol. Rev. 1999;11:1–88
  36. Duchek J, Balota DA, Thessing VC. Inhibition of visual and conceptual information during reading in healthily aging and Alzheimer's disease. Aging Neuropsychol. Cogn. 1998;5:169–181
  37. Dulaney CL, Rogers WA. Mechanisms underlying reduction in Stroop interference with practice for young and old adults. J. Exp. Psychol.: Learn. Memory Cogn. 1994;20:470–484
  38. Fabrigoule C, Rouch I, Letenneur L, Commenges D, Mazaux JM, Orgogozo JM, et al. Cognitive process in preclinical phase of dementia. Brain. 1998;121:135–141
  39. Faust ME, Balota DA. Inhibition of return and visuospatial attention in healthy older adults and individuals with dementia of the Alzheimer type. Neuropsychologia. 1997;11:13–29
  40. Fisher LM, Freed DM, Corkin S. Stroop color-word test performance in patients with Alzheimer's disease. J. Clin. Exp. Neuropsychol. 1990;12:745–758
  41. Fox LS, Olin JT, Erblich J, Ippen CG, Schneider LS. Severity of cognitive impairment in Alzheimer's disease affects list learning using the California Verbal Learning Test (CVLT). Int. J. Geriatric Psych. 1998;13:544–549
  42. Fuld P, Katzman R, Davies P, Terry RD. Intrusions as a sign of Alzheimer dementia: chemical and pathological verification. Ann. Neurol. 1982;11:155–159
  43. Garrard P, Patterson K, Hodges JR. Semantic processing in Alzheimer's disease. In:  Morris R,  Becker J editor. Cognitive Neuropsychology of Alzheimer's disease. Oxford: Oxford University Press; 2004;p. 179–196
  44. Hamm VP, Hasher L. Age and the availability of inferences. Psychol. Aging. 1992;7:56–64
  45. Harnishfeger KK, Bjorklund DF. The ontogeny of inhibitory mechanisms: A renewed approach to cognitive development. In:  Howe ML,  Pasnak R editor. Emerging Themes in Cognitive Development. vol. 1:New-York: Springer-Verlag; 1993;p. 28–49(Foundations)
  46. Harnishfeger KK. The development of cognitive inhibition. Theories, definitions, and research evidence. In:  Dempster FN,  Brainerd CJ editor. Interference and Inhibition in Cognition. London: Academic Press; 1995;p. 175–206
  47. Hartley AA. Evidence for the selective preservation of spatial selective attention in old age. Psychol. Aging. 1993;8:371–379
  48. Hartley AA, Kieley JM. Adult age differences in the inhibition of return of visual attention. Psychol. Aging. 1995;10:670–684
  49. Hartman M, Hasher L. Aging and suppression: memory for previously relevant information. Psychol. Aging. 1991;6:587–594
  50. Hasher L, Zacks R. Automatic and effortful processes in memory. J. Exp. Psychol.: Gen. 1979;108:356–388
  51. Hasher L, Stoltzfus ER, Zacks RT, Rypma B. Age and inhibition. J. Exp. Psychol.: Learn. Memory Cogn. 1991;17:163–169
  52. Hasher L, Zacks RT, May CP. Inhibitory control, circardian arousal, and age. In:  Gopher D,  Koriat A editor. Attention and Performance XVII, Cognitive Regulation of Performance: Interaction of Theory and Application. Cambridge, MA: MIT Press; 1999;p. 653–675
  53. Hasher L, Tonev ST, Lustig C, Zacks R. Inhibitory control, environmental support, and self-initiated processing in aging. In:  Naveh-Benjamin M,  Moscovitch M,  Roediger HLI editor. Perspectives on Human Memory and Cognitive Aging. Essays in Honour of Fergus Craik. New York: Psychology Press; 2001;p. 286–297
  54. Hedden T, Park DC. Contributions of source and inhibitory mechanisms to age-related retroactive interference in verbal working memory. J. Exp. Psychol.: Gen. 2003;132:93–112
  55. Hogge, M., Adam, S., Collette, F., 2004. Retrieval-induced forgetting in normal aging. In: Casini, A., Klein, O. (Eds.) Proceedings of the 2004 Annual. Meeting of the Belgian Psychological Society Brussels University Press: Bruxelles (Belgium), p. 63.
  56. Houghton G, Tipper SP. A model of inhibitory mechanisms in selective attention. In:  Dagenbach D,  Carr TH editor. Inhibitory Processes in Attention, Memory, and Language. San Diego: Academic Press; 1994;p. 53–112
  57. Houx PJ, Jolles J, Vreeling FW. Aging effects assessed with the Stroop color word test in childhood, adulthood, and aging. Exp. Aging Res. 1993;19:209–224
  58. Howard D, Patterson K. Pyramids and palm trees: a test of semantic access from pictures and words.. Bury St Edmonds: Thames Valley Company; 1992;
  59. Intons-Peterson MJ, Rocchi P, West T, McLellan K, Hackney A. Aging; optimal testing times, and negative priming. J. Exp. Psychol.: Learn. Memory Cogn. 1998;24:362–376
  60. Jennings JM, Merikle PM. Automatic versus intentional uses of memory: aging, attention, and control. Psychol. Aging. 1993;8:283–293
  61. Jonides J, Smith EE, Marshuetz C, Koeppe RA, Reuter-Lorenz PA. Inhibition in verbal working memory revealed by brain activation. Proc. Nat. Acad. Sci. U.S.A. 1998;95:8410–8413
  62. Kane MJ, Hasher L, Stoltzfus ER, Zacks RT, Connelly SL. Inhibitory attentional mechanisms and aging. Psychol. Aging. 1994;9:103–112
  63. Kieley JM, Hartley AA. Age-related equivalence of identity suppression in the Stroop color-word task. Psychol. Aging. 1997;12:22–29
  64. Klein M, Ponds R, Houx PJ, Jolles J. Effects of test duration on age-related differences in Stroop interference. J. Clin. Exp. Neuropsychol. 1997;19:77–82
  65. Koss E, Ober BA, Delis DC, Friedland RP. The Stroop Color-Word Test: indicator of dementia severity. Int. J. Neurosci. 1984;24:53–61
  66. Kramer AF, Humphrey DG, Larish JF, Logan G, Strayer D. Aging and inhibition: beyond an unitary view of inhibitory processing in attention. Psychol. Aging. 1994;9:491–512
  67. Langley LK, Overmier JB, Knopman DS, Prod’Homme MS. Inhibition and habituation: preserved mechanisms of attentional selection in aging and Alzheimer's disease. Neuropsychologia. 1998;12:353–366
  68. Langley LK, Fuentes LJ, Hochhalter AK, Brandt J, Overmier JB. Inhibition of return in aging and Alzheimer's disease: performance as a function of task demands and stimulus timing. J. Clin. Exp. Neuropsychol. 2001;23:431–446
  69. LeMoal S, Reymann JM, Thomas V, Cattenoz C, Lieury A, Allain H. Effect of normal aging and of Alzheimer's disease on episodic memory. Demen. Geriatr. Cogn. Dis. 1997;8:281–287
  70. Light L. Memory and aging: four hypotheses in search of data. Ann. Rev. Psychol. 1991;42:333–376
  71. Lustig CL, Hasher L, Tonev ST. Distraction as a determinant of processing speed. Psychon. Bull. Rev. 2006;13:619–625
  72. Mattis S. Dementia Rating Scale. Windsor: NFER-Nelson; 1973;
  73. May CP, Hasher L. Synchrony effects in inhibitory control over though and action. J. Exp. Psychol.: Hum. Percep. Perf. 1998;24:363–379
  74. McDowd JM, Oseas-Kreger DM. Aging, inhibitory processes, and negative priming. J. Gerontol. 1991;46:P340–P345
  75. McKhann G, Drachman D, Folstein M, Katzman R, Price D, Stadlan EM. 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. 1984;34:939–944
  76. Monsch AU, Bondi MW, Salmon DP, Butters N, Thal LJ, Hansen LA, et al. Clinical validity of the Mattis dementia rating scale in detecting dementia of the Alzheimer type. Arch. Neurol. 1995;52:504–899
  77. Moulin CJA, Perfect TJ, Conway MA, North AS, Jones RW, James N. Retrieval-induced forgetting in Alzheimer's disease. Neuropsychologia. 2002;40:862–867
  78. Multhaup KS, Balota DA. Generation effects and source memory in healthy older adults and in adults with dementia of the Alzheimer type. Neuropsychologia. 1997;11:382–391
  79. Nielson KA, Langenecker SA, Garavan H. Differences in the functional neuroanatomy of inhibitory control across the adult life span. Psychol. Aging. 2002;17:56–71
  80. Nigg JT. On inhibition/disinhibition in developmental psychopathology: views from cognitive and personality psychology and a working inhibition taxonomy. Psychol. Bull. 2000;126:220–246
  81. Park D, Hedden T. Working memory and aging. In:  Naveh-Benjamin M,  Moscovitch M,  Roediger HLI editor. Perspectives on Human Memory and Cognitive Aging. Essays in Honour of Fergus Craick. Hove: Psychology Press; 2001;p. 148–160
  82. Paul S. Search for semantic inhibition failure during sentence comprehension. Psychol. Aging. 1996;11:10–20
  83. Reed H. Studies of interference process in short-term memory. J. Exp. Psychol. 1970;84:452–457
  84. Salmon DP. Disorders of memory in Alzheimer's disease. In:  Boller F,  Grafman J editor. Handbook of Neuropsychology. second ed.. Amsterdam: Elsevier Science BV; 2000;p. 155–195
  85. Salthouse TA, Babcock RL. Decomposing adult age differences in working memory. Dev. Psychol. 1991;27:763–776
  86. Salthouse TA, Becker JT. Independent effects of Alzheimer's disease on neuropsychological functioning. Neuropsychologia. 1998;12:242–252
  87. Salthouse TA, Meinz EJ. Aging, inhibition, working memory and speed. J. Gerontol.: Psychol. Sci. 1995;50:297–306
  88. Salthouse TA, Thoth JP, Hancock HE, Woodard JL. Controlled and automatic forms of attention: process purity and the uniqueness of age-related influences. J. Gerontol.: Psychol. Sci. 1997;52B:P216–P228
  89. Schneider W, Eschman A, Zuccolotto A. E-Prime User's Guide. Pittsburgh, PA: Psychology Software Tools Inc; 2002;
  90. Sebastian MV, Menor J, Elusoa R. Patterns of errors in short-term forgetting in AD and ageing. Memory. 2001;9:223–321
  91. Shaw RJ. Age-related increases in the effects of automatic semantic activation. Psychol. Aging. 1991;6:595–604
  92. Shilling VM, Chetwynd A, Rabbitt PMA. Individual inconsistency across measures of inhibition: an investigation of the construct validity of inhibition in older adults. Neuropsychologia. 2002;40:605–619
  93. Spieler DH, Balota DA, Faust ME. Stroop performance in healthy younger and older adults and in individuals with dementia of the Alzheimer's type. J. Exp. Psychol. 1996;22:461–479
  94. Stoltzfus ER, Hasher L, Zacks RT, Ulivi MS, Goldstein D. Investigation of inhibition and interference in younger and older adults. J. Gerontol. 1993;48:P179–P188
  95. Sullivan MP, Faust ME, Balota DA. Identity negative priming in older adults and individuals with dementia of the Alzheimer type. Neuropsychologia. 1995;9:537–555
  96. Teresa Lechuga Ma, Moreno V, Pelegrina S, Gomez-Ariza CJ, Bajo Teresa Ma. Age differences in memory control: Evidence from updating and retrieval practice tasks. Acta Psychol. 2006;123:279–298
  97. Tipper SP. Less attentional selectivity as a result of declining inhibition in older adults. Bull. Psychon. Soc. 1991;29:45–47
  98. Titov N, Knight RG. Adult age differences in controlled and automatic memory processing. Psychol. Aging. 1997;12:565–573
  99. Van der Linden M, Hupet M, Feyereisen P, Schelstraete M, Bestgen Y, Bruyer R, et al. Cognitive mediators of age-related differences in language comprehension and verbal memory performance. Aging Neuropsychol. Cogn. 1999;6:32–55
  100. Verhaeghen P, De Meersman L. Aging and the Stroop effect: a meta-analysis. Psychol. Aging. 1998;13:120–126
  101. Verhaeghen P, De Meersman L. Aging and the negative priming effect: a meta-analysis. Psychol. Aging. 1998;13:435–444
  102. Weingartner H, Kaye W, Smallberg SA, Ebert MH, Gillin JC, Sitaram N. Memory failures in progressive idiopathic dementia. J. Abnormal. Psychol. 1981;90:187–196
  103. Wilson SP, Harnishfeger KK. The development of efficient inhibition: evidence from directed forgetting tasks. Dev. Rev. 1998;18:86–123
  104. Yoon C, May CP, Hasher L. Aging, circadian arousal patterns, and cognition. In:  Park D,  Schwartz N editor. Cognitive Aging: A Primer. Hove: Psychology Press; 2000;p. 151–170
  105. Zacks RT, Hasher L, Radvansky G. Studies of directed forgetting in older adults. J. Exp. Psychol.: Learn. Memory Cogn. 1996;22:143–156

PII: S0197-4580(07)00380-6

doi: 10.1016/j.neurobiolaging.2007.09.007

Neurobiology of Aging
Volume 30, Issue 6 , Pages 875-889 , June 2009