Skip to main content

Advertisement

SpringerLink
Log in

Competition between frontal lobe functions and implicit sequence learning: evidence from the long-term effects of alcohol

  • Research Article
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Abstract

Implicit sequence learning is a fundamental mechanism that underlies the acquisition of motor, cognitive and social skills. The relationship between implicit learning and executive functions is still debated due to the overlapping fronto-striatal networks. According to the framework of competitive neurocognitive networks, disrupting specific frontal lobe functions, such as executive functions, increases performance on implicit learning tasks. The aim of our study was to explore the nature of such a relationship by investigating the effect of long-term regular alcohol intake on implicit sequence learning. Since alcohol dependency impairs executive functions, we expected intact or even better implicit learning in patient group compared to the healthy controls based on the competitive relationship between these neurocognitive networks. To our knowledge, this is the first study to examine the long-term effects of alcohol dependency both on implicit learning and on executive functions requiring different but partly overlapping neurocognitive networks. Here, we show weaker executive functions but intact implicit learning in the alcohol-dependent group compared to the controls. Moreover, we found negative correlation between these functions in both groups. Our results confirm the competitive relationship between the fronto-striatal networks underlying implicit sequence learning and executive functions and suggest that the functional integrity of this relationship is unaltered in the alcohol-dependent group despite the weaker frontal lobe functions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Albouy G, Sterpenich V, Balteau E (2008) Both the hippocampus and striatum are involved in consolidation of motor sequence memory. Neuron 58:261–272

    Article  CAS  PubMed  Google Scholar 

  • Ashby FG, Ashby FG, Alfonso-Reese LA, Turken AU, Waldron EM (1998) A neuropsychological theory of multiple systems in category learning. Psychol Rev 105:442

    Article  CAS  PubMed  Google Scholar 

  • Ashby FG, Turner BO, Horvitz JC (2010) Cortical and basal ganglia contributions to habit learning and automaticity. Trends Cogn Sci 14:208–215

    Article  PubMed Central  PubMed  Google Scholar 

  • Baddeley A (1994) The magical number seven: still magic after all these years? Psychol Rev 101:353–356

    Article  CAS  PubMed  Google Scholar 

  • Baddeley A (1996) Exploring the central executive. Q J Exp Psychol Sect A 49:5–28

    Article  Google Scholar 

  • Baddeley A (2006) Working memory: an overview. In: Working memory and education, pp 1–31

  • Baddeley AD, Hitch G (1974) Working Memory. In: Bower GA (ed) The psychology of learning and motivation. Academic Press, New York, pp 47–89

    Google Scholar 

  • Baddeley A, Lewis V, Eldridge M, Thomson N (1984) Attention and retrieval from long-term memory. J Exp Psychol Gen 113:518

    Article  Google Scholar 

  • Baldo JV, Schwartz S, Wilkins D, Dronkers NF (2006) Role of frontal versus temporal cortex in verbal fluency as revealed by voxel-based lesion symptom mapping. J Int Neuropsychol Soc 12:896–900

    PubMed  Google Scholar 

  • Barnes KA, Howard JH Jr, Howard DV, Gilotty L, Kenworthy L, Gaillard WD, Vaidya CJ (2008) Intact implicit learning of spatial context and temporal sequences in childhood autism spectrum disorder. Neuropsychology 22:563–570

    Article  PubMed  Google Scholar 

  • Bellis MD, Narasimhan A, Thatcher DL, Keshavan MS, Soloff P, Clark DB (2005) Prefrontal cortex, thalamus, and cerebellar volumes in adolescents and young adults with adolescent-onset alcohol use disorders and comorbid mental disorders. Alcohol Clin Exp Res 29:1590–1600

    Article  PubMed  Google Scholar 

  • Bennett IJ, Howard J, James H, Howard DV (2007) Age-related differences in implicit learning of subtle third-order sequential structure. J Gerontol Psychol Sci 62B:P98–P103

    Article  Google Scholar 

  • Carpenter PA, Just MA, Reichle ED (2000) Working memory and executive function: evidence from neuroimaging. Curr Opin Neurobiol 10:195–199

    Article  CAS  PubMed  Google Scholar 

  • Case R, Kurland DM, Goldberg J (1982) Operational efficiency and the growth of short-term memory span. J Exp Child Psychol 33:386–404

    Article  Google Scholar 

  • Conway AR, Kane MJ, Bunting M, Hambrick DZ, Wilhelm O, Engle RW (2005) Working memory span tasks: a methodological review and user’s guide. Psychon Bull Rev 12:769–786

    Article  PubMed  Google Scholar 

  • Cowan N (1999) An embedded-process model of working memory. In: Miyake A, Shah P (eds) Models of working memory: mechanisms of active maintenance and executive control. Cambridge University Press, Cambridge, pp 62–101

    Chapter  Google Scholar 

  • Curtin JJ, Patrick CJ, Lang AR, Cacioppo JT, Birbaumer N (2001) Alcohol affects emotion through cognition. Psychol Sci 12:527–531

    Article  CAS  PubMed  Google Scholar 

  • Daneman M, Blennerhassett A (1984) How to assess the listening comprehension skills of prereaders. J Educ Psychol 76:1372–1381

    Article  Google Scholar 

  • Doyon J, Gaudreau D, Laforce R, Castonguay M, Bedard PJ, Bedard F, Bouchard JP (1997) Role of the striatum, cerebellum, and frontal lobes in the learning of a visuomotor sequence. Brain Cogn 34:218–245

    Article  CAS  PubMed  Google Scholar 

  • Doyon J, Bellec P, Amsel R (2009) Contributions of the basal ganglia and functionally related brain structures to motor learning. Behav Brain Res 199:61–75

    Article  PubMed  Google Scholar 

  • Duka T, Weissenborn R, Dienes Z (2001) State-dependent effects of alcohol on recollective experience, familiarity and awareness of memories. Psychopharmacology 153:295–306

    Article  CAS  PubMed  Google Scholar 

  • Egner T, Jamieson G, Gruzelier J (2005) Hypnosis decouples cognitive control from conflict monitoring processes of the frontal lobe. Neuroimage 27:969–978

    Article  PubMed  Google Scholar 

  • Engle RW, Tuholski SW, Laughlin JE, Conway ARA (1999) Working memory, short-term memory, and general fluid intelligence: a latent-variable approach. J Exp Psychol 128:309–331

    Article  CAS  Google Scholar 

  • Fama R, Pfefferbaum A, Sullivan EV (2006) Visuoperceptual learning in alcoholic Korsakoff syndrome. Alcohol Clin Exp Res 30:680–687

    Article  PubMed  Google Scholar 

  • Filoteo JV, Lauritzen S, Maddox WT (2010) Removing the frontal lobes the effects of engaging executive functions on perceptual category learning. Psychol Sci 21:415–423

    Article  PubMed Central  PubMed  Google Scholar 

  • Finn PR, Hall J (2004) Cognitive ability and risk for alcoholism: short-term memory capacity and intelligence moderate personality risk for alcohol problems. J Abnorm Psychol 113:569

    Article  PubMed  Google Scholar 

  • Frank MJ, O’Reilly RC, Curran T (2006) When memory fails, intuition reigns: midazolam enhances implicit inference in humans. Psychol Sci 17:700–707

    Article  PubMed  Google Scholar 

  • Galea JM, Albert NB, Ditye T, Miall RC (2010) Disruption of the dorsolateral prefrontal cortex facilitates the consolidation of procedural skills. J Cogn Neurosci 22:1158–1164

    Article  PubMed  Google Scholar 

  • Goldstein RZ, Leskovjan AC, Hoff AL et al (2004) Severity of neuropsychological impairment in cocaine and alcohol addiction: association with metabolism in the prefrontal cortex. Neuropsychologia 42:1447–1458

    Article  PubMed  Google Scholar 

  • Gruzelier JH (2006) Frontal functions, connectivity and neural efficiency underpinning hypnosis and hypnotic susceptibility. Contemp Hypn 23:15–32

    Article  Google Scholar 

  • Henke K (2010) A model for memory systems based on processing modes rather than consciousness. Nat Rev Neurosci 11:523–532

    Article  CAS  PubMed  Google Scholar 

  • Howard JH Jr, Howard DV (1997) Age differences in implicit learning of higher-order dependencies in serial patterns. Psychol Aging 12:634–656

    Article  PubMed  Google Scholar 

  • Howard DV, Howard JH Jr, Japikse K, DiYanni C, Thompson A, Somberg R (2004) Implicit sequence learning: effects of level of structure, adult age, and extended practice. Psychol Aging 19:79–92

    Article  PubMed Central  PubMed  Google Scholar 

  • Isaacs EB, Vargha-Khadem F (1989) Differential course of development of spatial and verbal memory span: a normative study. Br J Dev Psychol 7:377–380

    Article  Google Scholar 

  • Janacsek K, Nemeth D (2013) Implicit sequence learning and working memory: correlated or complicated? Cortex 49:2001–2006

    Article  PubMed  Google Scholar 

  • Janacsek K, Nemeth D (2015) The puzzle is complicated: when should working memory be related to implicit sequence learning, and when should it not? (Response to Martini et al.). Cortex 64:411–412

    Article  PubMed  Google Scholar 

  • Janacsek K, Tánczos T, Mészáros T, Nemeth D (2009) The Hungarian version of listening span task. Hung Rev Psychol 64:385–406

    Google Scholar 

  • Janacsek K, Fiser J, Nemeth D (2012) The best time to acquire new skills: age-related differences in implicit sequence learning across the human lifespan. Dev Sci 15:496–505

    Article  PubMed Central  PubMed  Google Scholar 

  • Kaiser J, Barker R, Haenschel C, Baldeweg T, Gruzelier JH (1997) Hypnosis and event-related potential correlates of error processing in a stroop-type paradigm: a test of the frontal hypothesis* 1. Int J Psychophysiol 27:215–222

    Article  CAS  PubMed  Google Scholar 

  • Kirchner TR, Sayette MA (2003) Effects of alcohol on controlled and automatic memory processes. Exp Clin Psychopharmacol 11:167

    Article  CAS  PubMed  Google Scholar 

  • Klivenyi P, Nemeth D, Sefcsik T, Janacsek K, Hoffmann I, Haden GP, Londe Z, Vecsei L (2012) Cognitive functions in ataxia with oculomotor apraxia type 2. Front Neurol 3(125):1–7

    Google Scholar 

  • Lister RG, Gorenstein C, Risher-Flowers D, Weingartner HJ, Eckardt MJ (1991) Dissociation of the acute effects of alcohol on implicit and explicit memory processes. Neuropsychologia 29:1205–1212

    Article  CAS  PubMed  Google Scholar 

  • Medina KL, McQueeny T, Nagel BJ, Hanson KL, Schweinsburg AD, Tapert SF (2008) Prefrontal cortex volumes in adolescents with alcohol use disorders: unique gender effects. Alcohol Clin Exp Res 32:386–394

    Article  PubMed Central  PubMed  Google Scholar 

  • Nemeth D, Janacsek K, Balogh V, Londe Z, Mingesz R, Fazekas M, Jambori S, Dányi I, Vetró Á (2010) Learning in autism: implicitly superb. PLoS ONE 5:e11731

    Article  PubMed Central  PubMed  Google Scholar 

  • Nemeth D, Janacsek K, Polner B, Kovacs ZA (2013) Boosting human learning by hypnosis. Cereb Cortex 23:801–805

    Article  PubMed  Google Scholar 

  • Noël X, Paternot J, Van der Linden M (2001) Correlation between inhibition, working memory and delimited frontal area blood flow measured by 99MTC–bicisate spect in alcohol–dependent patients. Alcohol Alcohol 36:556–563

    Article  PubMed  Google Scholar 

  • Oudman E, Van der Stigchel S, Wester AJ, Kessels RP, Postma A (2011) Intact memory for implicit contextual information in Korsakoff’s amnesia. Neuropsychologia 49:2848–2855

    Article  PubMed  Google Scholar 

  • Pfefferbaum A, Sullivan EV, Mathalon DH, Lim KO (1997) Frontal lobe volume loss observed with magnetic resonance imaging in older chronic alcoholics. Alcohol Clin Exp Res 21:521–529

    Article  CAS  PubMed  Google Scholar 

  • Poldrack R, Clark J, Pare-Blagoev EJ, Shohamy D, Creso Moyano J, Meyers C, Gluck MA (2001) Interactive memory systems in the human brain. Nature 414:546–550

    Article  CAS  PubMed  Google Scholar 

  • Racsmány M, Lukács Á, Németh D, Pléh C (2005) A verbális munkamemória magyar nyelvű vizsgálóeljárásai. Magyar Pszichológiai Szemle 60:479–506

    Article  Google Scholar 

  • Reber AS (1989) Implicit learning and tacit knowledge. J Exp Knowl 118:219–235

    Google Scholar 

  • Remillard G (2008) Implicit learning of second-, third-, and fourth-order adjacent and nonadjacent sequential dependencies. Q J Exp Psychol 61:400–424

    Article  Google Scholar 

  • Saults JS, Cowan N, Sher KJ, Moreno MV (2007) Differential effects of alcohol on working memory: distinguishing multiple processes. Exp Clin Psychopharmacol 15:576

    Article  PubMed Central  PubMed  Google Scholar 

  • Sefcsik T, Nemeth D, Janacsek K, Hoffmann I, Scialabba J, Klivenyi P, Ambrus G, Haden G, Vecsei L (2009) The role of the putamen in cognitive functions: a case study. Learn Percept 1:215–227

    Article  Google Scholar 

  • Soetens E, Melis A, Notebaert W (2004) Sequence learning and sequential effects. Psychol Res 69:124–137

    Article  CAS  PubMed  Google Scholar 

  • Song S, Howard JH, Howard DV (2007) Implicit probabilistic sequence learning is independent of explicit awareness. Learn Mem 14:167–176

    Article  PubMed Central  PubMed  Google Scholar 

  • Spreen O, Strauss E (1991) Language tests. In: A compendium of neuropsychological tests, pp 268–275

  • Tanczos T, Janacsek K, Nemeth D (2014a) Verbal fluency tasks I. Investigation of the Hungarian version of the letter fluency task between 5 and 89 years of age. Psychiatr Hung 29:158–180

    PubMed  Google Scholar 

  • Tanczos T, Janacsek K, Nemeth D (2014b) Verbal fluency tasks II. Investigation of the Hungarian version of the semantic fluency task between 5 and 89 years of age. Psychiatr Hung 29:181–207

    PubMed  Google Scholar 

  • Zinn S, Stein R, Swartzwelder HS (2004) Executive functioning early in abstinence from alcohol. Alcohol Clin Exp Res 28:1338–1346

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Hungarian Science Foundation KTIA NAP 13-2-2015-0002 (Dezso Nemeth), KTIA_NAP_13-1-2013-0001 (IV/5. Dr. Daniel Fabo) and Janos Bolyai Research Fellowship of the Hungarian Academy of Sciences (to K. J.).

Conflict of interest

The authors report no conflict of interest and have no financial disclosure.

Author information

Author notes

    Authors and Affiliations

    1. Department of Clinical Psychology and Addiction, Institute of Psychology, Eotvos Lorand University, Izabella utca 46, Budapest, 1064, Hungary

      Marta Virag, Karolina Janacsek & Dezso Nemeth

    2. National Institute of Clinical Neurosciences, Epilepy Centrum, Budapest, Hungary

      Marta Virag & Daniel Fabo

    3. MTA-ELTE NAP B Brain, Memory and Language Research Group, Institute of Cognitive Neuroscience and Psychology, Research Centre for Natural Sciences, MTA, Budapest, Hungary

      Karolina Janacsek & Dezso Nemeth

    4. Galfi Bela Hospital for Rehabilitation, Pomaz, Hungary

      Aniko Horvath & Zoltan Bujdoso

    Authors
    1. Marta Virag
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Karolina Janacsek
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Aniko Horvath
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Zoltan Bujdoso
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Daniel Fabo
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Dezso Nemeth
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Dezso Nemeth.

    Additional information

    Marta Virag and Karolina Janacsek have contributed equally to this work.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Virag, M., Janacsek, K., Horvath, A. et al. Competition between frontal lobe functions and implicit sequence learning: evidence from the long-term effects of alcohol. Exp Brain Res 233, 2081–2089 (2015). https://doi.org/10.1007/s00221-015-4279-8

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00221-015-4279-8

    Keywords

    Search

    Navigation