Progressive and interrelated functional and structural evidence of post-onset brain reduction in schizophrenia - PubMed (original) (raw)
Comparative Study
Progressive and interrelated functional and structural evidence of post-onset brain reduction in schizophrenia
Dean F Salisbury et al. Arch Gen Psychiatry. 2007 May.
Abstract
Context: Progressive brain abnormalities in schizophrenia remain controversial. Evidence of interrelated progressive functional impairment would buttress the case for structural progression. Mismatch negativity (MMN) is reduced in chronic but not first-hospitalized schizophrenia and may index progressive structural changes.
Objective: To determine whether MMN shows associations with underlying auditory cortex gray matter at first hospitalization and progressive reduction longitudinally.
Design: Cross-sectional (first hospitalization) and longitudinal (1.5-year follow-up).
Setting: A private psychiatric hospital.
Participants: Protocol entrance: MMN and magnetic resonance imaging at first hospitalization in 20 subjects with schizophrenia, 21 subjects with bipolar disorder with psychosis, and 32 control subjects. Longitudinal electrophysiologic testing: MMN in 16 subjects with schizophrenia, 17 subjects with bipolar disorder, and 20 control subjects. Longitudinal electrophysiologic testing and magnetic resonance imaging: MMN and magnetic resonance imaging in 11 subjects with schizophrenia, 13 subjects with bipolar disorder, and 13 control subjects. At each time point, reported samples were group matched for age, handedness, and parental socioeconomic status.
Interventions: Electrophysiologic testing and high-resolution structural magnetic resonance imaging.
Main outcome measures: Mismatch negativity amplitude and Heschl gyrus and planum temporale gray matter volumes.
Results: Initially, groups did not differ in MMN amplitude. Subjects with schizophrenia showed associations between MMN and Heschl gyrus (r=-0.52; P=.02) not present in the other groups. At longitudinal MMN testing, schizophrenia showed MMN reduction (P=.004). Only schizophrenia evinced longitudinal left hemisphere Heschl gyrus reduction (P=.003), highly correlated with MMN reduction (r=0.6; P=.04).
Conclusions: At first hospitalization for schizophrenia, MMN indexed left hemisphere Heschl gyrus gray matter volume, consistent with variable progression of pre-hospitalization cortical reduction. Longitudinally, the interrelated progressive reduction of functional and structural measures suggests progressive pathologic processes early in schizophrenia. An active process of progressive cortical reduction presents a potential therapeutic target. Mismatch negativity may be a simple, sensitive, and inexpensive index not only of this progressive pathologic process but also of successful intervention.
Figures
Figure 1
Venn diagram of the patient sample overlap among the 3 studies. FE indicates first-episode; MMN, mismatch negativity; MRI, magnetic resonance imaging; and T1, time 1.
Figure 2
Magnetic resonance imaging–defined regions of interest and correlations with mismatch negativity (MMN) at first hospitalization. A and B, Three-dimensional magnetic resonance imaging constructions of major subdivisions of the superior temporal plane. Heschl gyri (dark blue and dark green) mainly contain the primary auditory cortex. The planum temporale (light blue and yellow-green) contains secondary and tertiary auditory association cortices. The left side of the figure is the left hemisphere. Note the larger left hemisphere planum temporale. C, At first hospitalization, despite mean MMN amplitudes within the normal range, subjects with schizophrenia showed an abnormal relationship between MMN and underlying left hemisphere primary auditory cortex volumes, consistent with some degree of prehospitalization cortical volume reductions in some subjects with schizophrenia. HG indicates Heschl gyrus; colored lines, regression line.
Figure 3
At longitudinal retesting, subjects with schizophrenia, who showed normal mean mismatch negativity (MMN) initially, now show significant reduction in MMN. Control subjects and subjects with bipolar disorder showed essentially no change in MMN amplitude.
Figure 4
Relationship of mismatch negativity (MMN) amplitude reduction and left hemisphere primary auditory cortex gray matter volume loss. Whereas the subjects with bipolar disorder and control subjects cluster around 0 in both MMN amplitude change and gray matter change, those with schizophrenia are almost exclusively contained in the negative quadrant defined by MMN reduction and gray matter loss. HG indicates Heschl gyrus; colored lines, regression line.
Similar articles
- Progressive decrease of left Heschl gyrus and planum temporale gray matter volume in first-episode schizophrenia: a longitudinal magnetic resonance imaging study.
Kasai K, Shenton ME, Salisbury DF, Hirayasu Y, Onitsuka T, Spencer MH, Yurgelun-Todd DA, Kikinis R, Jolesz FA, McCarley RW. Kasai K, et al. Arch Gen Psychiatry. 2003 Aug;60(8):766-75. doi: 10.1001/archpsyc.60.8.766. Arch Gen Psychiatry. 2003. PMID: 12912760 Free PMC article. - Progressive gray matter reduction of the superior temporal gyrus during transition to psychosis.
Takahashi T, Wood SJ, Yung AR, Soulsby B, McGorry PD, Suzuki M, Kawasaki Y, Phillips LJ, Velakoulis D, Pantelis C. Takahashi T, et al. Arch Gen Psychiatry. 2009 Apr;66(4):366-76. doi: 10.1001/archgenpsychiatry.2009.12. Arch Gen Psychiatry. 2009. PMID: 19349306 Clinical Trial. - Planum temporale and Heschl gyrus volume reduction in schizophrenia: a magnetic resonance imaging study of first-episode patients.
Hirayasu Y, McCarley RW, Salisbury DF, Tanaka S, Kwon JS, Frumin M, Snyderman D, Yurgelun-Todd D, Kikinis R, Jolesz FA, Shenton ME. Hirayasu Y, et al. Arch Gen Psychiatry. 2000 Jul;57(7):692-9. doi: 10.1001/archpsyc.57.7.692. Arch Gen Psychiatry. 2000. PMID: 10891040 Free PMC article. - Progressive loss of cortical gray matter in schizophrenia: a meta-analysis and meta-regression of longitudinal MRI studies.
Vita A, De Peri L, Deste G, Sacchetti E. Vita A, et al. Transl Psychiatry. 2012 Nov 20;2(11):e190. doi: 10.1038/tp.2012.116. Transl Psychiatry. 2012. PMID: 23168990 Free PMC article. Review. - Auditory cortex asymmetry, altered minicolumn spacing and absence of ageing effects in schizophrenia.
Chance SA, Casanova MF, Switala AE, Crow TJ. Chance SA, et al. Brain. 2008 Dec;131(Pt 12):3178-92. doi: 10.1093/brain/awn211. Epub 2008 Sep 26. Brain. 2008. PMID: 18819990 Free PMC article. Review.
Cited by
- Auditory Cortex Thickness Is Associated With N100 Amplitude in Schizophrenia Spectrum Disorders.
Slapø NB, Nerland S, Nordbø Jørgensen K, Mørch-Johnsen L, Pettersen JH, Roelfs D, Parker N, Valstad M, Pentz A, Timpe CMF, Richard G, Beck D, Werner MCF, Lagerberg TV, Melle I, Agartz I, Westlye LT, Steen NE, Andreassen OA, Moberget T, Elvsåshagen T, Jönsson EG. Slapø NB, et al. Schizophr Bull Open. 2023 Jun 9;4(1):sgad015. doi: 10.1093/schizbullopen/sgad015. eCollection 2023 Jan 1. Schizophr Bull Open. 2023. PMID: 38812720 Free PMC article. - Identify Potential Causal Relationships Between Cortical Thickness, Mismatch Negativity, Neurocognition, and Psychosocial Functioning in Drug-Naïve First-Episode Psychosis Patients.
Li X, Wei W, Wang Q, Deng W, Li M, Ma X, Zeng J, Zhao L, Guo W, Hall MH, Li T. Li X, et al. Schizophr Bull. 2024 Jul 27;50(4):827-838. doi: 10.1093/schbul/sbae026. Schizophr Bull. 2024. PMID: 38635296 - Computational Synaptic Modeling of Pitch and Duration Mismatch Negativity in First-Episode Psychosis Reveals Selective Dysfunction of the N-Methyl-D-Aspartate Receptor.
López-Caballero F, Auksztulewicz R, Howard Z, Rosch RE, Todd J, Salisbury DF. López-Caballero F, et al. Clin EEG Neurosci. 2024 Mar 27:15500594241238294. doi: 10.1177/15500594241238294. Online ahead of print. Clin EEG Neurosci. 2024. PMID: 38533562 - A comparison of visual and acoustic mismatch negativity as potential biomarkers in schizophrenia.
Molnár H, Marosi C, Becske M, Békési E, Farkas K, Stefanics G, Czigler I, Csukly G. Molnár H, et al. Sci Rep. 2024 Jan 10;14(1):992. doi: 10.1038/s41598-023-49983-5. Sci Rep. 2024. PMID: 38200103 Free PMC article. - Correlation of motor-auditory cross-modal and auditory unimodal N1 and mismatch responses of schizophrenic patients and normal subjects: an MEG study.
Okazaki M, Yumoto M, Kaneko Y, Maruo K. Okazaki M, et al. Front Psychiatry. 2023 Oct 11;14:1217307. doi: 10.3389/fpsyt.2023.1217307. eCollection 2023. Front Psychiatry. 2023. PMID: 37886112 Free PMC article.
References
- Racenstein JM, Harrow M, Reed R, Martin E, Herbener E, Penn DL. The relationship between positive symptoms and instrumental work functioning in schizophrenia: a 10 year follow-up study. Schizophr Res. 2002;56:95–103. - PubMed
- Kraepelin E. Psychiatrie: Ein Lehrbuch fur Studirende und Aerzte. Leipzig, Germany: Verlag Von Johann Ambrosius Barth; 1899.
- Bleuler E. In: Dementia Praecox, or the Group of Schizophrenias. Zinkin J, translator. New York, NY: International Universities Press; 1911.
- O’Callaghan E, Sham P, Takei N, Glover G, Murray RM. Schizophrenia after prenatal exposure to 1957 A2 influenza epidemic. Lancet. 1991;337:1248–1250. - PubMed
- Machón RA, Mednick SA, Schlusinger F. Seasonality, birth complications and schizophrenia in a high risk sample. Br J Psychiatry. 1987;151:122–124. - PubMed
Publication types
MeSH terms
Grants and funding
- K05 MH 01110/MH/NIMH NIH HHS/United States
- R01 MH040799/MH/NIMH NIH HHS/United States
- K05 MH070047/MH/NIMH NIH HHS/United States
- R01 MH050740/MH/NIMH NIH HHS/United States
- R01 MH 50747/MH/NIMH NIH HHS/United States
- R01 MH050740-07/MH/NIMH NIH HHS/United States
- R01 MH 40799/MH/NIMH NIH HHS/United States
- R01 MH58704/MH/NIMH NIH HHS/United States
- R01 MH058704/MH/NIMH NIH HHS/United States
- K05 MH070047-01/MH/NIMH NIH HHS/United States
- R01 MH 052807/MH/NIMH NIH HHS/United States
- R01 MH058704-02/MH/NIMH NIH HHS/United States
- R01 MH052807/MH/NIMH NIH HHS/United States
- R01 MH040799-13/MH/NIMH NIH HHS/United States
- R01 MH052807-06/MH/NIMH NIH HHS/United States
LinkOut - more resources
Full Text Sources
Medical