Schizophrenia Research
Volume 115, Issue 2 , Pages 163-172 , December 2009

Grey and white matter abnormalities are associated with impaired spatial working memory ability in first-episode schizophrenia

  • Luca Cocchi

      Affiliations

    • Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne & Melbourne Health, Melbourne, Australia
    • Corresponding Author InformationCorresponding author. Melbourne Neuropsychiatry Centre, The University of Melbourne, c/o National Neuroscience Facility, 161 Barry Street, Carlton South 3053, Australia. Tel.: +61 3 8344 1861; fax: +61 3 9348 0469.
    web address
    • ,
  • Mark Walterfang

      Affiliations

    • Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne & Melbourne Health, Melbourne, Australia
    • ,
  • Renée Testa

      Affiliations

    • Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne & Melbourne Health, Melbourne, Australia
    • ,
  • Stephen J. Wood

      Affiliations

    • Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne & Melbourne Health, Melbourne, Australia
    • ,
  • Marc L. Seal

      Affiliations

    • Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne & Melbourne Health, Melbourne, Australia
    • ,
  • John Suckling

      Affiliations

    • Department of Psychiatry, University of Cambridge, Cambridge, United Kingdom
    • ,
  • Tsutomu Takahashi

      Affiliations

    • Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne & Melbourne Health, Melbourne, Australia
    • Department of Neuropsychiatry, University of Toyama, Toyama, Japan
    • ,
  • Tina-Marie Proffitt

      Affiliations

    • ORYGEN Research Centre, The University of Melbourne & Melbourne Health
    • ,
  • Warrick J. Brewer

      Affiliations

    • ORYGEN Research Centre, The University of Melbourne & Melbourne Health
    • ,
  • Christopher Adamson

      Affiliations

    • Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne & Melbourne Health, Melbourne, Australia
    • Developmental and Functional Brain Imaging, Murdoch Children's Research Institute, Royal Children's Hospital, Melbourne, Australia
    • ,
  • Bridget Soulsby

      Affiliations

    • Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne & Melbourne Health, Melbourne, Australia
    • ,
  • Dennis Velakoulis

      Affiliations

    • Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne & Melbourne Health, Melbourne, Australia
    • ,
  • Patrick D. McGorry

      Affiliations

    • ORYGEN Research Centre, The University of Melbourne & Melbourne Health
    • ,
  • Christos Pantelis

      Affiliations

    • Melbourne Neuropsychiatry Centre, Department of Psychiatry, The University of Melbourne & Melbourne Health, Melbourne, Australia

Received 2 February 2009 ,Revised 3 August 2009 ,Accepted 7 September 2009.

References 

  1. Antonova E, Kumari V, Morris R, Halari R, Anilkumar A, Mehrotra R, et al. The relationship of structural alterations to cognitive deficits in schizophrenia: a voxel-based morphometry study. Biol. Psychiatry. 2005;58:457–467
  2. Bartzokis G, Nuechterlein KH, Lu PH, Gitlin M, Rogers S, Mintz J. Dysregulated brain development in adult men with schizophrenia: a magnetic resonance imaging study. Biol. Psychiatry. 2003;53:412–421
  3. Bottmer C, Bachmann S, Pantel J, Essig M, Amann M, Schad LR, et al. Reduced cerebellar volume and neurological soft signs in first-episode schizophrenia. Psychiatry Res. 2005;140:239–250
  4. Brammer MJ, Bullmore ET, Simmons A, Williams SC, Grasby PM, Howard RJ, et al. Generic brain activation mapping in functional magnetic resonance imaging: a nonparametric approach. Magn. Reson. Imaging. 1997;15:763–770
  5. Bullmore E, Long C, Suckling J, Fadili J, Calvert G, Zelaya F, et al. Colored noise and computational inference in neurophysiological (fMRI) time series analysis: resampling methods in time and wavelet domains. Hum. Brain Mapp. 2001;12:61–78
  6. Bullmore ET, Suckling J, Overmeyer S, Rabe-Hesketh S, Taylor E, Brammer MJ. Global, voxel, and cluster tests, by theory and permutation, for a difference between two groups of structural MR images of the brain. IEEE Trans. Med. Imaging. 1999;18:32–42
  7. Chua SE, Cheung C, Cheung V, Tsang JT, Chen EY, Wong JC, et al. Cerebral grey, white matter and csf in never-medicated, first-episode schizophrenia. Schizophr. Res. 2007;89:12–21
  8. Cocchi L, Debbané M, Vianin P, Bircher R, Roulin S, Conus P, et al. Encoding dysfunctions in a dynamic–static paradigm for visuospatial working memory in first-episode psychosis patients: a 2-year follow-up study. Early Intervention in Psychiatry. 2009;3:44–51
  9. Danckert J, Saoud M, Maruff P. Attention, motor control and motor imagery in schizophrenia: implications for the role of the parietal cortex. Schizophr. Res. 2004;70:241–261
  10. Davis KL, Stewart DG, Friedman JI, Buchsbaum M, Harvey PD, Hof PR, et al. White matter changes in schizophrenia: evidence for myelin-related dysfunction. Arch. Gen. Psychiatry. 2003;60:443–456
  11. Douaud G, Smith S, Jenkinson M, Behrens T, Johansen-Berg H, Vickers J, et al. Anatomically related grey and white matter abnormalities in adolescent-onset schizophrenia. Brain. 2007;130:2375–2386
  12. Fornito A, Yucel M, Patti J, Wood SJ, Pantelis C. Mapping grey matter reductions in schizophrenia: an anatomical likelihood estimation analysis of voxel-based morphometry studies. Schizophr. Res. 2009;108:104–113
  13. Friedman JI, Tang C, Carpenter D, Buchsbaum M, Schmeidler J, Flanagan L, et al. Diffusion tensor imaging findings in first-episode and chronic schizophrenia patients. Am. J. Psychiatry. 2008;165:1024–1032
  14. Friston KJ, Frith CD. Schizophrenia: a disconnection syndrome?. Clin. Neurosci. 1995;3:89–97
  15. Glahn DC, Laird AR, Ellison-Wright I, Thelen SM, Robinson JL, Lancaster JL, et al. Meta-analysis of gray matter anomalies in schizophrenia: application of anatomic likelihood estimation and network analysis. Biol. Psychiatry. 2008;64:774–781
  16. Goldman-Rakic PS. Working memory dysfunction in schizophrenia. J. Neuropsychiatry Clin. Neurosci. 1994;6:348–357
  17. Goldman-Rakic PS, Selemon LD. Functional and anatomical aspects of prefrontal pathology in schizophrenia. Schizophr. Bull. 1997;23:437–458
  18. Good CD, Ashburner J, Frackowiak RS. Computational neuroanatomy: new perspectives for neuroradiology. Rev. Neurol. (Paris). 2001;157:797–806
  19. Good CD, Scahill RI, Fox NC, Ashburner J, Friston KJ, Chan D, et al. Automatic differentiation of anatomical patterns in the human brain: validation with studies of degenerative dementias. Neuroimage. 2002;17:29–46
  20. Hazlett EA, Buchsbaum MS, Haznedar MM, Newmark R, Goldstein KE, Zelmanova Y, et al. Cortical gray and white matter volume in unmedicated schizotypal and schizophrenia patients. Schizophr. Res. 2008;101:111–123
  21. Karlsgodt KH, van Erp TG, Poldrack RA, Bearden CE, Nuechterlein KH, Cannon TD. Diffusion tensor imaging of the superior longitudinal fasciculus and working memory in recent-onset schizophrenia. Biol. Psychiatry. 2008;63:512–518
  22. Kay SR, Fiszbein A, Opler LA. The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr. Bull. 1987;13:261–276
  23. Kaufman AS. Assessing Adolescent and Adult intelligence. Boston, USA: Allyn & Bacon; 1990;
  24. Kim JJ, Kwon JS, Park HJ, Youn T, Kang DH, Kim MS, et al. Functional disconnection between the prefrontal and parietal cortices during working memory processing in schizophrenia: a [15(O)]H2O PET study. Am. J. Psychiatry. 2003;160:919–923
  25. Lui S, Deng W, Huang X, Jiang L, Ma X, Chen H, et al. Association of cerebral deficits with clinical symptoms in antipsychotic-naive first-episode schizophrenia: an optimized voxel-based morphometry and resting state functional connectivity study. Am. J. Psychiatry. 2009;166:196–205
  26. Mathes B, Wood SJ, Proffitt TM, Stuart GW, Buchanan JA, Velakoulis D, et al. Early processing deficits in object working memory in first-episode schizophreniform psychosis and established schizophrenia. Psychol. Med. 2005;35:1053–1062
  27. McIntosh AM, Moorhead TW, Job D, Lymer GK, Munoz Maniega S, McKirdy J, et al. The effects of a neuregulin 1 variant on white matter density and integrity. Mol. Psychiatry. 2008;13:1054–1059
  28. Meyer-Lindenberg A, Poline JB, Kohn PD, Holt JL, Egan MF, Weinberger DR, et al. Evidence for abnormal cortical functional connectivity during working memory in schizophrenia. Am. J. Psychiatry. 2001;158:1809–1817
  29. Meyer-Lindenberg AS, Olsen RK, Kohn PD, Brown T, Egan MF, Weinberger DR, et al. Regionally specific disturbance of dorsolateral prefrontal–hippocampal functional connectivity in schizophrenia. Arch. Gen. Psychiatry. 2005;62:379–386
  30. Mitelman SA, Buchsbaum MS, Brickman AM, Shihabuddin L. Cortical intercorrelations of frontal area volumes in schizophrenia. Neuroimage. 2005;27:753–770
  31. Miyata J, Hirao K, Namiki C, Fujiwara H, Shimizu M, Fukuyama H, et al. Reduced white matter integrity correlated with cortico-subcortical gray matter deficits in schizophrenia. Schizophr. Res. 2009;111:78–85
  32. Nelson, H. and Willison, J., 1991. The Revised National Adult Reading Test (NART) Test Manual (2nd edn). Windsor:NFER: Nelson.
  33. Owen AM, Downes JJ, Sahakian BJ, Polkey CE, Robbins TW. Planning and spatial working memory following frontal lobe lesions in man. Neuropsychologia. 1990;28:1021–1034
  34. Pantelis C, Barnes TR, Nelson HE, Tanner S, Weatherley L, Owen AM, et al. Frontal–striatal cognitive deficits in patients with chronic schizophrenia. Brain. 1997;120(Pt 10):1823–1843
  35. Pantelis C, Maruff P. The cognitive neuropsychiatric approach to investigating the neurobiology of schizophrenia and other disorders. J. Psychosom. Res. 2002;53:655–664
  36. Pantelis C, Velakoulis D, McGorry PD, Wood SJ, Suckling J, Phillips LJ, et al. Neuroanatomical abnormalities before and after onset of psychosis: a cross-sectional and longitudinal MRI comparison. Lancet. 2003;361:281–288
  37. Pantelis C, Velakoulis D, Wood SJ, Yucel M, Yung AR, Phillips LJ, et al. Neuroimaging and emerging psychotic disorders: the Melbourne ultra-high risk studies. Int. Rev. Psychiatry. 2007;19:371–381
  38. Pantelis C, Yücel M, Wood SJ, Brewer WJ, Fornito A, Berger G, et al. Neurobiological endophenotypes of psychosis and schizophrenia: are there biological markers of illness onset?. In:  Jackson HJ,  McGorry PD editor. Recognition and Management of Early Psychosis: a Preventive Approach. Cambridge, UK: Cambridge University Press; 2009;
  39. Park S, Holzman PS. Schizophrenics show spatial working memory deficits. Arch. Gen. Psychiatry. 1992;49:975–982
  40. Paulus MP, Hozack NE, Zauscher BE, Frank L, Brown GG, McDowell J, et al. Parietal dysfunction is associated with increased outcome-related decision-making in schizophrenia patients. Biol. Psychiatry. 2002;51:995–1004
  41. Peters BD, de Haan L, Dekker N, Blaas J, Becker HE, Dingemans PM, et al. White matter fibertracking in first-episode schizophrenia, schizoaffective patients and subjects at ultra-high risk of psychosis. Neuropsychobiology. 2008;58:19–28
  42. Piskulic D, Olver JS, Norman TR, Maruff P. Behavioural studies of spatial working memory dysfunction in schizophrenia: a quantitative literature review. Psychiatry Res. 2007;150:111–121
  43. Ragland JD, Yoon J, Minzenberg MJ, Carter CS. Neuroimaging of cognitive disability in schizophrenia: search for a pathophysiological mechanism. Int. Rev. Psychiatry. 2007;19:417–427
  44. Reilly JL, Harris MS, Keshavan MS, Sweeney JA. Adverse effects of risperidone on spatial working memory in first-episode schizophrenia. Arch. Gen. Psychiatry. 2006;63:1189–1197
  45. Rissman J, Gazzaley A, DkEsposito M. Dynamic adjustments in prefrontal, hippocampal, and inferior temporal interactions with increasing visual working memory load. Cereb. Cortex. 2008;18:1618–1629
  46. Robbins TW, James M, Owen AM, Sahakian BJ, McInnes L, Rabbitt P. Cambridge Neuropsychological Test Automated Battery (CANTAB): a factor analytic study of a large sample of normal elderly volunteers. Dementia. 1994;5:266–281
  47. Sahakian BJ, Owen AM. Computerized assessment in neuropsychiatry using CANTAB: discussion paper. J. R. Soc. Med. 1992;85:399–402
  48. Schonell F. Backwardness in the Basic Subjects. London, UK: Oliver & Boyd; 1942;
  49. Seidman LJ, Giuliano AJ, Smith CW, Stone WS, Glatt SJ, Meyer E, et al. Neuropsychological functioning in adolescents and young adults at genetic risk for schizophrenia and affective psychoses: results from the Harvard and Hillside Adolescent High Risk Studies. Schizophr. Bull. 2006;32:507–524
  50. Seok JH, Park HJ, Chun JW, Lee SK, Cho HS, Kwon JS, et al. White matter abnormalities associated with auditory hallucinations in schizophrenia: a combined study of voxel-based analyses of diffusion tensor imaging and structural magnetic resonance imaging. Psychiatry Res. 2007;156:93–104
  51. Shapleske J, Rossell SL, Chitnis XA, Suckling J, Simmons A, Bullmore ET, et al. A computational morphometric MRI study of schizophrenia: effects of hallucinations. Cereb. Cortex. 2002;12:1331–1341
  52. Shaw P, Greenstein D, Lerch J, Clasen L, Lenroot R, Gogtay N, et al. Intellectual ability and cortical development in children and adolescents. Nature. 2006;440:676–679
  53. Shaw P, Kabani NJ, Lerch JP, Eckstrand K, Lenroot R, Gogtay N, et al. Neurodevelopmental trajectories of the human cerebral cortex. J. Neurosci. 2008;28:3586–3594
  54. Shenton ME, Dickey CC, Frumin M, McCarley RW. A review of MRI findings in schizophrenia. Schizophr. Res. 2001;49:1–52
  55. Smith CW, Park S, Cornblatt B. Spatial working memory deficits in adolescents at clinical high risk for schizophrenia. Schizophr. Res. 2006;81:211–215
  56. Spitzer RL, Williams JB, Gibbon M, First MB. The Structured Clinical Interview for DSM-III-R (SCID). I: history, rationale, and description. Arch. Gen. Psychiatry. 1992;49:624–629
  57. Spoletini I, Cherubini A, Di Paola M, Banfi G, Rusch N, Martinotti G, et al. Reduced fronto-temporal connectivity is associated with frontal gray matter density reduction and neuropsychological deficit in schizophrenia. Schizophr. Res. 2009;108:57–68
  58. Stephan KE, Baldeweg T, Friston KJ. Synaptic plasticity and dysconnection in schizophrenia. Biol. Psychiatry. 2006;59:929–939
  59. Suckling J, Bullmore E. Permutation tests for factorially designed neuroimaging experiments. Hum. Brain Mapp. 2004;22:193–205
  60. Suckling J, Davis MH, Ooi C, Wink AM, Fadili J, Salvador R, et al. Permutation testing of orthogonal factorial effects in a language-processing experiment using fMRI. Hum. Brain Mapp. 2006;27:425–433
  61. Sun D, Stuart GW, Jenkinson M, Wood SJ, McGorry PD, Velakoulis D, et al. Brain surface contraction mapped in first-episode schizophrenia: a longitudinal magnetic resonance imaging study. Mol. Psychiatry. 2008;July 8. PMID: 18607377. Electronic publication
  62. Tanskanen P, Ridler K, Murray GK, Haapea M, Veijola JM, Jaaskelainen E, et al. Morphometric brain abnormalities in schizophrenia in a population-based sample: relationship to duration of illness. Schizophr. Bull. 2008;Nov. 17. Electronic publication ahead of print
  63. Todd JJ, Marois R. Capacity limit of visual short-term memory in human posterior parietal cortex. Nature. 2004;428:751–754
  64. Walterfang M, McGuire PK, Yung AR, Phillips LJ, Velakoulis D, Wood SJ, et al. White matter volume changes in people who develop psychosis. Br. J. Psychiatry. 2008;193:210–215
  65. Walterfang M, Wood SJ, Velakoulis D, Pantelis C. Neuropathological, neurogenetic and neuroimaging evidence for white matter pathology in schizophrenia. Neurosci. Biobehav. Rev. 2006;30:918–948
  66. Wechsler D. A Manual for the Wechsler Adult Intelligence Scale—Revised. New York, USA: Psychological Corporation; 1981;
  67. Whitford TJ, Farrow TF, Gomes L, Brennan J, Harris AW, Williams LM. Grey matter deficits and symptom profile in first episode schizophrenia. Psychiatry Res. 2005;139:229–238
  68. Whitford TJ, Grieve SM, Farrow TF, Gomes L, Brennan J, Harris AW, et al. Progressive grey matter atrophy over the first 2–3years of illness in first-episode schizophrenia: a tensor-based morphometry study. Neuroimage. 2006;32:511–519
  69. Wolf RC, Hose A, Frasch K, Walter H, Vasic N. Volumetric abnormalities associated with cognitive deficits in patients with schizophrenia. Eur. Psychiatry. 2008;23:541–548
  70. Wood SJ, Pantelis C, Proffitt T, Phillips LJ, Stuart GW, Buchanan JA, et al. Spatial working memory ability is a marker of risk-for-psychosis. Psychol. Med. 2003;33:1239–1247
  71. Woods SW. Chlorpromazine equivalent doses for the newer atypical antipsychotics. J. Clin. Psychiatry. 2003;64:663–667
  72. Yoshihara Y, Sugihara G, Matsumoto H, Suckling J, Nishimura K, Toyoda T, et al. Voxel-based structural magnetic resonance imaging (MRI) study of patients with early onset schizophrenia. Ann. Gen. Psychiatry. 2008;7:25
  73. Zhou SY, Suzuki M, Takahashi T, Hagino H, Kawasaki Y, Matsui M, et al. Parietal lobe volume deficits in schizophrenia spectrum disorders. Schizophr. Res. 2007;89:35–48
  74. Zimmer HD. Visual and spatial working memory: from boxes to networks. Neurosci. Biobehav. Rev. 2008;32:1373–1395

PII: S0920-9964(09)00428-9

doi: 10.1016/j.schres.2009.09.009

Schizophrenia Research
Volume 115, Issue 2 , Pages 163-172 , December 2009

Article Tools

* Image Usage & Resolution