Schizophrenia Research
Volume 117, Issue 1 , Pages 42-51 , March 2010

Working memory circuitry in schizophrenia shows widespread cortical inefficiency and compensation

  • Miyoung A. Kim

      Affiliations

    • Department of Psychiatry and Human Behavior, University of California, Irvine, CA 92617, USA
    • ,
  • Emanuela Tura

      Affiliations

    • Faculty of Medicine, University of British Columbia, Vancouver, BC, Canada V6T 1Z3
    • ,
  • Steven G. Potkin

      Affiliations

    • Department of Psychiatry and Human Behavior, University of California, Irvine, CA 92617, USA
    • ,
  • James H. Fallon

      Affiliations

    • Department of Psychiatry and Human Behavior, University of California, Irvine, CA 92617, USA
    • ,
  • Dara S. Manoach

      Affiliations

    • Department of Psychiatry, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA
    • Athinoula A. Martinos Center for Biomedical Imaging, Harvard Medical School, Boston MA, USA
    • ,
  • Vince D. Calhoun

      Affiliations

    • The Mind Research Network, Albuquerque, NM 87131, USA
    • Department of ECE, University of New Mexico, Albuquerque, NM 87131, USA
    • ,
  • FBIRN

      Affiliations

    • www.fbirn.org
    • ,
  • Jessica A. Turner

      Affiliations

    • Department of Psychiatry and Human Behavior, University of California, Irvine, CA 92617, USA
    • Corresponding Author InformationCorresponding author. 5251 California Avenue, Suite 240, Irvine, California, 92617, USA. Tel.: +1 949 824 3331; fax: +1 949 824 3324.

Received 2 September 2009 ,Revised 9 December 2009 ,Accepted 14 December 2009.

References 

  1. Andreasen NC. Modified Scale for the Assessment of Negative Symptoms (SANS). Iowa City, IA: University of Iowa; 1984;
  2. Andreasen NC. Scale for the Assessment of Positive Symptoms (SAPS). Iowa City, IA: University of Iowa; 1984;
  3. Barch DM, Sheline YI, Csernansky JG, Snyder AZ. Working memory and prefrontal cortex dysfunction: specificity to schizophrenia compared with major depression. Biol. Psychiatry. 2003;53(5):376–384
  4. Braver TS, Cohen JD, Nystrom LE, Jonides J, Smith EE, et al. A parametric study of prefrontal cortex involvement in human working memory. NeuroImage. 1997;5(1):49–62
  5. Brown GG, McCarthy G, Bischoff-Grethe A, Ozyurt B, Greve D, et al. Brain-performance correlates of working memory retrieval in schizophrenia: a cognitive modeling approach. Schizophr. Bull. 2009;35(1):32–46
  6. Cairo TA, Liddle PF, Woodward TS, Ngan ET. The influence of working memory load on phase specific patterns of cortical activity. Brain Res. 2004;21(3):377–387
  7. Callicott JH, Bertolino A, Mattay VS, Langheim FJ, Duyn J, et al. Physiological dysfunction of the dorsolateral prefrontal cortex in schizophrenia revisited. Cereb. Cortex. 2000;10(11):1078–1092
  8. Callicott JH, Egan MF, Mattay VS, Bertolino A, Bone AD, et al. Abnormal fMRI response of the dorsolateral prefrontal cortex in cognitively intact siblings of patients with schizophrenia. Am. J. Psychiatry. 2003;160(4):709–719
  9. Callicott JH, Ramsey NF, Tallent K, Bertolino A, Knable MB, et al. Functional magnetic resonance imaging brain mapping in psychiatry: methodological issues illustrated in a study of working memory in schizophrenia. Neuropsychopharmacology. 1998;18(3):186–196
  10. Cannon TD, Glahn DC, Kim J, Van Erp TG, Karlsgodt K, et al. Dorsolateral prefrontal cortex activity during maintenance and manipulation of information in working memory in patients with schizophrenia. Arch. Gen. Psychiatry. 2005;62(10):1071–1080
  11. Carter CS, Perlstein W, Ganguli R, Brar J, Mintun M, et al. Functional hypofrontality and working memory dysfunction in schizophrenia. Am. J. Psychiatry. 1998;155(9):1285–1287
  12. Dronkers NF, Wilkins DP, Van Valin RD, Redfern BB, Jaeger JJ. Lesion analysis of the brain areas involved in language comprehension. Cognition. 2004;92(1–2):145–177
  13. First MB, Spitzer RL, Gibbon M, Williams JBW. Structured Clinical Interview for DSM-IV-TR Axis I Disorders. Research Version, Patient Edition. (SCID-I/P) Biometrics Research. New York: New York State Psychiatric Institute; 2002;
  14. Friston KJ, Ashburner J, Frith CD, Poline J-B, Heather JD, Frackowiak RSJ. Spatial registration and normalization of images. Hum. Brain Mapp. 1995;2:165–189
  15. Friston KJ, Holmes AP, Worsley KJ, Poline JB, Frith CD, Frackowiak RSJ. Statistical parametric maps in functional imaging: a general linear approach. Hum. Brain Mapp. 1995;2:189–210
  16. Glahn DC, Ragland JD, Abramoff A, Barrett J, Laird AR, et al. Beyond hypofrontality: a quantitative meta-analysis of functional neuroimaging studies of working memory in schizophrenia. Hum. Brain Mapp. 2005;25(1):60–69
  17. Honey GD, Bullmore ET, Sharma T. Prolonged reaction time to a verbal working memory task predicts increased power of posterior parietal cortical activation. NeuroImage. 2000;12(5):495–503
  18. Honey GD, Bullmore ET, Sharma T. De-coupling of cognitive performance and cerebral functional response during working memory in schizophrenia. Schizophr. Res. 2002;53(1–2):45–56
  19. Jansma JM, Ramsey NF, van der Wee NJ, Kahn RS. Working memory capacity in schizophrenia: a parametric fMRI study. Schizophr. Res. 2004;68(2–3):159–171
  20. Johnson MR, Morris NA, Astur RS, Calhoun VD, Mathalon DH, et al. A functional magnetic resonance imaging study of working memory abnormalities in schizophrenia. Biol. Psychiatry. 2006;60(1):11–21
  21. Kim DI, Manoach DS, Mathalon DH, Turner JA, Mannell M, et al. Dysregulation of working memory and default-mode networks in schizophrenia using independent component analysis, an fBIRN and MCIC study. Human Brain Mapping. 2009;
  22. Koch K, Wagner G, Nenadic I, Schachtzabel C, Schultz C, et al. Fronto-striatal hypoactivation during correct information retrieval in patients with schizophrenia: an fMRI study. Neuroscience. 2008;153(1):54–62
  23. Koch K, Wagner G, Schultz C, Schachtzabel C, Nenadic I, et al. Altered error-related activity in patients with schizophrenia. Neuropsychologia. 2009;47(13):2843–2849
  24. Kuroki N, Shenton ME, Salisbury DF, Hirayasu Y, Onitsuka T, et al. Middle and inferior temporal gyrus gray matter volume abnormalities in first-episode schizophrenia: an MRI study. Am. J. Psychiatry. 2006;163(12):2103–2110
  25. Manoach DS. Prefrontal cortex dysfunction during working memory performance in schizophrenia: reconciling discrepant findings. Schizophr. Res. 2003;60(2–3):285–298
  26. Manoach DS, Gollub RL, Benson ES, Searl MM, Goff DC, et al. Schizophrenic subjects show aberrant fMRI activation of dorsolateral prefrontal cortex and basal ganglia during working memory performance. Biol. Psychiatry. 2000;48(2):99–109
  27. Manoach DS, Press DZ, Thangaraj V, Searl MM, Goff DC, et al. Schizophrenic subjects activate dorsolateral prefrontal cortex during a working memory task, as measured by fMRI. Biol. Psychiatry. 1999;45(9):1128–1137
  28. Manoach DS, Schlaug G, Siewert B, Darby DG, Bly BM, et al. Prefrontal cortex fMRI signal changes are correlated with working memory load. NeuroReport. 1997;8(2):545–549
  29. McIntosh AR, Bookstein FL, Haxby JV, Grady CL. Spatial pattern analysis of functional brain images using partial least squares. NeuroImage. 1996;3(3 Pt 1):143–157
  30. McIntosh AR, Lobaugh NJ. Partial least squares analysis of neuroimaging data: applications and advances. NeuroImage. 2004;23(Suppl 1):S250–S263
  31. Mendrek A, Kiehl KA, Smith AM, Irwin D, Forster BB, et al. Dysfunction of a distributed neural circuitry in schizophrenia patients during a working-memory performance. Psychol. Med. 2005;35(2):187–196
  32. Onitsuka T, Shenton ME, Salisbury DF, Dickey CC, Kasai K, et al. Middle and inferior temporal gyrus gray matter volume abnormalities in chronic schizophrenia: an MRI study. Am. J. Psychiatry. 2004;161(9):1603–1611
  33. Owen AM, McMillan KM, Laird AR, Bullmore E. N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Hum. Brain Mapp. 2005;25(1):46–59
  34. Perlstein WM, Carter CS, Noll DC, Cohen JD. Relation of prefrontal cortex dysfunction to working memory and symptoms in schizophrenia. Am. J. Psychiatry. 2001;158(7):1105–1113
  35. Perlstein WM, Dixit NK, Carter CS, Noll DC, Cohen JD. Prefrontal cortex dysfunction mediates deficits in working memory and prepotent responding in schizophrenia. Biol. Psychiatry. 2003;53(1):25–38
  36. Potkin SG, Turner JA, Brown GG, McCarthy G, Greve DN, et al. Working memory and DLPFC inefficiency in schizophrenia: the FBIRN study. Schizophr. Bull. 2009;35(1):19–31
  37. Quintana J, Wong T, Ortiz-Portillo E, Kovalik E, Davidson T, et al. Prefrontal–posterior parietal networks in schizophrenia: primary dysfunctions and secondary compensations. Biol. Psychiatry. 2003;53(1):12–24
  38. Ragland JD, Moelter ST, Bhati MT, Valdez JN, Kohler CG, et al. Effect of retrieval effort and switching demand on fMRI activation during semantic word generation in schizophrenia. Schizophr. Res. 2008;99(1–3):312–323
  39. Ragland JD, Yoon J, Minzenberg MJ, Carter CS. Neuroimaging of cognitive disability in schizophrenia: search for a pathophysiological mechanism. Int. Rev. Psychiatry. 2007;19(4):417–427
  40. Ramsey NF, Koning HA, Welles P, Cahn W, van der Linden JA, et al. Excessive recruitment of neural systems subserving logical reasoning in schizophrenia. Brain. 2002;125(Pt 8):1793–1807
  41. Rypma B, D'Esposito M. The roles of prefrontal brain regions in components of working memory: effects of memory load and individual differences. Proc. Natl Acad. Sci. USA. 1999;96(11):6558–6563
  42. Schlosser RGM, Koch K, Wagner G, Nenadic I, Roebel M, et al. Inefficient executive cognitive control in schizophrenia is preceded by altered functional activation during information encoding: an fMRI study. Neuropsychologia. 2008;46:336–347
  43. Strand F, Forssberg H, Klingberg T, Norrelgen F. Phonological working memory with auditory presentation of pseudo-words — an event related fMRI study. Brain Res. 2008;1212:48–54
  44. Thermenos HW, Goldstein JM, Buka SL, Poldrack RA, Koch JK, et al. The effect of working memory performance on functional MRI in schizophrenia. Schizophr. Res. 2005;74(2–3):179–194
  45. Van Snellenberg JX, Torres IJ, Thornton AE. Functional neuroimaging of working memory in schizophrenia: task performance as a moderating variable. Neuropsychology. 2006;20(5):497–510
  46. Walter H, Vasic N, Hose A, Spitzer M, Wolf RC. Working memory dysfunction in schizophrenia compared to healthy controls and patients with depression: evidence from event-related fMRI. NeuroImage. 2007;35(4):1551–1561
  47. Wold H. Estimation of principal components and related models by iterative least squares. In:  Krishnaiah PR editors. Multivariate Analysis. New York: Academic Press; 1966;

PII: S0920-9964(09)00605-7

doi: 10.1016/j.schres.2009.12.014

Schizophrenia Research
Volume 117, Issue 1 , Pages 42-51 , March 2010

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