Hostname: page-component-78c5997874-j824f Total loading time: 0 Render date: 2024-11-10T17:43:15.258Z Has data issue: false hasContentIssue false
  • English
  • Français

Correlation of reduced social communicational and interactional skills with regional grey matter volumes in schizophrenia patients

Published online by Cambridge University Press:  10 April 2017

Miho Ota ,
Junko Matsuo ,
Noriko Sato ,
Toshiya Teraishi ,
Hiroaki Hori ,
Kotaro Hattori ,
Yoko Kamio  and
Hiroshi Kunugi
Miho Ota*
Affiliation:
Department of Mental Disorder Research, National Center of Neurology and Psychiatry, National Institute of Neuroscience, Kodaira, Tokyo, Japan
Junko Matsuo
Affiliation:
Department of Mental Disorder Research, National Center of Neurology and Psychiatry, National Institute of Neuroscience, Kodaira, Tokyo, Japan
Noriko Sato
Affiliation:
Department of Radiology, National Center of Neurology and Psychiatry, Ogawa-Higashi, Kodaira, Tokyo, Japan
Toshiya Teraishi
Affiliation:
Department of Mental Disorder Research, National Center of Neurology and Psychiatry, National Institute of Neuroscience, Kodaira, Tokyo, Japan
Hiroaki Hori
Affiliation:
Department of Mental Disorder Research, National Center of Neurology and Psychiatry, National Institute of Neuroscience, Kodaira, Tokyo, Japan
Kotaro Hattori
Affiliation:
Department of Mental Disorder Research, National Center of Neurology and Psychiatry, National Institute of Neuroscience, Kodaira, Tokyo, Japan
Yoko Kamio
Affiliation:
Department of Child and Adolescent Mental Health, National Center of Neurology and Psychiatry, Kodaira, Tokyo, Japan
Hiroshi Kunugi
Affiliation:
Department of Mental Disorder Research, National Center of Neurology and Psychiatry, National Institute of Neuroscience, Kodaira, Tokyo, Japan
*
Dr. Miho Ota, Department of Mental Disorder Research, National Center of Neurology and Psychiatry, National Institute of Neuroscience, 4-1-1, Ogawa-Higashi, Kodaira, Tokyo 187-8502, Japan. Tel: +81 42 341 2712; Fax: +81 42 346 2094; E-mail: ota@ncnp.go.jp
Get access Rights & Permissions [Opens in a new window]

Abstract

Objective

Recent studies have detected similarities between autism spectrum disorder and schizophrenia. We investigated structural abnormalities associated with autistic-like traits in patients with schizophrenia by voxel-based morphometry.

Methods

Patients with schizophrenia and healthy subjects were evaluated by the adult version of the social responsiveness scale (SRS-A), which is sensitive to autistic traits and symptoms even under subthreshold conditions, and magnetic resonance imaging.

Results

There were significant decreases in the anterior cingulate cortex, bilateral hippocampi, cerebellums, and right insula of patients with schizophrenia, compared with healthy subjects. We found significant negative correlations of the social communication and interaction (SCI) score, a subscale of SRS-A, with grey matter volume in the left posterior superior temporal region of schizophrenia patients. When subscales of SCI were examined separately in schizophrenic patients, negative correlations were observed between the social cognition score and the volumes of the left posterior superior temporal region, and between social motivation and the posterior cingulate cortex.

Conclusion

We found significant negative correlation between the SCI score and the grey matter volume in the left posterior superior temporal region of schizophrenia patients. This area was the region affected in previous studies of autistic spectrum disorders. Further, this area was associated with the theory of mind. Schizophrenia patients not necessarily show the impairment of SCI, nor this correlated region was not always the point with schizophrenia-specific change. However, we reveal the relationship between the left posterior superior temporal gyrus and the severity of the SCI in schizophrenia by using with SRS-A.

Keywords

autistic behaviourmagnetic resonance imagingschizophreniasocial responsiveness scale for adultsvolumetry
Type
Original Articles
Information
Acta Neuropsychiatrica , Volume 29 , Issue 6 , December 2017 , pp. 374 - 381
Check for updates
Copyright
© Scandinavian College of Neuropsychopharmacology 2017 

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

1. Edwards, J, Jackson, HJ, Pattison, PE. Emotion recognition via facial expression and affective prosody in schizophrenia: a methodological review. Clin Psychol Rev 2002;22:789–832.CrossRefGoogle ScholarPubMed
2. Tremeau, F. A review of emotion deficits in schizophrenia. Dialog Clin Neurosci 2006;8:59–70.CrossRefGoogle ScholarPubMed
3. Ellison-Wright, I, Glahn, DC, Laird, AR, Thelen, SM, Bullmore, E. The anatomy of first-episode and chronic schizophrenia: an anatomical likelihood estimation meta-analysis. Am J Psychiatry 2008;165:1015–1023.CrossRefGoogle ScholarPubMed
4. Glahn, DC, Laird, AR, Ellison-Wright, I et al. Meta-analysis of gray matter anomalies in schizophrenia: application of anatomic likelihood estimation and network analysis. Biol Psychiatry 2008;64:774–781.CrossRefGoogle ScholarPubMed
5. Honea, R, Crow, TJ, Passingham, D, Mackay, CE. Regional deficits in brain volume in schizophrenia: a meta-analysis of voxel-based morphometry studies. Am J Psychiatry 2005;162:2233–2245.CrossRefGoogle ScholarPubMed
6. Kanaan, RA, Kim, JS, Kaufmann, WE, Pearlson, GD, Barker, GJ, McGuire, PK. Diffusion tensor imaging in schizophrenia. Biol Psychiatry 2005;58:921–929.CrossRefGoogle ScholarPubMed
7. Kubicki, M, McCarley, R, Westin, CF et al. A review of diffusion tensor imaging studies in schizophrenia. J Psychiatr Res 2007;41:15–30.CrossRefGoogle ScholarPubMed
8. Shenton, ME, Dickey, CC, Frumin, M, McCarley, RW. A review of MRI findings in schizophrenia. Schizophr Res 2001;49:1–52.CrossRefGoogle ScholarPubMed
9. Weissman, MM, Prusoff, BA, Thompson, WD, Harding, PS, Myers, JK. Social adjustment by self-report in a community sample and in psychiatric outpatients. J Nerv Ment Dis 1978;166:317–326.CrossRefGoogle Scholar
10. Lincoln, SH, Hooker, CI. Neural structure and social dysfunction in individuals at clinical high risk for psychosis. Psychiatry Res 2014;224:152–158.CrossRefGoogle ScholarPubMed
11. Baron-Cohen, S, Wheelwright, S, Skinner, R, Martin, J, Clubley, E. The autism spectrum quotient (AQ): evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. J Autism Dev Disord 2001;31:5–17.CrossRefGoogle ScholarPubMed
12. Sasamoto, A, Miyata, J, Hirao, K et al. Social impairment in schizophrenia revealed by autism-spectrum quotient correlated with gray matter reduction. Soc Neurosci 2011;6:548–558.CrossRefGoogle ScholarPubMed
13. American Psychiatric Association. DSM-V: diagnostic and statistical manual of mental disorders, 5th edn. Washington, DC: American Psychiatric Press, 2013.Google Scholar
14. Brugha, TS, McManus, S, Bankart, J et al. Epidemiology of autism spectrum disorders in adults in the community in England. Arch Gen Psychiatry 2011;68:459–465.CrossRefGoogle ScholarPubMed
15. Lugnegård, T, Hallerbäck, MU, Gillberg, C. Asperger syndrome and schizophrenia: overlap of self-reported autistic traits using the autism-spectrum quotient (AQ). Nord J Psychiatry 2015;69:268–274.CrossRefGoogle ScholarPubMed
16. Matsuo, J, Kamio, Y, Takahashi, H et al. Autistic-like traits in adult patients with mood disorders and schizophrenia. PLoS One 2015;10:e0122711.CrossRefGoogle ScholarPubMed
17. Rapin, I, Tuchman, RF. Autism: definition, neurobiology, screening, diagnosis. Pediatr Clin North Am 2008;55:1129–1146.CrossRefGoogle ScholarPubMed
18. Meyer, U, Feldon, J, Dammann, O. Schizophrenia and autism: both shared and disorder-specific pathogenesis via perinatal inflammation? Pediatr Res 2011;69:26R–33R.CrossRefGoogle ScholarPubMed
19. Fatemi, SH. Reelin glycoprotein: structure, biology and roles in health and disease. Mol Psychiatry 2005;10:251–257.CrossRefGoogle ScholarPubMed
20. Cheung, C, Yu, K, Fung, G et al. Autistic disorders and schizophrenia: related or remote? An anatomical likelihood estimation. PLoS One 2010;5:e12233.CrossRefGoogle ScholarPubMed
21. Constantino, JN, Todd, RD. Autistic traits in the general population: a twin study. Arch Gen Psychiatry 2003;60:524–530.CrossRefGoogle ScholarPubMed
22. Bölte, S. Brief report: the social responsiveness scale for adults (SRS-A): initial results in a German cohort. J Autism Dev Disord 2012;42:1998–1999.CrossRefGoogle Scholar
23. Otsubo, T, Tanaka, K, Koda, R, Shinoda, J, Sano, N, Tanaka, S. Reliability and validity of Japanese version of the Mini-International Neuropsychiatric Interview. Psychiatry Clin Neurosci 2005;59:517–526.CrossRefGoogle ScholarPubMed
24. Sheehan, DV., Lecrubier, Y, Sheehan, KH et al. The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry 1998;59:22–57.Google ScholarPubMed
25. Kay, SR, Opler, LA, Fiszbein, A. Positive and Negative Syndrome Scale (PANSS) manual. Schizophr Bull 1987;13:261–276.CrossRefGoogle Scholar
26. Inada, T, Inagaki, A. Psychotropic dose equivalence in Japan. Psychiatry Clin Neurosci 2015;69:440–447.CrossRefGoogle ScholarPubMed
27. Constantino, JN, Gruber, CP. Social Responsiveness Scale (SRS). Los Angeles, CA: Western Psychological Services, 2005.Google Scholar
28. Constantino, JN, Todd, RD. Intergenerational transmission of subthreshold autistic traits in the general population. Biol Psychiatry 2005;57:655–660.CrossRefGoogle ScholarPubMed
29. Takei, R, Matsuo, J, Takahashi, H, Uchiyama, T, Kunugi, H, Kamio, Y. Verification of the utility of the social responsiveness scale for adults in non-clinical and clinical adult populations in Japan. BMC Psychiatry 2014;14:302.CrossRefGoogle ScholarPubMed
30. Kamio, Y, Inada, N, Moriwaki, A et al. Quantitative autistic traits ascertained in a national survey of 22529 Japanese schoolchildren. Acta Psychiatr Scand 2013;128:45–53.CrossRefGoogle Scholar
31. Frazier, TW, Youngstrom, EA, Speer, L. Validation of proposed DSM-5 criteria for autism spectrum disorder. J Am Acad Child Adolesc Psychiatry 2012;51:28–40.CrossRefGoogle ScholarPubMed
32. Uljarević, M, Evans, DW, Alvares, GA, Whitehouse, AJ. Short report: relationship between restricted and repetitive behaviours in children with autism spectrum disorder and their parents. Mol Autism 2016;7:29.CrossRefGoogle ScholarPubMed
33. Ota, M, Sato, N, Ishikawa, M et al. Discrimination of female schizophrenia patients from healthy women using multiple structural brain measures obtained with voxel-based morphometry. Psychiatry Clin Neurosci 2012;6:611–617.CrossRefGoogle Scholar
34. Ota, M, Noda, T, Sato, N et al. Effect of electroconvulsive therapy on gray matter volume in major depressive disorder. J Affect Disord 2015;186:186–191.CrossRefGoogle ScholarPubMed
35. Ashburner, J, Friston, KJ. Unified segmentation. Neuroimage 2005;26:839–851.CrossRefGoogle ScholarPubMed
36. Ashburner, J. A fast diffeomorphic image registration algorithm. Neuroimage 2007;38:95–113.CrossRefGoogle ScholarPubMed
37. Boddaert, N, Chabane, N, Gervais, H et al. Superior temporal sulcus anatomical abnormalities in childhood autism: a voxel-based morphometry MRI study. Neuroimage 2004;23:364–369.CrossRefGoogle ScholarPubMed
38. Bohrn, IC, Altmann, U, Jacobs, AM. Looking at the brains behind figurative language – a quantitative meta-analysis of neuroimaging studies on metaphor, idiom, and irony processing. Neuropsychologia 2012;50:2669–2683.CrossRefGoogle Scholar
39. Frith, U. Mind blindness and the brain in autism. Neuron 2001;32:969–979.CrossRefGoogle ScholarPubMed
40. Frith, U, Frith, CD. Development and neurophysiology of mentalizing. Philos Trans R Soc London Ser B Biol Sci 2003;358:459–473.CrossRefGoogle ScholarPubMed
41. Barnea-Goraly, N, Lotspeich, LJ, Reiss, AL. Similar white matter aberrations in children with autism and their unaffected siblings: a diffusion tensor imaging study using tractbased spatial statistics. Arch Gen Psychiatry 2010;67:1052–1060.CrossRefGoogle ScholarPubMed
42. von dem Hagen, EA, Nummenmaa, L, Yu, R, Engell, AD, Ewbank, MP, Calder, AJ. Autism spectrum traits in the typical population predict structure and function in the posterior superior temporal sulcus. Cerebral Cortex 2011;21:493–500.CrossRefGoogle ScholarPubMed
43. Fujiwara, H, Hirao, K, Namiki, C et al. Anterior cingulate pathology and social cognition in schizophrenia: a study of gray matter, white matter and sulcal morphometry. Neuroimage 2007;36:1236–1245.CrossRefGoogle ScholarPubMed
44. Lee, W, Reeve, J, Xue, Y, Xiong, J. Neural differences between intrinsic reasons for doing versus extrinsic reasons for doing: an fMRI study. Neurosci Res 2012;73:68–72.CrossRefGoogle ScholarPubMed
45. Smith, BW, Mitchell, DG, Hardin, MG et al. Neural substrates of reward magnitude, probability, and risk during a wheel of fortune decision-making task. Neuroimage 2009;44:600–609.CrossRefGoogle ScholarPubMed
46. Geurts, HM, Ridderinkhof, KR, Scholte, HS. The relationship between grey-matter and ASD and ADHD traits in typical adults. J Autism Dev Disord 2013;43:1630–1641.CrossRefGoogle ScholarPubMed
47. Saito, Y, Suga, M, Tochigi, M et al. Neural correlate of autistic-like traits and a common allele in the oxytocin receptor gene. Soc Cogn Affect Neurosci 2014;9:1443–1450.CrossRefGoogle Scholar
48. Kosaka, H, Omori, M, Munesue, T et al. Smaller insula and inferior frontal volumes in young adults with pervasive developmental disorders. Neuroimage 2010;50:1357–1363.CrossRefGoogle ScholarPubMed
49. Watanabe, H, Nakamura, M, Ohno, T et al. Altered orbitofrontal sulcogyral patterns in adult males with high-functioning autism spectrum disorders. Soc Cog Affect Neurosci 2014;9:520–528.CrossRefGoogle ScholarPubMed
50. Koolschijn, PC, Geurts, HM, van der Leij, AR, Scholte, HS. Are autistic traits in the general population related to global and regional brain differences? J Autism Dev Disord 2015;45:2779–2791.CrossRefGoogle ScholarPubMed
51. Altamura, AC, Serati, M, Buoli, M. Is duration of illness really influencing outcome in major psychoses? Nord J Psychiatry 2015;69:403–417.CrossRefGoogle ScholarPubMed