Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-17T05:18:21.581Z Has data issue: false hasContentIssue false
  • English
  • Français

Structural alterations of the superior temporal gyrus in schizophrenia: Detailed subregional differences

Published online by Cambridge University Press:  23 March 2020

K. Ohi ,
Y. Matsuda ,
T. Shimada ,
T. Yasuyama ,
K. Oshima ,
K. Sawai ,
H. Kihara ,
Y. Nitta ,
H. Okubo  and
T. Uehara
...Show all authors
K. Ohi*
Affiliation:
Department of Neuropsychiatry, Kanazawa Medical University, Ishikawa, Japan
Y. Matsuda*
Affiliation:
Department of Neuropsychiatry, Kanazawa Medical University, Ishikawa, Japan Project Research Center, Kanazawa Medical University, Ishikawa, Japan
T. Shimada
Affiliation:
Department of Neuropsychiatry, Kanazawa Medical University, Ishikawa, Japan
T. Yasuyama
Affiliation:
Department of Neuropsychiatry, Kanazawa Medical University, Ishikawa, Japan
K. Oshima
Affiliation:
Department of Neuropsychiatry, Kanazawa Medical University, Ishikawa, Japan
K. Sawai
Affiliation:
Department of Neuropsychiatry, Kanazawa Medical University, Ishikawa, Japan
H. Kihara
Affiliation:
Department of Neuropsychiatry, Kanazawa Medical University, Ishikawa, Japan
Y. Nitta
Affiliation:
Department of Neuropsychiatry, Kanazawa Medical University, Ishikawa, Japan
H. Okubo
Affiliation:
Department of Neuropsychiatry, Kanazawa Medical University, Ishikawa, Japan
T. Uehara
Affiliation:
Department of Neuropsychiatry, Kanazawa Medical University, Ishikawa, Japan
Y. Kawasaki
Affiliation:
Department of Neuropsychiatry, Kanazawa Medical University, Ishikawa, Japan
*
* Corresponding author. Department of Neuropsychiatry, Kanazawa Medical University, 1-1 Daigaku, Uchinada, Ishikawa, 920-0293, Japan. Tel.: +81 76 286 2211; fax: +81 76 286 3341. E-mail address:[email protected] (K. Ohi), E-mail address:[email protected] (Y. Matsuda).
* Corresponding author. Department of Neuropsychiatry, Kanazawa Medical University, 1-1 Daigaku, Uchinada, Ishikawa, 920-0293, Japan. Tel.: +81 76 286 2211; fax: +81 76 286 3341. E-mail address:[email protected] (K. Ohi), E-mail address:[email protected] (Y. Matsuda).
Get access

Abstract

Background

Reduced gray matter volumes in the superior temporal gyrus (STG) have been reported in patients with schizophrenia. Such volumetric abnormalities might denote alterations in cortical thickness, surface area, local gyrification or all of these factors. The STG can be anatomically divided into five subregions using automatic parcellation in FreeSurfer: lateral aspect of the STG, anterior transverse temporal gyrus of Heschl gyrus (HG), planum polare (PP) of the STG, planum temporale (PT) of the STG and transverse temporal sulcus.

Methods

We acquired magnetic resonance imaging (MRI) 3T scans from 40 age- and sex-matched patients with schizophrenia and 40 healthy subjects, and the scans were automatically processed using FreeSurfer. General linear models were used to assess group differences in regional volumes and detailed thickness, surface area and local gyrification.

Results

As expected, patients with schizophrenia had significantly smaller bilateral STG volumes than healthy subjects. Of the five subregions in the STG, patients with schizophrenia showed significantly and marginally reduced volumes in the lateral aspect of the STG and PT of the STG bilaterally compared with healthy subjects. The volumetric alteration in bilateral lateral STG was derived from both the cortical thickness and surface area but not local gyrification. There was no significant laterality of the alteration in the lateral STG between patients and controls and no correlation among the structures and clinical characteristics.

Conclusions

These findings suggest that of five anatomical subregions in the STG, the lateral STG is one of the most meaningful regions for brain pathophysiology in schizophrenia.

Keywords

MRI, magnetic resonance imagingROI, region of interestSE, standard errorSTG, superior temporal gyrusPT, planum temporaleHG, Heschl’s gyrusPP, planum polareSchizophreniaSuperior temporal gyrusVolumeThicknessSurface area
Type
Original article
Information
European Psychiatry , Volume 35 , May 2016 , pp. 25 - 31
Copyright
Copyright © European Psychiatry 2016

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

Ward, KEFriedman, LWise, ASchulz, SCMeta-analysis of brain and cranial size in schizophrenia. Schizophr Res 1996; 22: 197–213CrossRefGoogle Scholar
Wright, ICRabe-Hesketh, SWoodruff, PWDavid, ASMurray, RMBullmore, ETMeta-analysis of regional brain volumes in schizophrenia. Am J Psychiatry 2000; 157: 16–25CrossRefGoogle Scholar
Glahn, DCLaird, AREllison-Wright, IThelen, SMRobinson, JLLancaster, JLet al.Meta-analysis of gray matter anomalies in schizophrenia: application of anatomic likelihood estimation and network analysis. Biol Psychiatry 2008; 64: 774–781CrossRefGoogle ScholarPubMed
Honea, RCrow, TJPassingham, DMackay, CERegional deficits in brain volume in schizophrenia: a meta-analysis of voxel-based morphometry studies. Am J Psychiatry 2005; 162: 2233–2245CrossRefGoogle ScholarPubMed
Hirayasu, YMcCarley, RWSalisbury, DFTanaka, SKwon, JSFrumin, Met al.Planum temporale and Heschl gyrus volume reduction in schizophrenia: a magnetic resonance imaging study of first-episode patients. Arch Gen Psychiatry 2000; 57: 692–699CrossRefGoogle ScholarPubMed
Kasai, KShenton, MESalisbury, DFHirayasu, YLee, CUCiszewski, AAet al.Progressive decrease of left superior temporal gyrus gray matter volume in patients with first-episode schizophrenia. Am J Psychiatry 2003; 160: 156–164CrossRefGoogle ScholarPubMed
Shenton, MEDickey, CCFrumin, MMcCarley, RWA review of MRI findings in schizophrenia. Schizophr Res 2001; 49: 1–52CrossRefGoogle Scholar
Sun, JMaller, JJGuo, LFitzgerald, PBSuperior temporal gyrus volume change in schizophrenia: a review on region of interest volumetric studies. Brain Res Rev 2009; 61: 14–32CrossRefGoogle ScholarPubMed
Takahashi, TSuzuki, MZhou, SYTanino, RNakamura, KKawasaki, Yet al.A follow-up MRI study of the superior temporal subregions in schizotypal disorder and first-episode schizophrenia. Schizophr Res 2010; 119: 65–74CrossRefGoogle ScholarPubMed
Vita, ADe Peri, LDeste, GSacchetti, EProgressive loss of cortical gray matter in schizophrenia: a meta-analysis and meta-regression of longitudinal MRI studies. Transl Psychiatry 2 2012 e190CrossRefGoogle ScholarPubMed
Pantelis, CVelakoulis, DMcGorry, PDWood, SJSuckling, JPhillips, LJet al.Neuroanatomical abnormalities before and after onset of psychosis: a cross-sectional and longitudinal MRI comparison. Lancet 2003; 361: 281–288CrossRefGoogle ScholarPubMed
Takahashi, TWood, SJYung, ARWalterfang, MPhillips, LJSoulsby, Bet al.Superior temporal gyrus volume in antipsychotic-naive people at risk of psychosis. Br J Psychiatry 2010; 196: 206–211CrossRefGoogle ScholarPubMed
Takahashi, TWood, SJYung, ARSoulsby, BMcGorry, PDSuzuki, Met al.Progressive gray matter reduction of the superior temporal gyrus during transition to psychosis. Arch Gen Psychiatry 2009; 66: 366–376CrossRefGoogle ScholarPubMed
Thompson, PMVidal, CGiedd, JNGochman, PBlumenthal, JNicolson, Ret al.Mapping adolescent brain change reveals dynamic wave of accelerated gray matter loss in very early-onset schizophrenia. Proc Natl Acad Sci U S A 2001; 98: 11650–11655CrossRefGoogle ScholarPubMed
Goldman, ALPezawas, LMattay, VSFischl, BVerchinski, BAChen, Qet al.Widespread reductions of cortical thickness in schizophrenia and spectrum disorders and evidence of heritability. Arch Gen Psychiatry 2009; 66: 467–477CrossRefGoogle ScholarPubMed
Rimol, LMNesvag, RHagler, D.J. Jr.Bergmann, OFennema-Notestine, CHartberg, CBet al.Cortical volume, surface area, and thickness in schizophrenia and bipolar disorder. Biol Psychiatry 2012; 71: 552–560CrossRefGoogle ScholarPubMed
Nesvag, RSchaer, MHaukvik, UKWestlye, LTRimol, LMLange, EHet al.Reduced brain cortical folding in schizophrenia revealed in two independent samples. Schizophr Res 2014; 152: 333–338CrossRefGoogle ScholarPubMed
Palaniyappan, LLiddle, PFAberrant cortical gyrification in schizophrenia: a surface-based morphometry study. J Psychiatry Neurosci 2012; 37: 399–406CrossRefGoogle ScholarPubMed
Ratnanather, JTPoynton, CBPisano, DVCrocker, BPostell, ECebron, Set al.Morphometry of superior temporal gyrus and planum temporale in schizophrenia and psychotic bipolar disorder. Schizophr Res 2013; 150: 476–483CrossRefGoogle ScholarPubMed
Pearlson, GDSuperior temporal gyrus and planum temporale in schizophrenia: a selective review. Prog Neuropsychopharmacol Biol Psychiatry 1997; 21: 1203–1229CrossRefGoogle ScholarPubMed
Kim, JJCrespo-Facorro, BAndreasen, NCO’Leary, DSMagnotta, VNopoulos, PMorphology of the lateral superior temporal gyrus in neuroleptic naive patients with schizophrenia: relationship to symptoms. Schizophr Res 2003; 60: 173–181Google Scholar
Kasai, KShenton, MESalisbury, DFHirayasu, YOnitsuka, TSpencer, MHet al.Progressive decrease of left Heschl gyrus and planum temporale gray matter volume in first-episode schizophrenia: a longitudinal magnetic resonance imaging study. Arch Gen Psychiatry 2003; 60: 766–775CrossRefGoogle ScholarPubMed
Allen, PLaroi, FMcGuire, PKAleman, AThe hallucinating brain: a review of structural and functional neuroimaging studies of hallucinations. Neurosci Biobehav Rev 2008; 32: 175–191CrossRefGoogle ScholarPubMed
Moseley, PFernyhough, CEllison, AAuditory verbal hallucinations as atypical inner speech monitoring, and the potential of neurostimulation as a treatment option. Neurosci Biobehav Rev 2013; 37: 2794–2805CrossRefGoogle ScholarPubMed
Hirayasu, YShenton, MESalisbury, DFDickey, CCFischer, IAMazzoni, Pet 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: 1384–1391CrossRefGoogle ScholarPubMed
Keshavan, MSHaas, GLKahn, CEAguilar, EDick, ELSchooler, NRet al.Superior temporal gyrus and the course of early schizophrenia: progressive, static, or reversible?. J Psychiatr Res 1998; 32: 161–167CrossRefGoogle ScholarPubMed
Takahashi, TSuzuki, MTanino, RZhou, SYHagino, HNiu, Let al.Volume reduction of the left planum temporale gray matter associated with long duration of untreated psychosis in schizophrenia: a preliminary report. Psychiatry Res 2007; 154: 209–219CrossRefGoogle ScholarPubMed
Destrieux, CFischl, BDale, AHalgren, EAutomatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature. Neuroimage 2010; 53: 1–15CrossRefGoogle ScholarPubMed
Segonne, FDale, AMBusa, EGlessner, MSalat, DHahn, HKet al.A hybrid approach to the skull stripping problem in MRI. Neuroimage 2004; 22: 1060–1075CrossRefGoogle ScholarPubMed
Fischl, BSalat, DHBusa, EAlbert, MDieterich, MHaselgrove, Cet al.Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 2002; 33: 341–355CrossRefGoogle ScholarPubMed
Fischl, BSalat, DHvan der Kouwe, AJMakris, NSegonne, FQuinn, BTet al.Sequence-independent segmentation of magnetic resonance images. Neuroimage 2004; 23(Suppl. 1):S69–S84CrossRefGoogle ScholarPubMed
Sled, JGZijdenbos, APEvans, ACA nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 1998; 17: 87–97CrossRefGoogle ScholarPubMed
Fischl, BLiu, ADale, AMAutomated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Trans Med Imaging 2001; 20: 70–80CrossRefGoogle ScholarPubMed
Segonne, FPacheco, JFischl, BGeometrically accurate topology-correction of cortical surfaces using nonseparating loops. IEEE Trans Med Imaging 2007; 26: 518–529CrossRefGoogle ScholarPubMed
Dale, AMFischl, BSereno, MICortical surface-based analysis. I. Segmentation and surface reconstruction. Neuroimage 1999; 9: 179–194CrossRefGoogle ScholarPubMed
Dale, AMSereno, MIImproved localizadon of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: a linear approach. J Cogn Neurosci 1993; 5: 162–176CrossRefGoogle ScholarPubMed
Fischl, BDale, AMMeasuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci U S A 2000; 97: 11050–11055CrossRefGoogle ScholarPubMed
Fischl, BSereno, MIDale, AMCortical surface-based analysis. II: inflation, flattening, and a surface-based coordinate system. Neuroimage 1999; 9: 195–207CrossRefGoogle Scholar
Shapleske, JRossell, SLWoodruff, PWDavid, ASThe planum temporale: a systematic, quantitative review of its structural, functional and clinical significance. Brain Res Brain Res Rev 1999; 29: 26–49CrossRefGoogle ScholarPubMed
Schaer, MCuadra, MBTamarit, LLazeyras, FEliez, SThiran, JPA surface-based approach to quantify local cortical gyrification. IEEE Trans Med Imaging 2008; 27: 161–170CrossRefGoogle ScholarPubMed
Zilles, KQu, MSchleicher, ALuhmann, HJCharacterization of neuronal migration disorders in neocortical structures: quantitative receptor autoradiography of ionotropic glutamate. GABA(A) and GABA(B) receptors. Eur J Neurosci 1998; 10: 3095–3106CrossRefGoogle ScholarPubMed
Borgwardt, SJRiecher-Rossler, ADazzan, PChitnis, XAston, JDrewe, Met al.Regional gray matter volume abnormalities in the at risk mental state. Biol Psychiatry 2007; 61: 1148–1156CrossRefGoogle ScholarPubMed
Takahashi, TWood, SJKawasaki, YSuzuki, MVelakoulis, DPantelis, CLack of progressive gray matter reduction of the superior temporal subregions in chronic schizophrenia. Schizophr Res 2010; 117: 101–102CrossRefGoogle ScholarPubMed
Rajarethinam, RSahni, SRosenberg, DRKeshavan, MSReduced superior temporal gyrus volume in young offspring of patients with schizophrenia. Am J Psychiatry 2004; 161: 1121–1124CrossRefGoogle ScholarPubMed
Hedman, AMvan Haren, NEvan Baal, GCBrouwer, RMBrans, RGSchnack, HGet al.Heritability of cortical thickness changes over time in twin pairs discordant for schizophrenia. Schizophr Res 2015. http://dx.doi.org/10.1016/j.schres.2015.06.021 [Epub ahead of print].Google Scholar
Liao, JYan, HLiu, QYan, JZhang, LJiang, Set al.Reduced paralimbic system gray matter volume in schizophrenia: correlations with clinical variables, symptomatology and cognitive function. J Psychiatr Res 2015; 65: 80–86CrossRefGoogle ScholarPubMed
Zierhut, KCSchulte-Kemna, AKaufmann, JSteiner, JBogerts, BSchiltz, KDistinct structural alterations independently contributing to working memory deficits and symptomatology in paranoid schizophrenia. Cortex 2013; 49: 1063–1072CrossRefGoogle ScholarPubMed
van Tol, MJvan der Meer, LBruggeman, RModinos, GKnegtering, HAleman, AVoxel-based gray and white matter morphometry correlates of hallucinations in schizophrenia: the superior temporal gyrus does not stand alone. Neuroimage Clin 2013; 4: 249–257CrossRefGoogle Scholar
Chou, PHKoike, SNishimura, YSatomura, YKinoshita, ATakizawa, Ret al.Similar age-related decline in cortical activity over frontotemporal regions in schizophrenia: a multichannel near-infrared spectroscopy study. Schizophr Bull 2015; 41: 268–279CrossRefGoogle ScholarPubMed
Kubota, MMiyata, JYoshida, HHirao, KFujiwara, HKawada, Ret al.Age-related cortical thinning in schizophrenia. Schizophr Res 2011; 125: 21–29CrossRefGoogle Scholar
Kleinschmidt, AFalkai, PHuang, YSchneider, TFurst, GSteinmetz, HIn vivo morphometry of planum temporale asymmetry in first-episode schizophrenia. Schizophr Res 1994; 12: 9–18CrossRefGoogle ScholarPubMed
Kulynych, JJVladar, KFantie, BDJones, DWWeinberger, DRNormal asymmetry of the planum temporale in patients with schizophrenia. Three-dimensional cortical morphometry with MRI. Br J Psychiatry 1995; 166: 742–749CrossRefGoogle ScholarPubMed
Chou, PHKoike, SNishimura, YKawasaki, SSatomura, YKinoshita, Aet al.Distinct effects of duration of untreated psychosis on brain cortical activities in different treatment phases of schizophrenia: a multi-channel near-infrared spectroscopy study. Prog Neuropsychopharmacol Biol Psychiatry 2014; 49: 63–69CrossRefGoogle ScholarPubMed
Lesh, TATanase, CGeib, BRNiendam, TAYoon, JHMinzenberg, MJet al.A multimodal analysis of antipsychotic effects on brain structure and function in first-episode schizophrenia. JAMA Psychiatry 2015; 72: 226–234CrossRefGoogle ScholarPubMed
Lieberman, JATollefson, GDCharles, CZipursky, RSharma, TKahn, RSet al.Antipsychotic drug effects on brain morphology in first-episode psychosis. Arch Gen Psychiatry 2005; 62: 361–370CrossRefGoogle ScholarPubMed
Submit a response

Comments

No Comments have been published for this article.