Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-23T04:12:56.226Z Has data issue: false hasContentIssue false
  • English
  • Français

Errorless practice as a possible adjuvant to donepezil in Alzheimer’s disease

Published online by Cambridge University Press:  01 March 2009

LESLIE J. GONZALEZ ROTHI ,
RENEE FULLER ,
SUSAN A. LEON ,
DIANE KENDALL ,
ANNA MOORE ,
SAMUEL S. WU ,
BRUCE CROSSON ,
KENNETH M. HEILMAN  and
STEPHEN E. NADEAU
LESLIE J. GONZALEZ ROTHI*
Affiliation:
Brain Rehabilitation Research Center, Malcom Randall VA Medical Center, Gainesville, Florida Geriatric Research, Education and Clinical Center, Malcom Randall VA Medical Center, Gainesville, Florida Department of Neurology, University of Florida, Gainesville, Florida
RENEE FULLER
Affiliation:
Brain Rehabilitation Research Center, Malcom Randall VA Medical Center, Gainesville, Florida Cardinal Hill Rehabilitation Hospital, Lexington, Kentucky
SUSAN A. LEON
Affiliation:
Brain Rehabilitation Research Center, Malcom Randall VA Medical Center, Gainesville, Florida Department of Communication Sciences and Disorders, University of Florida, Gainesville, Florida Neurology Service, Malcom Randall VA Medical Center, Gainesville, Florida
DIANE KENDALL
Affiliation:
Brain Rehabilitation Research Center, Malcom Randall VA Medical Center, Gainesville, Florida Department of Speech and Hearing Sciences, University of Washington, Seattle, Washington
ANNA MOORE
Affiliation:
Rehabilitation Research Center of Excellence, VA Medical Center, Atlanta, Georgia Department of Rehabilitation Medicine, Emory University School of Medicine, Atlanta, Georgia
SAMUEL S. WU
Affiliation:
Brain Rehabilitation Research Center, Malcom Randall VA Medical Center, Gainesville, Florida Department of Epidemiology and Health Policy Research, University of Florida, Gainesville, Florida Rehabilitation Outcomes Research Center, Malcom Randall VA Medical Center, Gainesville, Florida
BRUCE CROSSON
Affiliation:
Brain Rehabilitation Research Center, Malcom Randall VA Medical Center, Gainesville, Florida Department of Clinical and Health Psychology, University of Florida, Gainesville, Florida
KENNETH M. HEILMAN
Affiliation:
Brain Rehabilitation Research Center, Malcom Randall VA Medical Center, Gainesville, Florida Geriatric Research, Education and Clinical Center, Malcom Randall VA Medical Center, Gainesville, Florida Department of Neurology, University of Florida, Gainesville, Florida Neurology Service, Malcom Randall VA Medical Center, Gainesville, Florida
STEPHEN E. NADEAU
Affiliation:
Brain Rehabilitation Research Center, Malcom Randall VA Medical Center, Gainesville, Florida Geriatric Research, Education and Clinical Center, Malcom Randall VA Medical Center, Gainesville, Florida Department of Neurology, University of Florida, Gainesville, Florida
*
*Correspondence and reprint requests to: Leslie J. Gonzalez Rothi, Ph.D., Brain Rehabilitation Research Center, Room 151a, Malcom Randall VA Medical Center, 1601 SW Archer Road, Gainesville, Florida 32608-1197. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Six individuals with probable Alzheimer’s disease (AD) participated in a phase 1 study employing a repeated measures, parallel baseline design testing the hypothesis that error-free experience during word production practice combined with an acetyl cholinesterase inhibitor would improve confrontation naming ability. While acetyl cholinesterase inhibitors are safe and delay cognition decline associated with AD, improvement over baseline cognition is less evident; clinically significant cognitive deficits persist and progress. Both animal and clinical research strongly implicate acetylcholine in learning, a form of neuroplasticity. In clinical practice, however, people with AD are given cholinergic medications without concomitant systematic/targeted retraining. In this study six participants with probable AD and taking donepezil participated in targeted word production practice using an errorless learning strategy. Results showed that combining behavioral enrichment training and an acetyl cholinesterase inhibitor resulted in significant improvements in verbal confrontation naming of trained items for three of six participants. Differences in baseline dementia severity, living conditions, and medications may have influenced the training response. Detection of substantial treatment effects in 50% of subjects suggests further language treatment studies in AD in combination with an acetyl cholinesterase inhibitor are warranted and provide useful information on inclusion/exclusion criteria for use in subsequent studies. (JINS, 2009, 15, 311–322.)

Keywords

DementiaRehabilitationAnomiaCholinesterase inhibitorsLanguage therapyVerbal learning
Type
Neurobehavioral Grand Rounds
Information
Journal of the International Neuropsychological Society , Volume 15 , Issue 2 , March 2009 , pp. 311 - 322
Copyright
Copyright © INS 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Baskerville, K.A., Schweitzer, J.B., & Herron, P. (1997). Effects of cholinergic depletion on experience-dependent plasticity in the cortex of the rat. Neuroscience, 80, 1159–1169.CrossRefGoogle ScholarPubMed
Beeson, P.M. & Robey, R.R. (2006). Evaluating single-subject treatment research: Lessons learned from the aphasia literature. Neuropsychological Review, 16, 161–169.CrossRefGoogle ScholarPubMed
Benke, T., Köylü, B., Delazer, M., Trinka, E., & Kemmler, G. (2005). Cholinergic treatment of amnesia following basal forebrain lesion due to aneurysm rupture – an open-label study. European Journal of Neurology, 12, 791–796.CrossRefGoogle Scholar
Bottino, C.M.C., Carvalho, I.A.M., Alvarez, A.M., Avila, R., Zukauskas, P.R., Bustamante, S.E.Z., Andrade, F.C., Hototian, S.R., Saffi, F., & Camargo, C.H.P. (2005). Cognitive rehabilitation combined with drug treatment in Alzheimer’s disease patients: A pilot study. Clinical Rehabilitation, 19, 861–869.CrossRefGoogle ScholarPubMed
Burns, A., Gauthier, S., & Perdomo, C.A. (2007). Efficacy and safety of donepezil over 3 years: An open-label, multicentre study of inpatients with Alzheimer’s disease. International Journal of Geriatric Psychiatry, 22, 806–812.CrossRefGoogle Scholar
Burns, A., Rossor, M., Hecker, J., Gauthier, S., Petit, H., Moller, H.J., Rogers, S.L., Friedhoff, L.T., & the International Donepezil Study Group. (1999). The effects of donepezil in Alzheimer’s disease: Results from a multinational trial. Dementia and Geriatric Cognitive Disorders, 10, 237–244.CrossRefGoogle ScholarPubMed
Busk, P.L. & Serlin, R. (1992). Meta-analysis for single-case research. In Kratochwill, T.R. & Levin, J.R. (Eds.), Single-case research design and analysis: New directions for psychology and education (pp. 187–212). Hillsdale, NJ: Erlbaum.Google Scholar
Butt, A.E. & Hodge, G.K. (1995). Acquisition, retention, and extinction of operant discriminations in rats with nucleus basalis magnocellularis lesions. Behavioral Neuroscience, 109, 699–713.CrossRefGoogle ScholarPubMed
Clare, L., Wilson, B.A., Carter, G., Breen, K., Gosses, A., & Hodges, J.R. (2000). Intervening with everyday memory problems in dementia of Alzheimer type: An errorless learning approach. Journal of Clinical and Experimental Neuropsychology, 22, 132–146.CrossRefGoogle ScholarPubMed
Clare, L., Wilson, B.A., Carter, G., Roth, I., & Hodges, J.R. (2002). Re-learning face-name associations in early Alzheimer’s disease. Neuropsychology, 16, 538–547.CrossRefGoogle Scholar
Cohen, J. (1988). Statistical power analysis for the behavioral sciences. Hillsdale, NJ: Erlbaum.Google Scholar
Conner, J.M., Culberson, A., Packowski, C., Chiba, A.A., & Tuszynski, M.H. (2003). Lesions of the basal forebrain cholinergic system impair task acquisition and abolish cortical plasticity associated with motor skill learning. Neuron, 38, 819–829.CrossRefGoogle ScholarPubMed
Crowell, T.A., Paramadevan, J., Abdullah, L., & Mullan, M. (2006). Beneficial effect of cholinesterase inhibitor medications on recognition memory performance in mild to moderate Alzheimer’s disease: Preliminary findings. Journal of Geriatric Psychiatry and Neurology, 19, 13–15.CrossRefGoogle ScholarPubMed
Delis, D.C., Kramer, J.H., Kaplan, E., & Ober, B.A. (1987). California Verbal Learning Test: Adult version manual. San Antonio, TX: The Psychological Corporation.Google Scholar
Doody, R.S.,Geldmacher, D.S., Gordon, B., Perdomo, C.A., Pratt, R.D., & the Donepezil Study Group. (2001). Open-label, multicenter, phase 3 extension study of the safety and efficacy of donepezil in patients with Alzheimer disease. Archives of Neurology, 58, 427–433.CrossRefGoogle ScholarPubMed
Doody, R.S., Stevens, J.C., Beck, C., Dubinski, R.M., Kaye, J.A., Gwyther, L., Mohs, R.C., Thal, L.J., Whitehouse, P.J., DeKosky, S.T., & Cummings, J.L. (2001). Practice parameter: Management of dementia (an evidence-based review). Report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology, 56, 1154–1166.CrossRefGoogle Scholar
Dooley, D.J., Taylor, C.P., Donevan, S., & Feltner, D. (2007). Ca2+ channel alpha2delta ligands: Novel modulators of neurotransmission. Trends in Pharmacological Science, 28, 75–82.CrossRefGoogle ScholarPubMed
Drachman, D.A. & Leavitt, J. (1974). Human memory and the cholinergic system. Archives of Neurology, 30, 113–121.CrossRefGoogle ScholarPubMed
Ernst, R.L. & Hay, J.W. (1997). Economic research on Alzheimer’s disease. A review of the literature. Alzheimer’s Disease and Associated Disorders, 11 (Suppl. 6), 135–145.Google ScholarPubMed
Evans, J.J., Wilson, B.A., Schuri, U., Andrade, J., Baddeley, A.D., Bruna, O., Canavan, T., Sala, S.D., Green, R., Laaksonen, R., Lorenzi, L., & Taussik, I. (2000). A comparison of “errorless” and “trial-and-error” learning methods for teaching individuals with acquired memory deficits. Neuropsychological Rehabilitation, 10, 67–101.CrossRefGoogle Scholar
Folstein, M.F., Folstein, S.E., & McHugh, P.R. (1975). ‘Mini-mental State’. A practical method for grading the cognitive state of patients for the clinician. Journal of Psychiatric Research, 12, 189–198.CrossRefGoogle Scholar
Francis, W.N. & Kucera, H. (1982). Frequency analysis of English usage: Lexicon and grammar. Boston: Houghton Mifflin.Google Scholar
Goldstein, L.B. (1998). Potential impact of drugs on poststroke motor recovery. In Goldstein, L.B. (Ed.), Restorative neurology: Advances in pharmacotherapy for recovery after stroke (pp. 241–256). Armonk, NY: Future Publishing.Google Scholar
Grön, G., Kirstein, M., Thielscher, A., Riepe, M.W., & Spitzer, M. (2005). Cholinergic enhancement of episodic memory in healthy young adults. Psychopharmacology, 182, 170–179.CrossRefGoogle ScholarPubMed
Gu, Q. (2003). Contribution of acetylcholine to visual cortical plasticity. Neurobiology of Learning and Memory, 80, 291–301.CrossRefGoogle Scholar
Haslam, C., Gilroy, D., Black, S., & Beesley, T. (2006). How successful is errorless learning in supporting memory for high and low-level knowledge in dementia? Neuropsycholgical Rehabilitation, 16, 505–536.CrossRefGoogle ScholarPubMed
Jones, R.S. & Eayrs, C.B. (1992). The use of errorless learning procedures in teaching people with a learning disability: A critical review. Mental Handicap Research, 5, 204–212.CrossRefGoogle Scholar
Juliano, S., Ma, W., & Eslin, D. (1991). Cholinergic depletion prevents expansion of topographic maps in somatosensory cortex. Proceedings of the National Academy of Sciences, 88, 7780–7784.CrossRefGoogle ScholarPubMed
Kaplan, E., Goodglass, H., & Weintraub, S. (1983). Boston Naming Test. Philadelphia: Lea & Febiger.Google Scholar
Kearns, K.P. (2000). Single-subject experimental designs in aphasia. In Nadeau, S.E., Rothi, L.J.G. & Crosson, B. (Eds.), Aphasia and language: Theory to practice (pp. 421–441). New York: Guilford Press.Google Scholar
Kertesz, A. (1982). Western Aphasia Battery. San Antonio, TX: Psychological Corporation.Google Scholar
Kilgard, M. (2003). Cholinergic modulation of skill learning and plasticity. Neuron, 38, 678–680.CrossRefGoogle ScholarPubMed
Kilgard, M.P. & Merzenich, M.M. (1998). Cortical map reorganization enabled by nucleus basalis activity. Science, 1714–1718.CrossRefGoogle ScholarPubMed
Kilgard, M.P. & Merzenich, M.M. (2002). Order-sensitive plasticity in adult primary auditory cortex. Proceedings of the National Academy of Sciences, 99, 3205–3209.CrossRefGoogle ScholarPubMed
Krnjevic, K., Pumain, R., & Renaud, L. (1971). The mechanism of excitation by acetylcholine in the cerebral cortex. Journal of Physiology, 215, 247–268.CrossRefGoogle ScholarPubMed
Krupp, L.B., Christodoulou, C., Melville, P., Scherl, W.F., MacAllister, W.S., & Elkins, L.E. (2004). Donepezil improved memory in multiple sclerosis in a randomized clinical trial. Neurology, 63, 1579–1585.CrossRefGoogle ScholarPubMed
Lazarov, O., Robinson, J., Tang, Y.-P., Hairston, I.S., Korade-Mirnics, Z., Lee, V.M.-Y., Hersh, L.B., Sapolsky, R.M., Mirnics, K., & Sisodia, S.S. (2005). Environmental enrichment reduces ab levels and amyloid deposition in transgenic mice. Cell, 120, 701–713.CrossRefGoogle Scholar
Loewenstein, D.A., Acevedo, A., Czaja, S.J., & Duara, R. (2004). Cognitive rehabilitation of mildly impaired Alzheimer’s disease patients on cholinesterase inhibitors. American Journal of Geriatric Psychiatry, 12, 395–402.CrossRefGoogle ScholarPubMed
McCormick, D.A. & Prince, D.A. (1985). Two types of muscarinic responses to acetylcholine in mammalian cortical neurons. Proceedings of the National Academy of Sciences, 82, 6344–6348.CrossRefGoogle ScholarPubMed
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 the Department of Health and Human Services Task Force on Alzheimer’s Disease. Neurology, 34, 939–944.CrossRefGoogle ScholarPubMed
McReynolds, L.V. & Kearns, K.P. (1983). Single-subject experimental designs in communicative disorders. Austin, TX: Pro-Ed.Google Scholar
Molteni, R., Ying, Z., & Gómez-Pinilla, F. (2002). Differential effects of acute and chronic exercise on plasticity-related genes in the rat hippocampus revealed by microarray. European Journal of Neuroscience, 16, 1107–1116.CrossRefGoogle ScholarPubMed
Nadeau, S.E., Behrman, A.L., Davis, S.E., Reid, K., Wu, S.S., Stidham, B.S., Helms, K.M., & Rothi, L.J.G. (2004). Donepezil: Possibly effective adjuvant to constraint induced therapy for upper extremity dysfunction after stroke. Journal of Rehabilitation Research and Development, 41, 525–535.CrossRefGoogle Scholar
Nadeau, S.E. & Rothi, L.J.G. (2004). Rehabilitation of language disorders. In Ponsford, J. (Ed.), Cognitive and behavioral rehabilitation: From neurobiology to clinical practice (pp. 129–174). New York: Guilford.Google Scholar
Nadeau, S.E., Rothi, L.J.G., & Rosenbek, J.C. (2008). Language rehabilitation from a neural perspective. In Chapey, R. (Ed.), language intervention strategies in aphasia and related neurogenic communication disorders (5th ed., pp. 689–734). Philadelphia, PA: Lippincott, Williams & Wilkins.Google Scholar
Nelson, D.L., McEvoy, C.L., & Schreiber, T.A. (1998). The University of South Florida Word Association, Rhyme, and Word Fragment Norms. http://www.usf.edu/FreeAssociation/.Google Scholar
Petersen, R.C., Stevens, J.C., Ganguli, M., Tangalos, E.G., Cummings, J.L., & DeKosky, S.T. (2001). Practice parameter: Early detection of dementia. Neurology, 56, 1133–1142.CrossRefGoogle ScholarPubMed
Rasmusson, D.D. (2000). The role of acetylcholine in cortical synaptic plasticity. Behavioural Brain Research, 115, 205–218.CrossRefGoogle ScholarPubMed
Rey, A. (1941). L’examen psychologique dans les cas d’encephalopathie traumatique. Archieves de Psychologie, 28, 286–340.Google Scholar
Robey, R.R. (2004). A five-phase model for clinical-outcome research. Journal of Communication Disorders, 37, 401–411.CrossRefGoogle ScholarPubMed
Robey, R.R. & Schultz, M.C. (1998). A model for conducting clincal-outcome research: An adaptation of the standard protocol for use in aphasiology. Aphasiology, 12, 787–810.CrossRefGoogle Scholar
Robey, R.R., Schultz, M.C., Crawford, A.B., & Sinner, C.A. (1999). Single-subject clinical-outcome research: Designs, data, effect sizes, and analyses. Aphasiology, 13, 445–473.CrossRefGoogle Scholar
Rodriguez, A.D. & Rothi, L.J.G. (2008). Principles in conducting rehabilitation research. In Stuss, D.T., Winocur, G., Robertson, I.H. (Eds.), Cognitive neurorehabilitation: Evidence and application (pp. 79–90). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Rogers, S.L., Doody, R.S., Pratt, R.D., & Ieni, J.R. (2000). Long-term efficacy and safety of donepezil in the treatment of Alzheimer’s disease: Final analysis of a multicentre open-label study. European Neuropsychopharmacology, 10, 195–203.CrossRefGoogle ScholarPubMed
Rogers, T.T., Ivanoiu, A., Patterson, K., & Hodges, J.R. (2006). Semantic memory in Alzheimer’s disease and the frontotemporal dementias: A longitudinal study of 236 patients. Neuropsychology, 20, 319–335.CrossRefGoogle ScholarPubMed
Roth, M., Tym, E., Mountjoy, C.Q., Huppert, F.A., Hendrie, H., Verma, S., & Goddard, R. (1986). CAMDEX – A standard instrument for the diagnosis of mental disorder in the elderly with special reference to the early detection of dementia. British Journal of Psychiatry, 149, 698–709.CrossRefGoogle Scholar
Rothi, L.J.G. (2006). Cognitive rehabilitation: The role of theoretical rationales and respect for the maturational process needed for our evidence. Journal of Head Trauma Research, 21, 194–197.Google Scholar
Rouleau, I., Salmon, D.P., Butters, N., Kennedy, C., & McGuire, K. (1992). Quantitative and qualitative analyses of clock drawings in Alzheimer’s and Huntington’s disease. Brain and Cognition, 18, 79–87.CrossRefGoogle ScholarPubMed
Royall, D.R., Mulroy, A.R., Chiodo, L.K., & Polk, M.J. (1999). Clock drawing is sensitive to executive control: A comparison of six methods. Journal of Gerontology, 54B, P328–P333.CrossRefGoogle Scholar
Rozzini, L., Costardi, D., Chilovi, B.V., Franzoni, S., Trabucchi, M., & Padovani, A. (2007). Efficacy of cognitive rehabilitation in patients with mild cognitive impairment treated with cholinesterase inhibitors. International Journal of Geriatric Psychiatry, 22, 356–360.CrossRefGoogle ScholarPubMed
Saponjic, R.M., Hoane, M.R., & Barth, T.M. (1998). Acetylcholine and recovery of function following brain injury. In Goldstein, L.B. (Ed.), Restorative neurology: Advances in pharmacotherapy for recovery after stroke (pp. 79–89). Armonk, NY: Futura Publishing.Google Scholar
Sarter, M. & Bruno, J.P. (1997). Cognitive functions of cortical acetylcholine: Toward a unifying hypothesis. Brain Research Reviews, 23, 28–46.CrossRefGoogle Scholar
Shulman, K.I., Pushkar, G.D., Cohen, C.A., & Zucchero, C.A. (1993). Clock-drawing and dementia in the community: A longitudinal study. International Journal of Geriatric Psychiatry, 8, 487–496.CrossRefGoogle Scholar
Schneider, L.S. (2001). Training of Alzheimer’s disease with cholinesterase inhibitors. Clinics in Geriatric Medicine, 17, 337–358.CrossRefGoogle Scholar
Small, G.W., Kaufer, D., Mendiondo, M.S., Quarg, P., & Speigel, R. (2005). Cognitive performance in Alzheimer’s disease patients receiving rivastigmine for up to 5 years. International Journal of Clinical Practice, 59, 473–477.CrossRefGoogle ScholarPubMed
Spreen, O. & Benton, A.L. (1969). Neurosensory Center Comprehensive Examination for Aphasia (NCCEA). Victoria: University of Victoria Neuropsychology Laboratory.Google Scholar
Tryon, W.W. (1982). A simplified time-series analysis for evaluating treatment interventions. Journal of Applied Behavior Analysis, 15, 423–429.CrossRefGoogle ScholarPubMed
van Praag, H., Kempermann, G., & Gage, F.H. (1999). Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nature Neuroscience, 2, 266–270.CrossRefGoogle ScholarPubMed
van Praag, H., Shubert, T., Zhao, C., & Gage, F.H. (2005). Exercise enhances learning and hippocampal neurogenesis in aged mice. Journal of Neuroscience, 25, 8680–8685.CrossRefGoogle ScholarPubMed
Webster, H.H., Hanisch, U.-K., Dykes, R.W., & Biesold, D. (1991). Basal forebrain lesions with or without reserpine injection inhibit cortical reorganization in rat hindpaw primary somatosensory cortex following sciatic nerve section. Somatosensory and Motor Research, 8, 327–346.CrossRefGoogle ScholarPubMed
Wezenberg, E., Verkes, R.J., Sabbe, B.G.C., Ruigt, G.S.F., & Hulstijn, W. (2005). Modulation of memory and visuospatial processes by biperiden and rivastigmine in elderly healthy subjects. Psychopharmacology, 181, 582–594.CrossRefGoogle ScholarPubMed
Whitehouse, P.J., Lerner, A., Hedera, P. (1993). Dementia. In Heilman, K.M., Valenstein, E. (Eds.), Clinical neuropsychology (pp 603–645). New York: Oxford University Press.Google Scholar