Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-18T05:00:22.324Z Has data issue: false hasContentIssue false
  • English
  • Français

Altered brain gyrification in deficit and non-deficit schizophrenia

Published online by Cambridge University Press:  09 May 2018

Yoichiro Takayanagi ,
Daiki Sasabayashi ,
Tsutomu Takahashi ,
Yuko Komori ,
Atsushi Furuichi ,
Mikio Kido ,
Yumiko Nishikawa ,
Mihoko Nakamura ,
Kyo Noguchi  and
Michio Suzuki
Yoichiro Takayanagi*
Affiliation:
Department of Neuropsychiatry, University of Toyama Graduate School of Medicine and Pharmaceutical Sciences, Toyama, Japan
Daiki Sasabayashi
Affiliation:
Department of Neuropsychiatry, University of Toyama Graduate School of Medicine and Pharmaceutical Sciences, Toyama, Japan
Tsutomu Takahashi
Affiliation:
Department of Neuropsychiatry, University of Toyama Graduate School of Medicine and Pharmaceutical Sciences, Toyama, Japan
Yuko Komori
Affiliation:
Department of Neuropsychiatry, University of Toyama Graduate School of Medicine and Pharmaceutical Sciences, Toyama, Japan
Atsushi Furuichi
Affiliation:
Department of Neuropsychiatry, University of Toyama Graduate School of Medicine and Pharmaceutical Sciences, Toyama, Japan
Mikio Kido
Affiliation:
Department of Neuropsychiatry, University of Toyama Graduate School of Medicine and Pharmaceutical Sciences, Toyama, Japan
Yumiko Nishikawa
Affiliation:
Department of Neuropsychiatry, University of Toyama Graduate School of Medicine and Pharmaceutical Sciences, Toyama, Japan
Mihoko Nakamura
Affiliation:
Department of Neuropsychiatry, University of Toyama Graduate School of Medicine and Pharmaceutical Sciences, Toyama, Japan
Kyo Noguchi
Affiliation:
Department of Radiology, University of Toyama Graduate School of Medicine and Pharmaceutical Sciences, Toyama, Japan
Michio Suzuki
Affiliation:
Department of Neuropsychiatry, University of Toyama Graduate School of Medicine and Pharmaceutical Sciences, Toyama, Japan
*
Author for correspondence: Yoichiro Takayanagi, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Patients with the deficit form of schizophrenia (D-SZ) are characterized by severe primary negative symptoms and differ from patients with the non-deficit form of schizophrenia (ND-SZ) in several aspects. No study has measured brain gyrification, which is a potential marker of neurodevelopment, in D-SZ and ND-SZ.

Methods

We obtained magnetic resonance scans from 135 schizophrenia patients and 50 healthy controls. The proxy scale for deficit syndrome (PDS) was used for the classification of D-SZ and ND-SZ. The local gyrification index (LGI) of the entire cortex was measured using FreeSurfer. Thirty-seven D-SZ and 36 ND-SZ patients were included in the LGI analyses. We compared LGI across the groups.

Results

SZ patients exhibited hyper-gyral patterns in the bilateral dorsal medial prefrontal and ventromedial prefrontal cortices, bilateral anterior cingulate gyri and right lateral parietal/occipital cortices as compared with HCs. Although patients with D-SZ or ND-SZ had higher LGI in similar regions compared with HC, the hyper-gyral patterns were broader in ND-SZ. ND-SZ patients exhibited a significantly higher LGI in the left inferior parietal lobule relative to D-SZ patients. Duration of illness inversely associated with LGI in broad regions only among ND-SZ patients.

Conclusions

The common hyper-gyral patterns among D-SZ and ND-SZ suggest that D-SZ and ND-SZ may share neurodevelopmental abnormalities. The different degrees of cortical gyrification seen in the left parietal regions, and the distinct correlation between illness chronicity and LGI observed in the prefrontal and insular cortices may be related to the differences in the clinical manifestations among D-SZ and ND-SZ.

Keywords

Deficit schizophrenialocal gyrification indexmagnetic resonance imagingnegative symptomsneurodevelopmental disorder
Type
Original Articles
Information
Psychological Medicine , Volume 49 , Issue 4 , March 2019 , pp. 573 - 580
Copyright
Copyright © Cambridge University Press 2018 

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

Andreasen, NC and Olsen, S (1982) Negative v positive schizophrenia. Definition and validation. Archives of General Psychiatry 39, 789–794.10.1001/archpsyc.1982.04290070025006Google Scholar
Andreasen, NC, Flaum, M and Arndt, S (1992) The comprehensive assessment of symptoms and history (CASH). An instrument for assessing diagnosis and psychopathology. Archives of General Psychiatry 49, 615–623.10.1001/archpsyc.1992.01820080023004Google Scholar
Andrews-Hanna, JR, Smallwood, J and Spreng, RN (2014) The default network and self-generated thought: component processes, dynamic control, and clinical relevance. Annals of the New York Academy of Sciences 1316, 29–52.10.1111/nyas.12360Google Scholar
Armstrong, E et al. (1995) The ontogeny of human gyrification. Cerebral Cortex (New York, N.Y.: 1991) 5, 56–63.10.1093/cercor/5.1.56Google Scholar
Carpenter, WT Jr., Heinrichs, DW and Wagman, AM (1988) Deficit and nondeficit forms of schizophrenia: the concept. The American Journal of Psychiatry 145, 578–583.Google Scholar
Cascella, NG et al. (2008) Neuropsychological impairment in deficit vs. non-deficit schizophrenia. Journal of Psychiatric Research 42, 930–937.10.1016/j.jpsychires.2007.10.002Google Scholar
Cascella, NG et al. (2010) Gray-matter abnormalities in deficit schizophrenia. Schizophrenia Research 120, 63–70.10.1016/j.schres.2010.03.039Google Scholar
Cohen, AS and Docherty, NM (2004) Deficit versus negative syndrome in schizophrenia: prediction of attentional impairment. Schizophrenia Bulletin 30, 827–835.10.1093/oxfordjournals.schbul.a007135Google Scholar
Desikan, RS et al. (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage 31, 968–980.10.1016/j.neuroimage.2006.01.021Google Scholar
Falkai, P et al. (2007) Disturbed frontal gyrification within families affected with schizophrenia. Journal of Psychiatric Research 41, 805–813.10.1016/j.jpsychires.2006.07.018Google Scholar
Fervaha, G et al. (2016) Neurocognitive impairment in the deficit subtype of schizophrenia. European Archives of Psychiatry and Clinical Neuroscience 266, 397–407.10.1007/s00406-015-0629-6Google Scholar
Fischer, BA et al. (2012) Cortical structural abnormalities in deficit versus nondeficit schizophrenia. Schizophrenia Research 136, 51–54.10.1016/j.schres.2012.01.030Google Scholar
Fischl, B (2012) Freesurfer. NeuroImage 62, 774–781.10.1016/j.neuroimage.2012.01.021Google Scholar
Galderisi, S et al. (2008) Patterns of structural MRI abnormalities in deficit and nondeficit schizophrenia. Schizophrenia Bulletin 34, 393–401.10.1093/schbul/sbm097Google Scholar
Gautam, P et al. (2015) Cortical gyrification and its relationships with cortical volume, cortical thickness, and cognitive performance in healthy mid-life adults. Behavioural Brain Research 287, 331–339.10.1016/j.bbr.2015.03.018Google Scholar
Goetz, RR et al. (2007) Validity of a ‘proxy’ for the deficit syndrome derived from the positive and negative syndrome scale (PANSS). Schizophrenia Research 93, 169–177.10.1016/j.schres.2007.02.018Google Scholar
Hagler, DJ Jr., Saygin, AP and Sereno, MI (2006) Smoothing and cluster thresholding for cortical surface-based group analysis of fMRI data. NeuroImage 33, 1093–1103.10.1016/j.neuroimage.2006.07.036Google Scholar
Harris, JM et al. (2007) Increased prefrontal gyrification in a large high-risk cohort characterizes those who develop schizophrenia and reflects abnormal prefrontal development. Biological Psychiatry 62, 722–729.10.1016/j.biopsych.2006.11.027Google Scholar
Haukvik, UK et al. (2012) Cortical folding in Broca's area relates to obstetric complications in schizophrenia patients and healthy controls. Psychological Medicine 42, 1329–1337.10.1017/S0033291711002315Google Scholar
Honey, GD et al. (2005) Functional dysconnectivity in schizophrenia associated with attentional modulation of motor function. Brain 128, 2597–2611.10.1093/brain/awh632Google Scholar
Insel, TR (2010) Rethinking schizophrenia. Nature 468, 187–193.10.1038/nature09552Google Scholar
Kanaan, RA et al. (2005) Diffusion tensor imaging in schizophrenia. Biological Psychiatry 58, 921–929.10.1016/j.biopsych.2005.05.015Google Scholar
Keefe, RS, Eesley, CE and Poe, MP (2005) Defining a cognitive function decrement in schizophrenia. Biological Psychiatry 57, 688–691.10.1016/j.biopsych.2005.01.003Google Scholar
Keefe, RS et al. (1996) Clinical characteristics of kraepelinian schizophrenia: replication and extension of previous findings. The American Journal of Psychiatry 153, 806–811.Google Scholar
Kirkpatrick, B et al. (1989) The schedule for the deficit syndrome: an instrument for research in schizophrenia. Psychiatry Research 30, 119–123.10.1016/0165-1781(89)90153-4Google Scholar
Kirkpatrick, B et al. (1993) Case identification and stability of the deficit syndrome of schizophrenia. Psychiatry Research 47, 47–56.10.1016/0165-1781(93)90054-KGoogle Scholar
Kirkpatrick, B et al. (2001) A separate disease within the syndrome of schizophrenia. Archives of General Psychiatry 58, 165–171.10.1001/archpsyc.58.2.165Google Scholar
Kochunov, P et al. (2005) Age-related morphology trends of cortical sulci. Human Brain Mapping 26, 210–220.10.1002/hbm.20198Google Scholar
Kremen, WS et al. (1995) The ‘3 Rs’ and neuropsychological function in schizophrenia: a test of the matching fallacy in biological relatives. Psychiatry Research 56, 135–143.10.1016/0165-1781(94)02652-1Google Scholar
Lawrie, SM et al. (2002) Reduced frontotemporal functional connectivity in schizophrenia associated with auditory hallucinations. Biological Psychiatry 51, 1008–1011.10.1016/S0006-3223(02)01316-1Google Scholar
Lee, JS et al. (2015) Neural basis of anhedonia and amotivation in patients with schizophrenia: the role of reward system. Current Neuropharmacology 13, 750–759.10.2174/1570159X13666150612230333Google Scholar
Messias, E et al. (2004) Summer birth and deficit schizophrenia: a pooled analysis from 6 countries. Archives of General Psychiatry 61, 985–989.10.1001/archpsyc.61.10.985Google Scholar
Nakamura, M et al. (2007) Altered orbitofrontal sulcogyral pattern in schizophrenia. Brain: A Journal of Neurology 130, 693–707.Google Scholar
Nanda, P et al. (2014) Local gyrification index in probands with psychotic disorders and their first-degree relatives. Biological Psychiatry 76, 447–455.Google Scholar
Narr, KL et al. (2004) Abnormal gyral complexity in first-episode schizophrenia. Biological Psychiatry 55, 859–867.10.1016/j.biopsych.2003.12.027Google Scholar
Nesvag, R et al. (2014) Reduced brain cortical folding in schizophrenia revealed in two independent samples. Schizophrenia Research 152, 333–338.10.1016/j.schres.2013.11.032Google Scholar
Nishikawa, Y et al. (2016) Orbitofrontal sulcogyral pattern and olfactory sulcus depth in the schizophrenia spectrum. European Archives of Psychiatry and Clinical Neuroscience 266, 15–23.Google Scholar
Palaniyappan, L et al. (2011) Folding of the prefrontal cortex in schizophrenia: regional differences in gyrification. Biological Psychiatry 69, 974–979.Google Scholar
Palaniyappan, L et al. (2013) Gyrification of Broca's region is anomalously lateralized at onset of schizophrenia in adolescence and regresses at 2 year follow-up. Schizophrenia Research 147, 39–45.Google Scholar
Quarantelli, M et al. (2002) Stereotaxy-based regional brain volumetry applied to segmented MRI: validation and results in deficit and nondeficit schizophrenia. NeuroImage 17, 373–384.Google Scholar
Rhoades, HM and Overall, JE (1988) The semistructured BPRS interview and rating guide. Psychopharmacology Bulletin 24, 101–104.Google Scholar
Roy, MA et al. (2001) Male gender is associated with deficit schizophrenia: a meta-analysis. Schizophrenia Research 47, 141–147.Google Scholar
Sasabayashi, D et al. (2017) Increased frontal gyrification negatively correlates with executive function in patients with first-episode schizophrenia. Cerebral Cortex (New York, N.Y.: 1991) 27(4), 2686–2694.Google Scholar
Schaer, M et al. (2008) A surface-based approach to quantify local cortical gyrification. IEEE Transactions on Medical Imaging 27, 161–170.10.1109/TMI.2007.903576Google Scholar
Schneider, K (1959) Clinical Psychopathology, 5th Edn. New York: Grune and Stratton.Google Scholar
Schultz, CC et al. (2010) Increased parahippocampal and lingual gyrification in first-episode schizophrenia. Schizophrenia Research 123, 137–144.10.1016/j.schres.2010.08.033Google Scholar
Shaffer, JJ et al. (2015) Neural correlates of schizophrenia negative symptoms: distinct subtypes impact dissociable brain circuits. Molecular Neuropsychiatry 1, 191–200.Google Scholar
Strauss, GP et al. (2010) Periods of recovery in deficit syndrome schizophrenia: a 20-year multi-follow-up longitudinal study. Schizophrenia Bulletin 36, 788–799.Google Scholar
Subotnik, KL et al. (1998) Prediction of the deficit syndrome from initial deficit symptoms in the early course of schizophrenia. Psychiatry Research 80, 53–59.Google Scholar
Takayanagi, M et al. (2013) Reduced anterior cingulate gray matter volume and thickness in subjects with deficit schizophrenia. Schizophrenia Research 150, 484–490.Google Scholar
Tallinen, T et al. (2014) Gyrification from constrained cortical expansion. Proceedings of the National Academy of Sciences of the United States of America 111, 12667–12672.10.1073/pnas.1406015111Google Scholar
Tek, C, Kirkpatrick, B and Buchanan, RW (2001) A five-year follow up study of deficit and nondeficit schizophrenia. Schizophrenia Research 49, 253–260.Google Scholar
Tepest, R et al. (2013) Morphometry of structural disconnectivity indicators in subjects at risk and in age-matched patients with schizophrenia. European Archives of Psychiatry and Clinical Neuroscience 263, 15–24.Google Scholar
Toro, R and Burnod, Y (2005) A morphogenetic model for the development of cortical convolutions. Cerebral Cortex 15, 1900–1913.10.1093/cercor/bhi068Google Scholar
Torrey, EF (2007) Schizophrenia and the inferior parietal lobule. Schizophrenia Research 97, 215–225.Google Scholar
Vogeley, K et al. (2000) Disturbed gyrification of the prefrontal region in male schizophrenic patients: a morphometric postmortem study. The American Journal of Psychiatry 157, 34–39.Google Scholar
Voineskos, AN et al. (2013) Neuroimaging evidence for the deficit subtype of schizophrenia. JAMA Psychiatry 70, 472–480.10.1001/jamapsychiatry.2013.786Google Scholar
Weinberger, DR (1987) Implications of normal brain development for the pathogenesis of schizophrenia. Archives of General Psychiatry 44, 660–669.Google Scholar
Wheeler, AL et al. (2015) Further neuroimaging evidence for the deficit subtype of schizophrenia: a cortical connectomics analysis. JAMA Psychiatry 72, 446–455.10.1001/jamapsychiatry.2014.3020Google Scholar
World Health Organization (1993) The ICD-10 Classification of Mental and Behavioral Disorders: Diagnostic Criteria for Research. Geneva, Switzerland: World Health Organization.Google Scholar
Zilles, K et al. (1988) The human pattern of gyrification in the cerebral cortex. Anatomy and Embryology 179, 173–179.10.1007/BF00304699Google Scholar
Zilles, K, Palomero-Gallagher, N and Amunts, K (2013) Development of cortical folding during evolution and ontogeny. Trends in Neurosciences 36, 275–284.Google Scholar
Supplementary material: File

Takayanagi et al. supplementary material

Takayanagi et al. supplementary material 1

Download Takayanagi et al. supplementary material(File)
File 1.2 MB