Hostname: page-component-7c8c6479df-nwzlb Total loading time: 0 Render date: 2024-03-28T15:03:07.073Z Has data issue: false hasContentIssue false

Salience of working-memory maintenance and manipulation deficits in schizophrenia

Published online by Cambridge University Press:  10 March 2010

S. K. Hill*
Affiliation:
Center for Cognitive Medicine, University of Illinois at Chicago, Chicago, IL, USA
G. B. Griffin
Affiliation:
Center for Cognitive Medicine, University of Illinois at Chicago, Chicago, IL, USA
T. Kazuto Miura
Affiliation:
Department of Psychology, Loyola University Chicago, Chicago, IL, USA
E. S. Herbener
Affiliation:
Center for Cognitive Medicine, University of Illinois at Chicago, Chicago, IL, USA
J. A. Sweeney
Affiliation:
Center for Cognitive Medicine, University of Illinois at Chicago, Chicago, IL, USA
*
*Address for correspondence: Dr S. Kristian Hill, Center for Cognitive Medicine, Department of Psychiatry (M/C 913), University of Illinois at Chicago, 912 South Wood Street, Suite 235, Chicago, IL60612, USA. (Email: shill@psych.uic.edu)

Abstract

Background

Encoding and maintenance of information in working memory, followed by internal manipulation of that information for planning adaptive behavior, are two key components of working-memory systems. Both processes have been reported to be impaired in schizophrenia, but few studies have directly compared the relative severity of these abnormalities, or the degree to which manipulation deficits might be secondary to alterations in maintenance processes.

Method

Clinically stable schizophrenia patients (n=25) and a demographically similar healthy comparison group (n=24) were administered a verbal span task with three levels of working-memory load. Maintenance was assessed using sequential position questions. Manipulation processes were assessed by requiring comparison of the relative sequential position of test items, which entailed simultaneous serial search strategies regarding item order.

Results

Both groups showed reduced accuracy and increased reaction time for manipulation compared with maintenance processing. There were significant patient impairments across working-memory loads. There was no differential deficit in manipulation processing, and effect sizes of relative deficit in the patient group were higher for maintenance than manipulation processing.

Conclusions

The strong correlation for maintenance and manipulation deficits suggest that impairments in the ability to internally manipulate information stored in working-memory systems are not greater than alterations in the encoding and maintaining of information in working memory and that disturbances in maintenance processing may contribute to deficits in higher-order working-memory operations.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2010

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

Baddeley, A (2000). The episodic buffer: a new component of working memory? Trends in Cognitive Sciences 4, 417423.CrossRefGoogle ScholarPubMed
Baddeley, A (2003). Working memory: looking back and looking forward. Nature Reviews Neuroscience 4, 829839.CrossRefGoogle ScholarPubMed
Barch, DM, Carter, CS, Braver, TS, Sabb, FW, MacDonald, A III, Noll, DC, Cohen, JD (2001). Selective deficits in prefrontal cortex function in medication-naive patients with schizophrenia. Archives of General Psychiatry 58, 280288.CrossRefGoogle ScholarPubMed
Cairo, TA, Woodward, TS, Ngan, ET (2006). Decreased encoding efficiency in schizophrenia. Biological Psychiatry 59, 740746.CrossRefGoogle ScholarPubMed
Cannon, TD, Glahn, DC, Kim, J, van Erp, TG, Karlsgodt, K, Cohen, MS, Nuechterlein, KH, Bava, S, Shirinyan, D (2005). Dorsolateral prefrontal cortex activity during maintenance and manipulation of information in working memory in patients with schizophrenia. Archives of General Psychiatry 62, 10711080.CrossRefGoogle ScholarPubMed
Christoff, K, Gabrieli, JDE (2000). The frontopolar cortex and human cognition: evidence for a rostrocaudal hierarchical organization within the human prefrontal cortex. Psychobiology 28, 168186.CrossRefGoogle Scholar
D'Esposito, M (2001). Functional neuroimaging of working memory. In Handbook of Functional Neuroimaging of Cognition (ed. Cabeza, R. and Kingstone, A.), MIT Press: Cambridge, MA.Google Scholar
D'Esposito, M, Aguirre, GK, Zarahn, E, Ballard, D, Shin, RK, Lease, J (1998). Functional MRI studies of spatial and nonspatial working memory. Cognitive Brain Research 7, 113.CrossRefGoogle ScholarPubMed
D'Esposito, M, Postle, BR, Ballard, D, Lease, J (1999). Maintenance versus manipulation of information held in working memory: an event-related fMRI study. Brain and Cognition 41, 6686.CrossRefGoogle ScholarPubMed
Driesen, NR, Leung, HC, Calhoun, VD, Constable, RT, Gueorguieva, R, Hoffman, R, Skudlarski, P, Goldman-Rakic, PS, Krystal, JH (2008). Impairment of working memory maintenance and response in schizophrenia: functional magnetic resonance imaging evidence. Biol Psychiatry 64, 10261034.CrossRefGoogle ScholarPubMed
Fraser, D, Park, S, Clark, G, Yohanna, D, Houk, JC (2004). Spatial serial order processing in schizophrenia. Schizophrenia Research 70, 203213.CrossRefGoogle ScholarPubMed
Glahn, DC, Kim, J, Cohen, MS, Poutanen, VP, Therman, S, Bava, S, van Erp, TG, Manninen, M, Huttunen, M, Lonnqvist, J, Standertskjold-Nordenstam, CG, Cannon, TD (2002). Maintenance and manipulation in spatial working memory: dissociations in the prefrontal cortex. Neuroimage 17, 201213.CrossRefGoogle ScholarPubMed
Hutton, SB, Huddy, V, Barnes, TR, Robbins, TW, Crawford, TJ, Kennard, C, Joyce, EM (2004). The relationship between antisaccades, smooth pursuit, and executive dysfunction in first-episode schizophrenia. Biological Psychiatry 56, 553559.CrossRefGoogle ScholarPubMed
Karlsgodt, KH, Sanz, J, van Erp, TG, Bearden, CE, Nuechterlein, KH, Cannon, TD (2009). Re-evaluating dorsolateral prefrontal cortex activation during working memory in schizophrenia. Schizophrenia Research 108, 143150.CrossRefGoogle ScholarPubMed
Keedy, SK, Ebens, CL, Keshavan, MS, Sweeney, JA (2006). Functional magnetic resonance imaging studies of eye movements in first episode schizophrenia: smooth pursuit, visually guided saccades and the oculomotor delayed response task. Psychiatry Research 146, 199211.CrossRefGoogle ScholarPubMed
Kim, J, Glahn, DC, Nuechterlein, KH, Cannon, TD (2004). Maintenance and manipulation of information in schizophrenia: further evidence for impairment in the central executive component of working memory. Schizophrenia Research 68, 173187.CrossRefGoogle ScholarPubMed
Lee, J, Park, S (2005). Working memory impairments in schizophrenia: a meta-analysis. Journal of Abnormal Psycholology 114, 599611.CrossRefGoogle ScholarPubMed
Lencz, T, Bilder, RM, Turkel, E, Goldman, RS, Robinson, D, Kane, JM, Lieberman, JA (2003). Impairments in perceptual competency and maintenance on a visual delayed match-to-sample test in first-episode schizophrenia. Archives of General Psychiatry 60, 238243.CrossRefGoogle ScholarPubMed
Low, A, Rockstroh, B, Harsch, S, Berg, P, Cohen, R (2000). Event-related potentials in a working-memory task in schizophrenics and controls. Schizophrenia Research 46, 175186.CrossRefGoogle Scholar
MacDonald, AW III, Carter, CS, Kerns, JG, Ursu, S, Barch, DM, Holmes, AJ, Stenger, VA, Cohen, JD (2005). Specificity of prefrontal dysfunction and context processing deficits to schizophrenia in never-medicated patients with first-episode psychosis. American Journal of Psychiatry 162, 475484.CrossRefGoogle ScholarPubMed
Manoach, DS (2003). Prefrontal cortex dysfunction during working memory performance in schizophrenia: reconciling discrepant findings. Schizophrenia Research 60, 285298.CrossRefGoogle ScholarPubMed
Mattay, VS, Goldberg, TE, Fera, F, Hariri, AR, Tessitore, A, Egan, MF, Kolachana, B, Callicott, JH, Weinberger, DR (2003). Catechol O-methyltransferase val158-met genotype and individual variation in the brain response to amphetamine. Proceedings of the National Academy of Sciences in the U.S.A 100, 61866191.CrossRefGoogle ScholarPubMed
Miyake, A, Shah, P (1999). Toward unified theories of working memory: Emerging general consensus, unresolved theoretical issues, and future research directions. In Models of Working Memory: Mechanisms of Maintenance and Executive Control (ed. Miyake, A. and Shah, P.), pp. 442481. Cambridge University Press: New York.CrossRefGoogle Scholar
Myles-Worsley, M, Park, S (2002). Spatial working memory deficits in schizophrenia patients and their first degree relatives from Palau, Micronesia. American Journal of Medical Genetics 114, 609615.CrossRefGoogle ScholarPubMed
Nunnally, CJ (1967). Psychometric Theory. McGraw-Hill: Columbus, OH.Google Scholar
Owen, AM, Evans, AC, Petrides, M (1996). Evidence for a two-stage model of spatial working memory processing within the lateral frontal cortex: a positron emission tomography study. Cerebral Cortex 6, 3138.CrossRefGoogle ScholarPubMed
Pantelis, C, Barnes, TR, Nelson, HE, Tanner, S, Weatherley, L, Owen, AM, Robbins, TW (1997). Frontal-striatal cognitive deficits in patients with chronic schizophrenia. Brain 120, 18231843.CrossRefGoogle ScholarPubMed
Park, S (1999). Hemispheric asymmetry of spatial working memory deficit in schizophrenia. International Journal of Psychophysiology 34, 313322.CrossRefGoogle ScholarPubMed
Park, S, Holzman, PS (1992). Schizophrenics show spatial working memory deficits. Archives of General Psychiatry 49, 975982.CrossRefGoogle ScholarPubMed
Park, S, Holzman, PS (1993). Association of working memory deficit and eye tracking dysfunction in schizophrenia. Schizophrenia Research 11, 5561.CrossRefGoogle ScholarPubMed
Park, S, Holzman, PS, Goldman-Rakic, PS (1995). Spatial working memory deficits in the relatives of schizophrenic patients. Archives of General Psychiatry 52, 821828.CrossRefGoogle ScholarPubMed
Park, S, Puschel, J, Sauter, BH, Rentsch, M, Hell, D (1999). Spatial working memory deficits and clinical symptoms in schizophrenia: a 4-month follow-up study. Biological Psychiatry 46, 392400.CrossRefGoogle ScholarPubMed
Park, S, Puschel, J, Sauter, BH, Rentsch, M, Hell, D (2003). Visual object working memory function and clinical symptoms in schizophrenia. Schizophrenia Research 59, 261268.CrossRefGoogle ScholarPubMed
Reilly, JL, Harris, MS, Keshavan, MS, Sweeney, JA (2006). Adverse effects of risperidone on spatial working memory in first-episode schizophrenia. Archives of General Psychiatry 63, 11891197.CrossRefGoogle ScholarPubMed
Reilly, JL, Harris, MS, Khine, TT, Keshavan, MS, Sweeney, JA (2008). Reduced attentional engagement contributes to deficits in prefrontal inhibitory control in schizophrenia. Biological Psychiatry 63, 776783.CrossRefGoogle ScholarPubMed
Reilly, JL, Harris, MSH, Khine, TT, Keshavan, MS, Sweeney, JA (2007). Antipsychotic drugs exacerbate impairment on a working memory task in first-episode schizophrenia. Biological Psychiatry 62, 818821.CrossRefGoogle ScholarPubMed
Rypma, B, Berger, JS, D'Esposito, M (2002). The influence of working-memory demand and subject performance on prefrontal cortical activity. Journal of Cognitive Neuroscience 14, 721731.CrossRefGoogle ScholarPubMed
Schneider, W, Eschmann, A, Zuccolotto, A (2002). E-prime User's Guide. Psychology Software Tools, Inc.: Pittsburgh, PA.Google Scholar
Tan, HY, Callicott, JH, Weinberger, DR (2007). Dysfunctional and compensatory prefrontal cortical systems, genes and the pathogenesis of schizophrenia. Cerebral Cortex 17, 171181.CrossRefGoogle ScholarPubMed
Tan, HY, Choo, WC, Fones, CS, Chee, MW (2005). fMRI study of maintenance and manipulation processes within working memory in first-episode schizophrenia. American Journal of Psychiatry 162, 18491858.CrossRefGoogle ScholarPubMed
Tan, HY, Sust, S, Buckholtz, JW, Mattay, VS, Meyer-Lindenberg, A, Egan, MF, Weinberger, DR, Callicott, JH (2006). Dysfunctional prefrontal regional specialization and compensation in schizophrenia. American Journal of Psychiatry 163, 19691977.CrossRefGoogle ScholarPubMed
Veltman, DJ, Rombouts, SA, Dolan, RJ (2003). Maintenance versus manipulation in verbal working memory revisited: an fMRI study. Neuroimage 18, 247256.CrossRefGoogle ScholarPubMed