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Archival Report| Volume 76, ISSUE 6, P486-494, September 15, 2014

Working Memory in Schizophrenia: Behavioral and Neural Evidence for Reduced Susceptibility to Item-Specific Proactive Interference

      Background

      Susceptibility to item-specific proactive interference (PI) contributes to interindividual differences in working memory (WM) capacity and complex cognition relying on WM. Although WM deficits are a well-recognized impairment in schizophrenia, the underlying pathophysiological effects on specific WM control functions, such as the ability to resist item-specific PI, remain unknown. Moreover, opposing hypotheses on increased versus reduced PI susceptibility in schizophrenia are both justifiable by the extant literature.

      Methods

      To provide first insights into the behavioral and neural correlates of PI-related WM control in schizophrenia, a functional magnetic resonance imaging experiment was conducted in a sample of 20 patients and 20 well-matched control subjects. Demands on item-specific PI were experimentally manipulated in a recent-probes task (three runs, 64 trials each) requiring subjects to encode and maintain a set of four target items per trial.

      Results

      Compared with healthy control subjects, schizophrenia patients showed a significantly reduced PI susceptibility in both accuracy and latency measures. Notably, reduced PI susceptibility in schizophrenia was not associated with overall WM impairments and thus constituted an independent phenomenon. In addition, PI-related activations in inferior frontal gyrus and anterior insula, typically assumed to support PI resistance, were reduced in schizophrenia, thus ruling out increased neural efforts as a potential cause of the patients’ reduced PI susceptibility.

      Conclusions

      The present study provides first evidence for a diminished vulnerability of schizophrenia patients to item-specific PI, which is presumably a consequence of the patients’ more efficient clearing of previously relevant WM traces and the accordingly reduced likelihood for item-specific PI to occur.

      Key Words

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      References

        • Goldman-Rakic P.S.
        Working memory dysfunction in schizophrenia.
        J Neuropsychiatry Clin Neurosci. 1994; 6: 348-357
        • Lee J.
        • Park S.
        Working memory impairments in schizophrenia: A meta-analysis.
        J Abnorm Psychol. 2005; 114: 599-611
        • Kane M.J.
        • Engle R.W.
        Working-memory capacity, proactive interference, and divided attention: Limits on long-term memory retrieval.
        J Exp Psychol Learn Mem Cogn. 2000; 26: 336-358
        • Hasher L.
        • Lustig C.
        • Zacks R.
        Inhibitory mechanisms and the control of attention.
        in: Conway A. Jarrold C. Kane M. Miyake A. Towse J. Variation in Working Memory. Oxford University Press, New York2008
        • Dempster F.N.
        • Corkill A.J.
        Individual differences in susceptibility to interference and general cognitive ability.
        Acta Psychol (Amst). 1999; 101: 395-416
        • Lustig C.
        • May C.P.
        • Hasher L.
        Working memory span and the role of proactive interference.
        J Exp Psychol Gen. 2001; 130: 199-207
        • Gray J.R.
        • Chabris C.F.
        • Braver T.S.
        Neural mechanisms of general fluid intelligence.
        Nat Neurosci. 2003; 6: 316-322
        • Bunting M.
        Proactive interference and item similarity in working memory.
        J Exp Psychol Learn Mem Cogn. 2006; 32: 183-196
        • Burgess G.C.
        • Gray J.R.
        • Conway A.R.
        • Braver T.S.
        Neural mechanisms of interference control underlie the relationship between fluid intelligence and working memory span.
        J Exp Psychol Gen. 2011; 140: 674-692
        • Jonides J.
        • Nee D.E.
        Brain mechanisms of proactive interference in working memory.
        Neuroscience. 2006; 139: 181-193
        • Carter C.S.
        • Barch D.M.
        Cognitive neuroscience-based approaches to measuring and improving treatment effects on cognition in schizophrenia: The CNTRICS initiative.
        Schizophr Bull. 2007; 33: 1131-1137
        • Monsell S.
        Recency, immediate recognition memory, and reaction time.
        Cogn Psychol. 1978; 10: 465-501
        • Barch D.M.
        • Berman M.G.
        • Engle R.
        • Jones J.H.
        • Jonides J.
        • Macdonald 3rd, A.
        • et al.
        CNTRICS final task selection: Working memory.
        Schizophr Bull. 2009; 35: 136-152
        • Barch D.M.
        • Moore H.
        • Nee D.E.
        • Manoach D.S.
        • Luck S.J.
        CNTRICS imaging biomarkers selection: Working memory.
        Schizophr Bull. 2012; 38: 43-52
        • Mecklinger A.
        • Weber K.
        • Gunter T.C.
        • Engle R.W.
        Dissociable brain mechanisms for inhibitory control: Effects of interference content and working memory capacity.
        Brain Res Cogn Brain Res. 2003; 18: 26-38
        • Smith E.E.
        • Eich T.S.
        • Cebenoyan D.
        • Malapani C.
        Intact and impaired cognitive-control processes in schizophrenia.
        Schizophr Res. 2011; 126: 132-137
        • Gray J.A.
        • Feldon J.
        • Rawlins J.
        • Hemsley D.R.
        • Smith A.D.
        The neuropsychology of schizophrenia.
        Behav Brain Sci. 1991; 14: 1-84
        • Hemsley D.R.
        The development of a cognitive model of schizophrenia: Placing it in context.
        Neurosci Biobehav Rev. 2005; 29: 977-988
        • Westerhausen R.
        • Kompus K.
        • Hugdahl K.
        Impaired cognitive inhibition in schizophrenia: A meta-analysis of the Stroop interference effect.
        Schizophr Res. 2011; 133: 172-181
        • Friedman N.P.
        • Miyake A.
        The relations among inhibition and interference control functions: A latent-variable analysis.
        J Exp Psychol Gen. 2004; 133: 101-135
        • Randolph C.
        • Gold J.M.
        • Carpenter C.J.
        • Goldberg T.E.
        • Weinberger D.R.
        Release from proactive interference: Determinants of performance and neuropsychological correlates.
        J Clin Exp Neuropsychol. 1992; 14: 785-800
        • Traupmann K.L.
        • Berzofsky M.
        • Kesselman M.
        Encoding of taxonomic word categories by schizophrenics.
        J Abnorm Psychol. 1976; 85: 350-355
        • American Psychiatric Association
        Diagnostic and Statistical Manual of Mental Disorders, DSM-IV-TR.
        4th ed. American Psychiatric Association, Washington, DC2000
        • Andreasen N.C.
        Scale for the Assessment of Positive Symptoms (SAPS).
        University of Iowa, Iowa City1984
        • Andreasen N.C.
        Scale for the Assessment of Negative Symptoms (SANS).
        University of Iowa, Iowa City1984
        • Andreasen N.C.
        Scale for the assessment of thought, language, and communication (TLC).
        Schizophr Bull. 1986; 12: 473-482
        • Hamilton M.
        A rating scale for depression.
        J Neurol Neurosurg Psychiatry. 1960; 23: 56-62
        • Young R.C.
        • Biggs J.T.
        • Ziegler V.E.
        • Meyer D.A.
        A rating scale for mania: Reliability, validity and sensitivity.
        Br J Psychiatry. 1978; 133: 429-435
        • Ackenheil M.
        • Stotz G.
        • Dietz-Bauer R.
        • Vossen A.
        Mini International Neuropsychiatric Interview (German Version 5.0.0, DSM-IV).
        Psychiatrische Universitätsklinik, Munich1999
        • Fydrich T.
        • Renneberg B.
        • Schmitz B.
        • Wittchen H.U.
        Strukturiertes Klinisches Interview für DSM-IV. Achse II: Persönlichkeitsstörungen Interviewheft.
        Hogrefe, Göttingen, Germany1997
        • Lehrl S.
        Mehrfachwahl-Wortschatz-Intelligenztest MWT-B..
        Spitta Verlag, Balingen, Germany1999
        • Sternberg S.
        High-speed scanning in human memory.
        Science. 1966; 153: 652-654
        • Badre D.
        • Wagner A.D.
        Frontal lobe mechanisms that resolve proactive interference.
        Cereb Cortex. 2005; 15: 2003-2012
        • Kriegeskorte N.
        • Simmons W.K.
        • Bellgowan
        • Patrick S.F.
        • Baker C.I.
        Circular analysis in systems neuroscience: The dangers of double dipping.
        Nat Neurosci. 2009; 12: 535-540
        • Leonard C.J.
        • Kaiser S.T.
        • Robinson B.M.
        • Kappenman E.S.
        • Hahn B.
        • Gold J.M.
        • Luck S.J.
        Toward the neural mechanisms of reduced working memory capacity in schizophrenia.
        Cereb Cortex. 2013; 23: 1582-1592
        • Jonides J.
        • Smith E.E.
        • Marshuetz C.
        • Koeppe R.A.
        • Reuter-Lorenz P.A.
        Inhibition in verbal working memory revealed by brain activation.
        Proc Natl Acad Sci U S A. 1998; 95: 8410-8413
        • D’Esposito M.
        • Postle B.R.
        • Jonides J.
        • Smith E.E.
        The neural substrate and temporal dynamics of interference effects in working memory as revealed by event-related functional MRI.
        Proc Natl Acad Sci U S A. 1999; 96: 7514-7519
        • Postle B.R.
        • Brush L.N.
        • Nick A.M.
        Prefrontal cortex and the mediation of proactive interference in working memory.
        Cogn Affect Behav Neurosci. 2004; 4: 600-608
        • Nee D.E.
        • Jonides J.
        • Berman M.G.
        Neural mechanisms of proactive interference-resolution.
        Neuroimage. 2007; 38: 740-751
        • Bunge S.A.
        • Ochsner K.N.
        • Desmond J.E.
        • Glover G.H.
        • Gabrieli J.D.
        Prefrontal regions involved in keeping information in and out of mind.
        Brain. 2001; 124: 2074-2086
        • Nelson J.K.
        • Reuter-Lorenz P.A.
        • Sylvester C.C.
        • Jonides J.
        • Smith E.E.
        Dissociable neural mechanisms underlying response-based and familiarity-based conflict in working memory.
        Proc Natl Acad Sci U S A. 2003; 100: 11171-11175
        • Oberauer K.
        Removing irrelevant information from working memory: A cognitive aging study with the modified Sternberg task.
        J Exp Psychol Learn Mem Cogn. 2001; 27: 948-957
        • Oberauer K.
        Binding and inhibition in working memory: Individual and age differences in short-term recognition.
        J Exp Psychol Gen. 2005; 134: 368-387
        • Cowan N.
        Attention and Memory. An Integrated Framework.
        Oxford University Press, New York1995
        • Kane M.J.
        • Conway A.
        • Hambrick D.Z.
        • Engle R.W.
        Variation in working memory capacity as variation in executive attention and control.
        in: Conway A. Jarrold C. Kane M. Miyake A. Towse J. Variation in Working Memory. Oxford University Press, New York2008: 21-48
        • Goldberg T.E.
        • Patterson K.J.
        • Taqqu Y.
        • Wilder K.
        Capacity limitations in short-term memory in schizophrenia: Tests of competing hypotheses.
        Psychol Med. 1998; 28: 665-673
        • Driesen N.R.
        • Leung H.
        • Calhoun V.D.
        • Constable R.T.
        • Gueorguieva R.
        • Hoffman R.
        • et al.
        Impairment of working memory maintenance and response in schizophrenia: Functional magnetic resonance imaging evidence.
        Biol Psychiatry. 2008; 64: 1026-1034
        • Anticevic A.
        • Repovs G.
        • Barch D.M.
        Working memory encoding and maintenance deficits in schizophrenia: Neural evidence for activation and deactivation abnormalities.
        Schizophr Bull. 2013; 39: 168-178
        • Hahn B.
        • Hollingworth A.
        • Robinson B.M.
        • Kaiser S.T.
        • Leonard C.J.
        • Beck V.M.
        • et al.
        Control of working memory content in schizophrenia.
        Schizophr Res. 2012; 134: 70-75
        • Eich T.S.
        • Nee D.E.
        • Insel C.
        • Malapani C.
        • Smith E.E.
        Neural correlates of impaired cognitive control over working memory in schizophrenia [published online ahead of print October 10].
        Biol Psychiatry. 2013; (http://dx.doi.org/10.1016/j.biopsych.2013.09.032)
        • Bledowski C.
        • Kaiser J.
        • Rahm B.
        Basic operations in working memory: Contributions from functional imaging studies.
        Behav Brain Res. 2010; 214: 172-179
        • Sawaguchi T.
        • Goldman-Rakic P.S.
        D1 dopamine receptors in prefrontal cortex: Involvement in working memory.
        Science. 1991; 251: 947-950
        • Sawaguchi T.
        • Goldman-Rakic P.S.
        The role of D1-dopamine receptor in working memory: Local injections of dopamine antagonists into the prefrontal cortex of rhesus monkeys performing an oculomotor delayed-response task.
        J Neurophysiol. 1994; 71: 515-528
        • Barch D.M.
        What can research on schizophrenia tell us about the cognitive neuroscience of working memory?.
        Neuroscience. 2006; 139: 73-84
        • Rolls E.T.
        • Loh M.
        • Deco G.
        • Winterer G.
        Computational models of schizophrenia and dopamine modulation in the prefrontal cortex.
        Nat Rev Neurosci. 2008; 9: 696-709
        • Hemsley D.R.
        An experimental psychological model for schizophrenia.
        in: Hafner H. Gattaz W.F. Janzavik W. Search for the Causes of Schizophrenia. Springer, Heidelberg, Germany1987: 179-188
        • Baruch I.
        • Hemsley D.R.
        • Gray J.A.
        Differential performance of acute and chronic schizophrenics in a latent inhibition task.
        J Nerv Ment Dis. 1988; 176: 598-606
        • Beech A.
        • Powell T.
        • McWilliam J.
        • Claridge G.
        Evidence of reduced ‘cognitive inhibition’ in schizophrenia.
        Br J Clin Psychol. 1989; 28: 109-116
        • May C.P.
        • Kane M.J.
        • Hasher L.
        Determinants of negative priming.
        Psychol Bull. 1995; 118: 35-54
        • Peters E.R.
        • Pickering A.D.
        • Kent A.
        • Glasper A.
        • Irani M.
        • David A.S.
        • et al.
        The relationship between cognitive inhibition and psychotic symptoms.
        J Abnorm Psychol. 2000; 109: 386-395
        • Neill W.T.
        • Valdes L.A.
        • Terry K.M.
        • Gorfein D.S.
        Persistence of negative priming: II. Evidence for episodic trace retrieval.
        J Exp Psychol Learn Mem Cogn. 1992; 18: 993-1000
        • Fox E.
        Negative priming from ignored distractors in visual selection: A review.
        Psychol Bull Rev. 1995; 2: 145-173
        • Snodgrass J.G.
        • Vanderwart M.
        A standardized set of 260 pictures: Norms for name agreement, image agreement, familiarity, and visual complexity.
        J Exp Psychol Hum Learn. 1980; 6: 174-215