Skip to main content
SpringerLink
Log in

Directed forgetting in schizophrenia

Prefrontal memory and inhibition deficits

  • ORIGINAL PAPER
  • Published:
European Archives of Psychiatry and Clinical Neuroscience Aims and scope Submit manuscript

Abstract

Schizophrenia is associated with cognitive deficits in the domains of working memory, strategic memory and other executive functions. In the current study we used a computerised and item–cued variant of the directed forgetting (DF) task to assess inhibitory processes in verbal memory. Twenty–five patients with schizophrenia and a group of matched controls were tested. Recognition memory was better for to–be–remembered (TBR) than for to–be–forgotten (TBF) words in both patients and controls. As compared to healthy controls the patients with schizophrenia showed overall memory deficits and difficulties to inhibit memories as indicated by a significant group by cue interaction and a smaller DF effect. The DF effect was associated with disease duration but not with symptom severity. Memoryrelated inhibition problems are difficult to assess in patients with schizophrenia and might be related to fronto–temporal disconnection.

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

Similar content being viewed by others

References

  1. Anderson MC, Green C (2001) Suppressing unwanted memories by executive control. Nature 410:366–369

    Article  PubMed  Google Scholar 

  2. Anderson MC, Ochsner KN, Kuhl B, Cooper J, Robertson E, Gabrieli SW, Glover GH, Gabrieli JD (2004) Neural systems underlying the suppression of unwanted memories. Science 303:232–235

    Article  PubMed  Google Scholar 

  3. Aleman A, Hijman R, de Haan EH, Kahn RS (1999) Memory impairment in schizophrenia: a meta-analysis. Am J Psychiatry 156:1358–1366

    PubMed  Google Scholar 

  4. Andreasen NC, Paradiso S, O’Leary DS (1998) “Cognitive dysmetria” as an integrative theory of schizophrenia: a dysfunction in cortical-subcortical-cerebellar circuitry? Schizophr Bull 24:203–218

    PubMed  Google Scholar 

  5. Andrés P, Van der Linden M (2002) Are central executive functions working in patients with focal frontal lesions? Neuropsychologia 40:835–845

    Article  PubMed  Google Scholar 

  6. Andrés P, Van der Linden M, Parmentier FB (2004) Directed forgetting in working memory: age-related differences. Memory 12:248–256

    Article  PubMed  Google Scholar 

  7. Aron A, Robbins T, Poldrack R (2004) Inhibition and the right inferior frontal cortex. Trends Cogn Sci 8:170–177

    Article  PubMed  Google Scholar 

  8. Barch DM, Carter CS, Hachten PC, Usher M, Cohen JD (1999) The “benefits” of distractibility: mechanisms underlying increased Stroop effects in schizophrenia. Schizophr Bull 25:749–762

    PubMed  Google Scholar 

  9. Barch DM, Csernansky JG, Conturo T, Snyder AZ (2002) Working and long-term memory deficits in schizophrenia: is there a common prefrontal mechanism? J Abnorm Psychol 111:478–494

    Article  PubMed  Google Scholar 

  10. Basden BH, Basden DR (1996) Directed forgetting: further comparisons of the item and list methods. Memory 4:633–653

    PubMed  Google Scholar 

  11. Braver TS, Barch DM, Cohen JD (1999) Cognition and control in schizophrenia: a computational model of dopamine and prefrontal function. Biol Psychiatry 46:312–328

    Article  PubMed  Google Scholar 

  12. Bokat CE, Goldberg TE (2003) Letter and category fluency in schizophrenic patients: a meta-analysis. Schizophr Res 64:73–78

    Article  PubMed  Google Scholar 

  13. Cameron AM, Oram J, Geffen GM, Kavanagh DJ, McGrath JJ, Geffen LB (2002) Working memory correlates of three symptom clusters in schizophrenia. Psychiatry Res 110:49–61

    Article  PubMed  Google Scholar 

  14. Cirillo MA, Seidman LJ (2003) Verbal declarative memory dysfunction in schizophrenia: from clinical assessment to genetics and brain mechanisms. Neuropsychol Rev 13:43–77

    Article  PubMed  Google Scholar 

  15. Cohen JD, Servan-Schreiber D (1992) Context, cortex, and dopamine: a connectionist approach to behavior and biology in schizophrenia. Psychol Rev 99:45–77

    Article  PubMed  Google Scholar 

  16. Conway MA, Fthenaki A (2003) Disruption of inhibitory control of memory following lesions to the frontal and temporal lobes. Cortex 39:667–686

    PubMed  Google Scholar 

  17. Dulaney CL, Marks W, Link KE (2004) Aging and directed forgetting: pre-cue encoding and post-cue rehearsal effects. Exp Aging Res 30:95–112

    PubMed  Google Scholar 

  18. Elvevåg B, Egan MF, Goldberg TE (2000) Paired-associate learning and memory interference in schizophrenia. Neuropsychologia 38:1565–1575

    Article  PubMed  Google Scholar 

  19. Elvevåg B, Goldberg TE (2000) Cognitive impairment in schizophrenia is the core of the disorder. Crit Rev Neurobiol 14:1–21

    PubMed  Google Scholar 

  20. Earles JL, Kersten AW (2002) Directed forgetting of actions by younger and older adults. Psychol Bull Rev 9:383–388

    Google Scholar 

  21. Ferman TJ, Primeau M, Delis D, Jampala CV (1999) Global-local processing in schizophrenia: hemispheric asymmetry and symptom-specific interference. J Int Neuropsychol Soc 5:442–451

    Article  PubMed  Google Scholar 

  22. Fleck DE, Berch DB, Shear PK, Schefft BK, Privitera MD, Strakowski SM (1999) Directed forgetting deficits in patients with temporal lobe epilepsy: an information processing perspective. J Int Neuropsychol Soc 5:549–555

    Article  PubMed  Google Scholar 

  23. Friston KJ (1999) Schizophrenia and the disconnection hypothesis. Acta Psychiatr Scand 395(Suppl):68–79

    Google Scholar 

  24. Frith CD, Leary J, Cahill C, Johnstone EC (1991) Performance on psychological tests: demographic and clinical correlates of the results of these tests. In: Johnstone EC (ed) Disabilities and Circumstances of Schizophrenic Patients: A Follow-up Study. Br J Psychiatry 159(Suppl 13):26–29

    Google Scholar 

  25. Fuentes LJ, Boucart M, Vivas AB, Alvarez R, Zimmerman MA (2000) Inhibitory tagging in inhibition of return is affected in schizophrenia: evidence from the stroop task. Neuropsychology 14:134–140

    Article  PubMed  Google Scholar 

  26. Goldman-Rakic PS (1999) The physiological approach: functional architecture of working memory and disordered cognition in schizophrenia. Biol Psychiatry 46:650–661

    Article  PubMed  Google Scholar 

  27. Green MF, Kern RS, Braff DL, Mintz J (2000) Neurocognitive deficits and functional outcome in schizophrenia: are we measuring the “right stuff ”? Schizophr Bull 26:119–136

    PubMed  Google Scholar 

  28. Harvey PD, Keefe RS (2001) Studies of cognitive change in patients with schizophrenia following novel antipsychotic treatment. Am J Psychiatry 158:176–184

    Article  PubMed  Google Scholar 

  29. Heckers S, Rauch SL, Goff D, Savage CR, Schacter DL, Fischman AJ, Alpert NM (1998) Impaired recruitment of the hippocampus during conscious recollection in schizophrenia. Nat Neurosci 1:318–323

    Article  PubMed  Google Scholar 

  30. Heinrichs RW, Zakzanis KK (1998) Neurocognitive deficit in schizophrenia: a quantitative review of the evidence. Neuropsychology 12:426–445

    Article  PubMed  Google Scholar 

  31. Henik A, Carter CS, Salo R, Chaderjian M, Kraft L, Nordahl TE, Robertson LC (2002) Attentional control and word inhibition in schizophrenia. Psychiatry Res 110:137–149

    Article  PubMed  Google Scholar 

  32. Hofer A, Weiss EM, Golaszewski SM, Siedentopf CM, Brinkhoff C, Kremser C, Felber S, Fleischhacker WW (2003) An fMRI study of episodic encoding and recognition of words in patients with schizophrenia in remission. Am J Psychiatry 160:911–918

    Article  PubMed  Google Scholar 

  33. Iddon JL, McKenna PJ, Sahakian BJ, Robbins TW (1998) Impaired generation and use of strategy in schizophrenia: evidence from visuospatial and verbal tasks. Psychol Med 28:1049–1062

    Article  PubMed  Google Scholar 

  34. Janca A, Hiller W (1996) ICD-10 checklists: a tool for clinicians’ use of the ICD-10 classification of mental and behavioural disorders. Compr Psychiatry 37:180–187

    Article  PubMed  Google Scholar 

  35. Jessen F, Scheef L, Germeshausen L, Tawo Y, Kockler M, Kuhn KU, Maier W, Schild HH, Heun R (2003) Reduced hippocampal activation during encoding and recognition of words in schizophrenia patients. Am J Psychiatry 160:1305–1312

    Article  PubMed  Google Scholar 

  36. Johnson HM (1994) Processes of successful intentional forgetting. Psychol Bull 116:274–292

    Google Scholar 

  37. Johnson-Selfridge M, Zalewski C (2001) Moderator variables of executive functioning in schizophrenia: meta-analytic findings. Schizophr Bull 27:305–316

    PubMed  Google Scholar 

  38. Kaasinen V, Rinne JO (2002) Functional imaging studies of dopamine system and cognition in normal aging and Parkinson’s disease. Neurosci Biobehav Rev 26:785–793

    Article  PubMed  Google Scholar 

  39. Kapur S (2003) Psychosis as a state of aberrant salience: a framework linking biology, phenomenology, and pharmacology in schizophrenia. Am J Psychiatry 160:13–23

    Article  PubMed  Google Scholar 

  40. Kay SR, Fiszbein A, Opler LA (1987) The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull 13:261–276

    PubMed  Google Scholar 

  41. Keefe RS, Mohs RC, Bilder RM, Harvey PD, Green MF, Meltzer HY, Gold JM, Sano M (2003) Neurocognitive assessment in the Clinical Antipsychotic Trials of Intervention Effectiveness (CATIE) project schizophrenia trial: development, methodology, and rationale. Schizophr Bull 29:45–55

    PubMed  Google Scholar 

  42. Liddle PF, Morris DL (1991) Schizophrenic syndromes and frontal lobe performance. Br J Psychiatry 158:340–345

    PubMed  Google Scholar 

  43. MacLeod CM (1998) Directed forgetting. In: Golding JM, MacLeod CM (eds) Intentional Forgetting: Interdisciplinary Approaches. Lawrence Earlbaum, Mahwah, pp 1–57

  44. Meltzer HY (1999) Treatment of schizophrenia and spectrum disorders: pharmacotherapy, psychosocial treatments, and neurotransmitter interactions. Biol Psychiatry 46:1321–1327

    Article  PubMed  Google Scholar 

  45. Menon M, Pomarol-Clotet E, McKenna PJ, McCarthy RA (2004) Exploring memory control in schizophrenia using a modified directed forgetting paradigm (abstract). Schizophr Res 67 (Suppl):264

    Google Scholar 

  46. Moritz S, Jacobsen D, Mersmann K, Kloss M, Andresen B (2000) Negative priming in schizophrenia: no evidence for reduced cognitive inhibition. J Nerv Mental Disord 188:624–627

    Article  Google Scholar 

  47. Müller U, Gruber O (1999) Prefrontal cortex and schizophrenia. Psycho 25:489–495

    Google Scholar 

  48. Müller U, Wächter T, Barthel H, Reuter M, von Cramon DY (2000) Striatal [123I]β-CIT SPECT and prefrontal memory functions in Parkinson’s disease. J Neural Transm 107:303–319

    Article  PubMed  Google Scholar 

  49. Müller U, Werheid K, Hammerstein E, Sachweh S, Becker T (2004) Prefrontal cognitive deficits in patients with schizophrenia treated with atypical or conventional antipsychotics. Eur Psychiatry (in press)

  50. Nieuwenstein MR, Aleman A, de Haan EH (2001) Relationship between symptom dimensions and neurocognitive functioning in schizophrenia: a meta-analysis of WCST and CPT studies. J Psychiatry Res 35:119–125

    Google Scholar 

  51. Paz-Caballero MD, Menor J, Jimenez JM (2004) Predictive validity of event-related potentials (ERPs) in relation to the directed forgetting effects. Clin Neurophysiol 115:369–377

    Article  PubMed  Google Scholar 

  52. Robbins TW (1990) The case of frontostriatal dysfunction in schizophrenia. Schizophr Bull 16:391–402

    PubMed  Google Scholar 

  53. Roesch-Ely D, Spitzer M,Weisbrod M (2003) Cognitive inhibition and thought disorder in schizophrenia. Psychopathology 36:23–32

    Article  PubMed  Google Scholar 

  54. Schmitter-Edgecombe M, Marks W, Wright MJ, Ventura M (2004) Retrieval inhibition in directed forgetting following severe closed-head injury. Neuropsychology 18:104–114

    Article  PubMed  Google Scholar 

  55. Schnider A, Ptak R (1999) Spontaneous confabulators fail to suppress currently irrelevant memory traces. Nat Neurosci 2:677–681

    Article  PubMed  Google Scholar 

  56. Simon AE, Giacomini V, Ferrero F, Mohr S (2003) Is executive function associated with symptom severity in schizophrenia? Eur Arch Psychiatry Clin Neurosci 253:216–218

    Article  PubMed  Google Scholar 

  57. Sonntag P, Gokalsing E, Olivier C, Robert P, Burglen F, Kauffmann- Muller F, Huron C, Salame P, Danion JM (2003) Impaired strategic regulation of contents of conscious awareness in schizophrenia. Conscious Cogn 12:190–200

    Article  PubMed  Google Scholar 

  58. Stone M, Gabrieli JD, Stebbins GT, Sullivan EV (1998) Working and strategic memory deficits in schizophrenia. Neuropsychology 12:278–288

    Article  PubMed  Google Scholar 

  59. Ullsperger M (2000) The Role of Retrieval Inhibition in Directed Forgetting – An Event-Related Brain Potential Analysis (MPI Series in Cognitive Neuroscience 13). MPI of Cognitive Neuroscience, Leipzig

  60. Ullsperger M, Mecklinger A, Müller U (2000) An electrophysiological test of directed forgetting: the role of retrieval inhibition. J Cogn Neurosci 12:924–920

    Article  PubMed  Google Scholar 

  61. Volkow ND, Logan J, Fowler JS, Wang GJ, Gur RC, Wong C, Felder C, Gatley SJ, Ding YS, Hitzemann R, Pappas N (2000) Association between age-related decline in brain dopamine activity and impairment in frontal and cingulate metabolism. Am J Psychiatry 157:75–80

    Article  PubMed  Google Scholar 

  62. Waters FA, Badcock JC, Maybery MT, Michie PT (2003) Inhibition in schizophrenia: association with auditory hallucinations. Schizophr Res 62:275–280

    Article  PubMed  Google Scholar 

  63. Weiss AP, Dodson CS, Goff DC, Schacter DL, Heckers S (2002) Intact suppression of increased false recognition in schizophrenia. Am J Psychiatry 159:1506–1513

    Article  PubMed  Google Scholar 

  64. Weiss AP, Schacter DL, Goff DC, Rauch SL, Alpert NM, Fischman AJ, Heckers S (2003) Impaired hippocampal recruitment during normal modulation of memory performance in schizophrenia. Biol Psychiatry 53:48–55

    Article  PubMed  Google Scholar 

  65. Werheid K, Hoppe C, Thöne A, Müller U, Müngersdorf M, von Cramon DY (2002) The adaptive digit ordering test: clinical application, reliability and validity of a verbal working memory test. Arch Clin Neuropsychol 17:547–565

    Article  PubMed  Google Scholar 

  66. Zacks RT, Hasher L (1994) Directed Ignoring: inhibitory regulation of working memory. In: Dagenbach D, Carr TH (eds) Inhibitory Processes in Attention, Memory, and Language. Academic Press, San Diego, pp 241–264

  67. Zacks RT, Radvansky G, Hasher L (1996) Studies of directed forgetting in older adults. J Exp Psychol Learn Mem Cogn 22:143–156

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Dept. of Psychiatry, University of Leipzig, Leipzig, Germany

    U. Müller, E. Hammerstein, S. Sachweh & T. Becker

  2. Dept. of Experimental Psychology, University of Cambridge, Downing Site, Cambridge CB2 3EB, UK

    U. Müller

  3. Max-Planck-Institute for Human Cognitive and Brain Sciences, Leipzig, Germany

    M. Ullsperger

  4. Dept. of Psychiatry II, University of Ulm, BKH Günzburg, Günzburg, Germany

    T. Becker

Authors
  1. U. Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. M. Ullsperger
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. E. Hammerstein
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. S. Sachweh
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. T. Becker
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to U. Müller.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Müller, U., Ullsperger, M., Hammerstein, E. et al. Directed forgetting in schizophrenia. Eur Arch Psychiatry Clin Neurosci 255, 251–257 (2005). https://doi.org/10.1007/s00406-004-0554-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00406-004-0554-6

Key words

Search

Navigation