Schizophrenia Research
Volume 122, Issue 1 , Pages 72-80 , September 2010

Neural markers of remission in first-episode schizophrenia: A volumetric neuroimaging study of the hippocampus and amygdala

  • Michael Bodnar

      Affiliations

    • Brain Imaging Group, Douglas Mental Health University Institute, Montreal, Canada
    • Prevention and Early Intervention Program for Psychoses (PEPP-Montreal), Douglas Mental Health University Institute, Montreal, Canada
  • ,
  • Ashok K. Malla

      Affiliations

    • Prevention and Early Intervention Program for Psychoses (PEPP-Montreal), Douglas Mental Health University Institute, Montreal, Canada
  • ,
  • Yvonne Czechowska

      Affiliations

    • Prevention and Early Intervention Program for Psychoses (PEPP-Montreal), Douglas Mental Health University Institute, Montreal, Canada
  • ,
  • Audrey Benoit

      Affiliations

    • Brain Imaging Group, Douglas Mental Health University Institute, Montreal, Canada
    • Prevention and Early Intervention Program for Psychoses (PEPP-Montreal), Douglas Mental Health University Institute, Montreal, Canada
  • ,
  • Ferid Fathalli

      Affiliations

    • Brain Imaging Group, Douglas Mental Health University Institute, Montreal, Canada
  • ,
  • Ridha Joober

      Affiliations

    • Brain Imaging Group, Douglas Mental Health University Institute, Montreal, Canada
    • Prevention and Early Intervention Program for Psychoses (PEPP-Montreal), Douglas Mental Health University Institute, Montreal, Canada
  • ,
  • Marita Pruessner

      Affiliations

    • Prevention and Early Intervention Program for Psychoses (PEPP-Montreal), Douglas Mental Health University Institute, Montreal, Canada
  • ,
  • Jens Pruessner

      Affiliations

    • Brain Imaging Group, Douglas Mental Health University Institute, Montreal, Canada
  • ,
  • Martin Lepage

      Affiliations

    • Brain Imaging Group, Douglas Mental Health University Institute, Montreal, Canada
    • Prevention and Early Intervention Program for Psychoses (PEPP-Montreal), Douglas Mental Health University Institute, Montreal, Canada
    • Corresponding Author InformationCorresponding author. Douglas Mental Health University Institute, Frank B Common Pavilion, F1143, 6875 LaSalle Blvd., Verdun, Quebec, Canada H4H 1R3. Tel.: +1 514 761 6131x4393; fax: +1 514 888 4064.

Received 8 March 2010 ,Revised 11 June 2010 ,Accepted 18 June 2010.

References 

  1. Andreasen NC, Carpenter WT, Kane JM, Lasser RA, Marder SR, Weinberger DR. Remission in schizophrenia: proposed criteria and rationale for consensus. Am. J. Psychiatry. 2005;162:441–449
  2. Barbas H, Blatt GJ. Topographically specific hippocampal projections target functionally distinct prefrontal areas in the rhesus monkey. Hippocampus. 1995;5:511–533
  3. Becker T, Elmer K, Schneider F, Schneider M, Grodd W, Bartels M, et al. Confirmation of reduced temporal limbic structure volume on magnetic resonance imaging in male patients with schizophrenia. Psychiatry Res. 1996;67:135–143
  4. Binder JR, Desai RH, Graves WW, Conant LL. Where is the semantic system? A critical review and meta-analysis of 120 functional neuroimaging studies. Cereb Cortex. 2009;19:2767–2796
  5. Bodnar, M., Harvey, P.-O., Malla, A., Joober, R., Lepage, M., in press. The parahippocampal gyrus as a neural marker of early remission in first episode psychosis: a voxel-based morphometry study. Clin Schizophr Related Psychosis.
  6. Cassidy CM, Norman R, Manchanda R, Schmitz N, Malla A. Testing Definitions of Symptom Remission in First-Episode Psychosis for Prediction of Functional Outcome at 2Years. Schizophr Bull. 2010;36:1001–1008
  7. Collins DL, Neelin P, Peters TM, Evans AC. Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J. Comput. Assist. Tomogr. 1994;18:192–205
  8. DeLisi LE, Sakuma M, Tew W, Kushner M, Hoff AL, Grimson R. Schizophrenia as a chronic active brain process: a study of progressive brain structural change subsequent to the onset of schizophrenia. Psychiatry Res. 1997;74:129–140
  9. Duvernoy HM. The Human Hippocampus: Functional Anatomy, Vascularization, and Serial Sections with MRI., Ed. Berlin: Springer Verlag; 2005;
  10. Emsley R, Chiliza B, Schoeman R. Predictors of long-term outcome in schizophrenia. Curr. Opin. Psychiatry. 2008;21:173–177
  11. First MB, Spitzer RL, Gibbon M, Williams JBW. Structured Clinical Interview for DSM-IV Axis I Disorders, Patient Edition (SCID-I/P & SCID-I/NP), Version 2, Ed. New York: New York Psychiatric Institute, Biometrics Research; 1998;
  12. Fitzsimmons J, Kubicki M, Smith K, Bushell G, Estepar RS, Westin CF, et al. Diffusion tractography of the fornix in schizophrenia. Schizophr. Res. 2009;107:39–46
  13. Goldman-Rakic PS, Selemon LD, Schwartz ML. Dual pathways connecting the dorsolateral prefrontal cortex with the hippocampal formation and parahippocampal cortex in the rhesus monkey. Neuroscience. 1984;12:719–743
  14. Gothelf D, Soreni N, Nachman RP, Tyano S, Hiss Y, Reiner O, et al. Evidence for the involvement of the hippocampus in the pathophysiology of schizophrenia. Eur. Neuropsychopharmacol. 2000;10:389–395
  15. Green MF. What are the functional consequences of neurocognitive deficits in schizophrenia?. Am. J. Psychiatry. 1996;153:321–330
  16. Hackert VH, den Heijer T, Oudkerk M, Koudstaal PJ, Hofman A, Breteler MM. Hippocampal head size associated with verbal memory performance in nondemented elderly. Neuroimage. 2002;17:1365–1372
  17. Harrison G, Hopper K, Craig T, Laska E, Siegel C, Wanderling J, et al. Recovery from psychotic illness: a 15- and 25-year international follow-up study. Br. J. Psychiatry. 2001;178:506–517
  18. Harrison PJ. The hippocampus in schizophrenia: a review of the neuropathological evidence and its pathophysiological implications. Psychopharmacology (Berl). 2004;174:151–162
  19. Harrison PJ, Weinberger DR. Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol. Psychiatry. 2005;10:40–68
  20. Helldin L, Kane JM, Karilampi U, Norlander T, Archer T. Remission and cognitive ability in a cohort of patients with schizophrenia. J. Psychiatr. Res. 2006;40:738–745
  21. Hirayasu Y, Shenton ME, Salisbury DF, Dickey CC, Fischer IA, Mazzoni P, et al. Lower left temporal lobe MRI volumes in patients with first-episode schizophrenia compared with psychotic patients with first-episode affective disorder and normal subjects. Am. J. Psychiatry. 1998;155:1384–1391
  22. Ho BC, Andreasen NC, Nopoulos P, Arndt S, Magnotta V, Flaum M. Progressive structural brain abnormalities and their relationship to clinical outcome: a longitudinal magnetic resonance imaging study early in schizophrenia. Arch. Gen. Psychiatry. 2003;60:585–594
  23. Hollingshead A. Two-Factor Index of Social Position, Ed. New Haven, CN: Yale University Press; 1965;
  24. Honey G, Bullmore E. Human pharmacological MRI. Trends Pharmacol. Sci. 2004;25:366–374
  25. Hubbard KB, Hepler JR. Cell signalling diversity of the Gqalpha family of heterotrimeric G proteins. Cell. Signal. 2006;18:135–150
  26. In:  Jensen B,  Regier LD editor. Drug Comparison Charts. seventh ed.. RxFiles Academic Detailing Program, Saskatoon, Saskatchewan. 2010;
  27. Kalus P, Buri C, Slotboom J, Gralla J, Remonda L, Dierks T, et al. Volumetry and diffusion tensor imaging of hippocampal subregions in schizophrenia. NeuroReport. 2004;15:867–871
  28. Karlsgodt KH, Niendam TA, Bearden CE, Cannon TD. White matter integrity and prediction of social and role functioning in subjects at ultra-high risk for psychosis. Biol. Psychiatry. 2009;66:562–569
  29. Kay S, Fiszbein A, Opler L. The positive and negative synfrome scale (PANSS) for schizophrenia. Schizophr. Bull. 1987;13:261–276
  30. Konrad C, Ukas T, Nebel C, Arolt V, Toga AW, Narr KL. Defining the human hippocampus in cerebral magnetic resonance images—an overview of current segmentation protocols. Neuroimage. 2009;47:1185–1195
  31. Lieberman J, Chakos M, Wu H, Alvir J, Hoffman E, Robinson D, et al. Longitudinal study of brain morphology in first episode schizophrenia. Biol. Psychiatry. 2001;49:487–499
  32. Malla A, Norman R, McLean T, Scholten D, Townsend L. A Canadian programme for early intervention in non-affective psychotic disorders. Aust. N. Z. J. Psychiatry. 2003;37:407–413
  33. Moncrieff J, Leo J. A systematic review of the effects of antipsychotic drugs on brain volume. Psychol. Med. 2010;1–14
  34. Moser MB, Moser EI. Functional differentiation in the hippocampus. Hippocampus. 1998;8:608–619
  35. Narr KL, Thompson PM, Szeszko P, Robinson D, Jang S, Woods RP, et al. Regional specificity of hippocampal volume reductions in first-episode schizophrenia. Neuroimage. 2004;21:1563–1575
  36. Nesvaderani M, Matsumoto I, Sivagnanasundaram S. Anterior hippocampus in schizophrenia pathogenesis: molecular evidence from a proteome study. Aust. N. Z. J. Psychiatry. 2009;43:310–322
  37. O'Driscoll GA, Florencio PS, Gagnon D, Wolff AV, Benkelfat C, Mikula L, et al. Amygdala–hippocampal volume and verbal memory in first-degree relatives of schizophrenic patients. Psychiatry Res. 2001;107:75–85
  38. Oldfield RC. The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia. 1971;9:97–113
  39. Pajonk FG, Wobrock T, Gruber O, Scherk H, Berner D, Kaizl I, et al. Hippocampal plasticity in response to exercise in schizophrenia. Arch. Gen. Psychiatry. 2010;67:133–143
  40. Pruessner JC, Li LM, Serles W, Pruessner M, Collins DL, Kabani N, et al. Volumetry of hippocampus and amygdala with high-resolution MRI and three-dimensional analysis software: minimizing the discrepancies between laboratories. Cereb. Cortex. 2000;10:433–442
  41. Rajarethinam R, DeQuardo JR, Miedler J, Arndt S, Kirbat R, Brunberg JA, et al. Hippocampus and amygdala in schizophrenia: assessment of the relationship of neuroanatomy to psychopathology. Psychiatry Res. 2001;108:79–87
  42. Rametti G, Segarra N, Junque C, Bargallo N, Caldu X, Ibarretxe N, et al. Left posterior hippocampal density reduction using VBM and stereological MRI procedures in schizophrenia. Schizophr. Res. 2007;96:62–71
  43. Rametti G, Junque C, Falcon C, Bargallo N, Catalan R, Penades R, et al. A voxel-based diffusion tensor imaging study of temporal white matter in patients with schizophrenia. Psychiatry Res. 2009;171:166–176
  44. Robinson DG, Woerner MG, McMeniman M, Mendelowitz A, Bilder RM. Symptomatic and functional recovery from a first episode of schizophrenia or schizoaffective disorder. Am. J. Psychiatry. 2004;161:473–479
  45. Schmidt-Wilcke T, Poljansky S, Hierlmeier S, Hausner J, Ibach B. Memory performance correlates with gray matter density in the ento-/perirhinal cortex and posterior hippocampus in patients with mild cognitive impairment and healthy controls—a voxel based morphometry study. Neuroimage. 2009;47:1914–1920
  46. Schmitt A, Steyskal C, Bernstein HG, Schneider-Axmann T, Parlapani E, Schaeffer EL, et al. Stereologic investigation of the posterior part of the hippocampus in schizophrenia. Acta Neuropathol. 2009;117:395–407
  47. Sled JG, Zijdenbos AP, Evans AC. A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans. Med. Imaging. 1998;17:87–97
  48. Steen RG, Mull C, McClure R, Hamer RM, Lieberman JA. Brain volume in first-episode schizophrenia: systematic review and meta-analysis of magnetic resonance imaging studies. Br. J. Psychiatry. 2006;188:510–518
  49. Stein EA. fMRI: a new tool for the in vivo localization of drug actions in the brain. J. Anal. Toxicol. 2001;25:419–424
  50. Szeszko PR, Strous RD, Goldman RS, Ashtari M, Knuth KH, Lieberman JA, et al. Neuropsychological correlates of hippocampal volumes in patients experiencing a first episode of schizophrenia. Am. J. Psychiatry. 2002;159:217–226
  51. Szeszko PR, Goldberg E, Gunduz-Bruce H, Ashtari M, Robinson D, Malhotra AK, et al. Smaller anterior hippocampal formation volume in antipsychotic-naive patients with first-episode schizophrenia. Am. J. Psychiatry. 2003;160:2190–2197
  52. Takei K, Yamasue H, Abe O, Yamada H, Inoue H, Suga M, et al. Disrupted integrity of the fornix is associated with impaired memory organization in schizophrenia. Schizophr. Res. 2008;103:52–61
  53. Talairach J, Tournoux P. Co-Planar Stereotaxic Atlas of the Human Brain, Ed. New York: Thieme; 1988;
  54. Talamini LM, Meeter M, Elvevag B, Murre JM, Goldberg TE. Reduced parahippocampal connectivity produces schizophrenia-like memory deficits in simulated neural circuits with reduced parahippocampal connectivity. Arch. Gen. Psychiatry. 2005;62:485–493
  55. Toulopoulou T, Murray RM. Verbal memory deficit in patients with schizophrenia: an important future target for treatment. Expert Rev. Neurother. 2004;4:43–52
  56. Vawter MP, Ferran E, Galke B, Cooper K, Bunney WE, Byerley W. Microarray screening of lymphocyte gene expression differences in a multiplex schizophrenia pedigree. Schizophr. Res. 2004;67:41–52
  57. Velakoulis D, Wood SJ, Wong MT, McGorry PD, Yung A, Phillips L, et al. Hippocampal and amygdala volumes according to psychosis stage and diagnosis: a magnetic resonance imaging study of chronic schizophrenia, first-episode psychosis, and ultra-high-risk individuals. Arch. Gen. Psychiatry. 2006;63:139–149
  58. Verma S, Sitoh YY, Ho YC, Poon LY, Subramaniam M, Chan YH, et al. Hippocampal volumes in first-episode psychosis. J. Neuropsychiatry Clin. Neurosci. 2009;21:24–29
  59. Vita A, de Peri L. Hippocampal and amygdala volume reductions in first-episode schizophrenia. Br. J. Psychiatry. 2007;190:271
  60. Vita A, De Peri L, Silenzi C, Dieci M. Brain morphology in first-episode schizophrenia: a meta-analysis of quantitative magnetic resonance imaging studies. Schizophr. Res. 2006;82:75–88
  61. Witter MP, Wouterlood FG, Naber PA, Van Haeften T. Anatomical organization of the parahippocampal–hippocampal network. In:  W. Scharfman HE,  M.P., Schwarcz R editor. The Parahippocampal Region, Implications for Neurological and Psychiatric Diseases. New York: Annals of the New York Academy of Sciences; 2000;p. 1–24
  62. Witthaus H, Mendes U, Brune M, Ozgurdal S, Bohner G, Gudlowski Y, et al. Hippocampal subdivision and amygdalar volumes in patients in an at-risk mental state for schizophrenia. J. Psychiatry Neurosci. 2010;35:33–40
  63. Wobrock T, Gruber O, Schneider-Axmann T, Wolwer W, Gaebel W, Riesbeck M, et al. Internal capsule size associated with outcome in first-episode schizophrenia. Eur. Arch. Psychiatry Clin. Neurosci. 2009;259:278–283
  64. Woods SW. Chlorpromazine equivalent doses for the newer atypical antipsychotics. J. Clin. Psychiatry. 2003;64:663–667
  65. Zhou Y, Shu N, Liu Y, Song M, Hao Y, Liu H, et al. Altered resting-state functional connectivity and anatomical connectivity of hippocampus in schizophrenia. Schizophr. Res. 2008;100:120–132

PII: S0920-9964(10)01370-8

doi: 10.1016/j.schres.2010.06.013

Schizophrenia Research
Volume 122, Issue 1 , Pages 72-80 , September 2010