Genuine Episodic Memory Deficits and Executive Dysfunctions in Alcoholic Subjects Early in Abstinence
Anne Lise Pitel
Inserm–EPHE–Université de Caen/Basse-Normandie, Unité E0218, GIP Cyceron, CHU Côte de Nacre, Caen, France
Search for more papers by this authorHélène Beaunieux
Inserm–EPHE–Université de Caen/Basse-Normandie, Unité E0218, GIP Cyceron, CHU Côte de Nacre, Caen, France
Search for more papers by this authorThomas Witkowski
Inserm–EPHE–Université de Caen/Basse-Normandie, Unité E0218, GIP Cyceron, CHU Côte de Nacre, Caen, France
Search for more papers by this authorFrançois Vabret
Inserm–EPHE–Université de Caen/Basse-Normandie, Unité E0218, GIP Cyceron, CHU Côte de Nacre, Caen, France
Service d'Alcoologie, CHR Clémenceau, Caen, France
Search for more papers by this authorBérengère Guillery-Girard
Inserm–EPHE–Université de Caen/Basse-Normandie, Unité E0218, GIP Cyceron, CHU Côte de Nacre, Caen, France
Search for more papers by this authorPeggy Quinette
Inserm–EPHE–Université de Caen/Basse-Normandie, Unité E0218, GIP Cyceron, CHU Côte de Nacre, Caen, France
Search for more papers by this authorBéatrice Desgranges
Inserm–EPHE–Université de Caen/Basse-Normandie, Unité E0218, GIP Cyceron, CHU Côte de Nacre, Caen, France
Search for more papers by this authorFrancis Eustache
Inserm–EPHE–Université de Caen/Basse-Normandie, Unité E0218, GIP Cyceron, CHU Côte de Nacre, Caen, France
Search for more papers by this authorAnne Lise Pitel
Inserm–EPHE–Université de Caen/Basse-Normandie, Unité E0218, GIP Cyceron, CHU Côte de Nacre, Caen, France
Search for more papers by this authorHélène Beaunieux
Inserm–EPHE–Université de Caen/Basse-Normandie, Unité E0218, GIP Cyceron, CHU Côte de Nacre, Caen, France
Search for more papers by this authorThomas Witkowski
Inserm–EPHE–Université de Caen/Basse-Normandie, Unité E0218, GIP Cyceron, CHU Côte de Nacre, Caen, France
Search for more papers by this authorFrançois Vabret
Inserm–EPHE–Université de Caen/Basse-Normandie, Unité E0218, GIP Cyceron, CHU Côte de Nacre, Caen, France
Service d'Alcoologie, CHR Clémenceau, Caen, France
Search for more papers by this authorBérengère Guillery-Girard
Inserm–EPHE–Université de Caen/Basse-Normandie, Unité E0218, GIP Cyceron, CHU Côte de Nacre, Caen, France
Search for more papers by this authorPeggy Quinette
Inserm–EPHE–Université de Caen/Basse-Normandie, Unité E0218, GIP Cyceron, CHU Côte de Nacre, Caen, France
Search for more papers by this authorBéatrice Desgranges
Inserm–EPHE–Université de Caen/Basse-Normandie, Unité E0218, GIP Cyceron, CHU Côte de Nacre, Caen, France
Search for more papers by this authorFrancis Eustache
Inserm–EPHE–Université de Caen/Basse-Normandie, Unité E0218, GIP Cyceron, CHU Côte de Nacre, Caen, France
Search for more papers by this authorThis study was funded by Inserm (ATC Alcool).
Abstract
Background: Chronic alcoholism is known to impair episodic memory function, but the specific nature of this impairment is still unclear. Moreover, it has never been established whether episodic memory deficit in alcoholism is an intrinsic memory deficit or whether it has an executive origin. Thus, the objectives are to specify which episodic memory processes are impaired early in abstinence from alcohol and to determine whether they should be regarded as genuine memory deficits or rather as the indirect consequences of executive impairments.
Methods: Forty recently detoxified alcoholic inpatients at alcohol entry treatment and 55 group-matched controls underwent a neuropsychological assessment of episodic memory and executive functions. The episodic memory evaluation consisted of 3 tasks complementing each other designed to measure the different episodic memory components (learning, storage, encoding and retrieval, contextual memory, and autonoetic consciousness) and 5 executive tasks testing capacities of organization, inhibition, flexibility, updating, and integration.
Results: Compared with control subjects, alcoholic patients presented impaired learning abilities, encoding processes, retrieval processes, contextual memory and autonoetic consciousness. However, there was no difference between the 2 groups regarding the storage capacities assessed by the rate of forgetting. Concerning executive functions, alcoholic subjects displayed deficits in each executive task used. Nevertheless, stepwise regression analyses showed that only performances on fluency tasks were significantly predictive of some of the episodic memory disorders (learning abilities for 40%, encoding processes for 20%, temporal memory for 21%, and state of consciousness associated with memories for 26%) in the alcoholic group.
Discussion: At alcohol treatment entry, alcoholic patients present genuine episodic memory deficits that cannot be regarded solely as the consequences of executive dysfunctions. These results are in accordance with neuroimaging findings showing hippocampal atrophy. Moreover, given the involvement of episodic memory and executive functions in alcohol treatment, these data could have clinical implications.
REFERENCES
- Agartz I, Momenan R, Rawlings RR, Kerich MJ, Hommer DW (1999) Hippocampal volume in patients with alcohol dependence. Arch Gen Psychiatry 56: 356–363.
- Ambrose ML, Bowden SC, Whelan G (2001) Working memory impairments in alcohol-dependent participants without clinical amnesia. Alcohol Clin Exp Res 25: 185–191.
- American Psychiatric Association (1994) Diagnostic and Statistical Manual of Mental Disorders. American Psychiatric Association, Washington.
- Aupée AM, Desgranges B, Eustache F, Lalevée C, De La Sayette V, Viader F, Baron JC (2001) Voxel-based mapping of brain hypometabolism in permanent amnesia with PET. Neuroimage 13: 1164–1173.
- Baddeley A (1986) Working Memory. Oxford University Press, Oxford.
- Baddeley A (1996) The fractionation of working memory. Proc Natl Acad Sci U S A 93: 13468–13472.
- Baddeley A (2000) The episodic buffer: a new component of working memory? Trends Cogn Sci 4: 417–423.
- Baddeley A (2003) Working memory: looking back and looking forward. Nat Rev Neurosci 4: 829–839.
- Baddeley A, Wilson BA (1994) When implicit learning fails: amnesia and the problem of error elimination. Neuropsychologia 32: 53–68.
- Bartels C, Kunert HJ, Stawicki S, Kroner-Herwig B, Ehrenreich H, Krampe H (2006) Recovery of hippocampus-related functions in chronic alcoholics during monitored long-term abstinence. Alcohol Alcohol Dec 21 [epub ahead of print].
- Beatty WW, Katzung VM, Moreland VJ, Nixon SJ (1995) Neuropsychological performance of recently abstinent alcoholics and cocaine abusers. Drug Alcohol Depend 37: 247–253.
- Beatty WW, Tivis R, Stott HD, Nixon SJ, Parsons OA (2000) Neuropsychological deficits in sober alcoholics: influences of chronicity and recent alcohol consumption. Alcohol Clin Exp Res 24: 149–154.
- Beresford TP, Arciniegas DB, Alfers J, Clapp L, Martin B, Du Y, Liu D, Shen D, Davatzikos C (2006) Hippocampus volume loss due to chronic heavy drinking. Alcohol Clin Exp Res 30: 1866–1870.
- Bleich S, Sperling W, Degner D, Graesel E, Bleich K, Wilhelm J, Havemann-Reinecke U, Javaheripour K, Kornhuber J (2003) Lack of association between hippocampal volume reduction and first-onset alcohol withdrawal seizure. A volumetric MRI study. Alcohol Alcohol 38: 40–44.
- Blume AW, Schmaling KB, Marlatt GA (2005) Memory, executive cognitive function, and readiness to change drinking behavior. Addict Behav 30: 301–314.
- Brokate B, Hildebrandt H, Eling P, Fichtner H, Runge K, Timm C (2003) Frontal lobe dysfunctions in Korsakoff's syndrome and chronic alcoholism: continuity or discontinuity? Neuropsychology 17: 420–428.
- Buschke H, Sliwinski M, Kuslansky G, Lipton RB (1995) Aging, encoding specificity, and memory change in the Double Memory Test. J Int Neuropsychol Soc 1: 483–493.
- Cardebat D, Doyon B, Puel M, Goulet P, Joanette Y (1990) Formal and semantic lexical evocation in normal subjects. Performance and dynamics of production as a function of sex, age and educational level. Acta Neurol Belg 90: 207–217.
- Chételat G, Desgranges B, De La Sayette V, Viader F, Berkouk K, Landeau B, Lalevée C, Le Doze F, Dupuy B, Hannequin D, Baron JC, Eustache F (2003) Dissociating atrophy and hypometabolism impact on episodic memory in mild cognitive impairment. Brain 126: 1955–1967.
- Curran HV, Hildebrandt M (1999) Dissociative effects of alcohol on recollective experience. Conscious Cogn 8: 497–509.
- Dao-Castellana MH, Samson Y, Legault F, Martinot JL, Aubin HJ, Crouzel C, Feldman L, Barrucand D, Rancurel G, Feline A, Syrota A (1998) Frontal dysfunction in neurologically normal chronic alcoholic subjects: metabolic and neuropsychological findings. Psychol Med 28: 1039–1048.
- Davidson PS, Troyer AK, Moscovitch M (2006) Frontal lobe contributions to recognition and recall: linking basic research with clinical evaluation and remediation. J Int Neuropsychol Soc 12: 210–223.
- De Rosa E, Sullivan EV (2003) Enhanced release from proactive interference in nonamnesic alcoholic individuals: implications for impaired associative binding. Neuropsychology 17: 469–481.
- Demir B, Ulug B, Lay EE, Erbas B (2002) Regional cerebral blood flow and neuropsychological functioning in early and late onset alcoholism. Psychiatry Res 115: 115–125.
- DiClemente CC, Bellino LE, Neavins TM (1999) Motivation for change and alcoholism treatment. Alcohol Res Health 23: 86–92.
- Duka T, Weissenborn R, Dienes Z (2001) State-dependent effects of alcohol on recollective experience, familiarity and awareness of memories. Psychopharmacology (Berlin) 153: 295–306.
- Everett M, Schaeffer KW, Parsons OA (1988) Learning impairment in male and female alcoholics. Arch Clin Neuropsychol 3: 203–211.
- Fama R, Pfefferbaum A, Sullivan EV (2004) Perceptual learning in detoxified alcoholic men: contributions from explicit memory, executive function, and age. Alcohol Clin Exp Res 28: 1657–1665.
- Fox AM, Coltheart M, Solowij N, Michie PT, Fox GA (2000) Dissociable cognitive impairments in problem drinkers. Alcohol Alcohol 35: 52–54.
- Gardiner JM, Ramponi C, Richardson-Klavehn A (1998) Experiences of remembering, knowing, and guessing. Conscious Cogn 7: 1–26.
- Gardiner JM, Ramponi C, Richardson-Klavehn A (2002) Recognition memory and decision processes: a meta-analysis of remember, know, and guess responses. Memory 10: 83–98.
- Glenn SW, Parsons OA (1992) Neuropsychological efficiency measures in male and female alcoholics. J Stud Alcohol 53: 546–552.
- Glisky EL, Delaney SM (1996) Implicit memory and new semantic learning in posttraumatic amnesia. J Head Trauma Rehabil 11: 31–42.
- Goldstein RZ, Leskovjan AC, Hoff AL, Hitzemann R, Bashan F, Khalsa SS, Wang GJ, Fowler JS, Volkow ND (2004) Severity of neuropsychological impairment in cocaine and alcohol addiction: association with metabolism in the prefrontal cortex. Neuropsychologia 42: 1447–1458.
- Grant BF, Harford T, Dawson D, Chou P, Dufour M, Pickering R (1994) Prevalence of DSM-IV alcohol abuse and dependence: US, 1992. Alcohol Health Res World 18: 243–248.
- Grober E, Buschke H (1987) Genuine memory deficits in dementia. Dev Neuropsychol 3: 13–36.
- Grober E, Buschke H, Crystal H, Bang S, Dresner R (1988) Screening for dementia by memory testing. Neurology 38: 900–903.
- Habib R, Nyberg L, Tulving E (2003) Hemispheric asymmetries of memory: the HERA model revisited. Trends Cogn Sci 7: 241–245.
- Hildebrandt H, Brokate B, Eling P, Lanz M (2004) Response shifting and inhibition, but not working memory, are impaired after long-term heavy alcohol consumption. Neuropsychology 18: 203–211.
- Horner MD, Waid LR, Johnson DE, Latham PK, Anton RF (1999) The relationship of cognitive functioning to amount of recent and lifetime alcohol consumption in outpatient alcoholics. Addict Behav 24: 449–453.
- Ihara H, Berrios GE, London M (2000) Group and case study of the dysexecutive syndrome in alcoholism without amnesia. J Neurol Neurosurg Psychiatry 68: 731–737.
- Inserm (Institut National de la Santé et de la Recherche Médicale) Expertise Collective 2001. Available at: http://ist.inserm.fr/basisrapports/alcool.html. Accessed February 7, 2007.
- Joyce EM, Robbins TW (1991) Frontal lobe function in Korsakoff and non-Korsakoff alcoholics: planning and spatial working memory. Neuropsychologia 29: 709–723.
- Kapur S, Craik FI, Tulving E, Wilson AA, Houle S, Brown GM (1994) Neuroanatomical correlates of encoding in episodic memory: levels of processing effect. Proc Natl Acad Sci U S A 91: 2008–2011.
- Kopelman MD, Stanhope N, Kingsley D (1997) Temporal and spatial context memory in patients with focal frontal, temporal lobe, and diencephalic lesions. Neuropsychologia 35: 1533–1545.
- Kramer JH, Rosen HJ, Du AT, Schuff N, Hollnagel C, Weiner MW, Miller BL, Delis DC (2005) Dissociations in hippocampal and frontal contributions to episodic memory performance. Neuropsychology 19: 799–805.
- McAndrews MP, Milner B (1991) The frontal cortex and memory for temporal order. Neuropsychologia 29: 849–859.
- Miyake A, Friedman NP, Emerson MJ, Witzki AH, Howerter A, Wager TD (2000) The unity and diversity of executive functions and their contributions to complex “Frontal Lobe” tasks: a latent variable analysis. Cognit Psychol 41: 49–100.
- Moselhy HF, Georgiou G, Kahn A (2001) Frontal lobe changes in alcoholism: a review of the literature. Alcohol Alcohol 36: 357–368.
- Munro CA, Saxton J, Butters MA (2000) The neuropsychological consequences of abstinence among older alcoholics: a cross-sectional study. Alcohol Clin Exp Res 24: 1510–1516.
- Nixon SJ, Tivis RD, Jenkins MR, Parsons OA (1998) Effects of cues on memory in alcoholics and controls. Alcohol Clin Exp Res 22: 1065–1069.
- Noel X, Paternot J, Van der Linden M., Sferrazza R, Verhas M, Hanak C, Kornreich C, Martin P, De Mol J, Pelc I, Verbanck P (2001a) Correlation between inhibition, working memory and delimited frontal area blood flow measure by 99mTc-Bicisate SPECT in alcohol-dependent patients. Alcohol Alcohol 36: 556–563.
- Noel X, Van der Linden M., Schmidt N, Sferrazza R, Hanak C, Le Bon O, De Mol J, Kornreich C, Pelc I, Verbanck P (2001b) Supervisory attentional system in nonamnesic alcoholic men. Arch Gen Psychiatry 58: 1152–1158.
- Oscar-Berman M, Kirkley SM, Gansler DA, Couture A (2004) Comparisons of Korsakoff and non-Korsakoff alcoholics on neuropsychological tests of prefrontal brain functioning. Alcohol Clin Exp Res 28: 667–675.
- Parsons OA, Nixon SJ (1993) Neurobehavioral sequelae of alcoholism. Alcohol Clin Exp Res 11: 206–218.
- Pitel AL, Witkowski T, Vabret F, Guillery-Girard B, Desgranges B, Eustache F, Beaunieux H (2007) Effect of episodic and working memory impairments on semantic and cognitive procedural learning at alcohol treatment entry. Alcohol Clin Exp Res 31: 238–248.
- Postma A, Van AM, Keuper O, Wester AJ, Kessels RP (2006) Spatial and temporal order memory in Korsakoff patients. J Int Neuropsychol Soc 12: 327–336.
- Quinette P, Guillery B, Desgranges B, De La Sayette V, Viader F, Eustache F (2003) Working memory and executive functions in transient global amnesia. Brain 126: 1917–1934.
- Quinette P, Guillery-Girard B, Noël A, De La Sayette V, Viader F, Desgranges B, Eustache F (2006) The relationship between working memory and episodic memory disorders in transient global amnesia. Neuropsychologia 44: 2508–2519.
- Reed RJ, Grant I, Rourke SB (1992) Long-term abstinent alcoholics have normal memory. Alcohol Clin Exp Res 16: 677–683.
- Roehrich L, Goldman MS (1993) Experience-dependent neuropsychological recovery and the treatment of alcoholism. J Consult Clin Psychol 61: 812–821.
- Rourke SB, Grant I (1999) The interactive effects of age and length of abstinence on the recovery of neuropsychological functioning in chronic male alcoholics: a 2-year follow-up study. J Int Neuropsychol Soc 5: 234–246.
- Schaeffer KW, Parsons OA (1987) Learning impairment in alcoholics using an ecologically relevant test. J Nerv Ment Dis 175: 213–218.
- Sherer M, Nixon SJ, Parsons OA, Adams RL (1992) Performance of alcoholic and brain-damaged subjects on the Luria Memory Words test. Arch Clin Neuropsychol 7: 499–504.
- Stroop J (1935) Studies of interference in serial verbal reactions. J Exp Psychol 18: 643–662.
- Sullivan EV, Fama R, Rosenbloom MJ, Pfefferbaum A (2002) A profile of neuropsychological deficits in alcoholic women. Neuropsychology 16: 74–83.
- Sullivan EV, Marsh L, Mathalon DH, Lim KO, Pfefferbaum A (1995) Anterior hippocampal volume deficits in nonamnesic, aging chronic alcoholics. Alcohol Clin Exp Res 19: 110–122.
- Sullivan EV, Rosenbloom MJ, Pfefferbaum A (2000) Pattern of motor and cognitive deficits in detoxified alcoholic men. Alcohol Clin Exp Res 24: 611–621.
- Sullivan EV, Shear PK, Zipursky RB, Sagar HJ, Pfefferbaum A (1997) Patterns of content, contextual, and working memory impairments in schizophrenia and nonamnesic alcoholism. Neuropsychology 11: 195–206.
- Tedstone D, Coyle K (2004) Cognitive impairments in sober alcoholics: performance on selective and divided attention tasks. Drug Alcohol Depend 75: 277–286.
- Tivis R, Beatty WW, Nixon SJ, Parsons OA (1995) Patterns of cognitive impairment among alcoholic: are there subtypes? Alcohol Clin Exp Res 19: 496–500.
- Tulving E (2001) Episodic memory and common sense: how far apart? Philos Trans Roy Soc Lond B Biol Sci 356: 1505–1515.
- Tulving E, Kapur S, Craik FI, Moscovitch M, Houle S (1994) Hemispheric encoding/retrieval asymmetry in episodic memory: positron emission tomography findings. Proc Natl Acad Sci U S A 91: 2016–2020.
- Uekermann J, Daum I, Schlebusch P, Wiebel B, Trenckmann U (2003) Depression and cognitive functioning in alcoholism. Addiction 98: 1521–1529.
- Weingartner HJ, Andreason PJ, Hommer DW, Sirocco KY, Rio DE, Ruttimann UE, Rawlings RR, Eckardt MJ (1996) Monitoring the source of memory in detoxified alcoholics. Biol Psychiatry 40: 43–53.
- Wheeler MA, Stuss DT, Tulving E (1997) Toward a theory of episodic memory: the frontal lobes and autonoetic consciousness. Psychol Bull 121: 331–354.
- Zimmermann P, Fimm B (1993) Testbatterie zur Erfassung von Aufmerksamkeitsstorungen. Psytest, Freiburg.
- Zinn S, Stein R, Swartzwelder HS (2004) Executive functioning early in abstinence from alcohol. Alcohol Clin Exp Res 28: 1338–1346.