Brain Structure and Function

, Volume 220, Issue 1, pp 407–418 | Cite as

Not on speaking terms: hallucinations and structural network disconnectivity in schizophrenia

  • Branislava Ćurčić-Blake
  • Luca Nanetti
  • Lisette van der Meer
  • Leonardo Cerliani
  • Remco Renken
  • Gerdina H. M. Pijnenborg
  • André Aleman
Original Article

Abstract

Auditory verbal hallucinations (AVH) in schizophrenia have previously been associated with functional deficiencies in language networks, specifically with functional disconnectivity in fronto-temporal connections in the left hemisphere and in interhemispheric connections between frontal regions. Here, we investigate whether AVH are accompanied by white matter abnormalities in tracts connecting the frontal, parietal and temporal lobes, also engaged during language tasks. We combined diffusion tensor imaging with tract-based spatial statistics and found white matter abnormalities in patients with schizophrenia as compared with healthy controls. The patients showed reduced fractional anisotropy bilaterally: in the anterior thalamic radiation (ATR), body of the corpus callosum (forceps minor), cingulum, temporal part of the superior longitudinal fasciculus (SLF) and a small area in the inferior fronto-occipital fasciculus (IFOF); and in the right hemisphere: in the visual cortex, forceps major, body of the corpus callosum (posterior parts) and inferior parietal cortex. Compared to patients without current hallucinations, patients with hallucinations revealed decreased fractional anisotropy in the left IFOF, uncinate fasciculus, arcuate fasciculus with SLF, corpus callosum (posterior parts–forceps major), cingulate, corticospinal tract and ATR. The severity of hallucinations correlated negatively with white matter integrity in tracts connecting the left frontal lobe with temporal regions (uncinate fasciculus, IFOF, cingulum, arcuate fasciculus anterior and long part and superior long fasciculus frontal part) and in interhemispheric connections (anterior corona radiata). These findings support the hypothesis that hallucinations in schizophrenia are accompanied by a complex pattern of white matter alterations that negatively affect the language, emotion and attention/perception networks.

Keywords

Hallucinations Anatomical connectivity Diffusion tensor imaging (DTI) Language network Thalamo-cortical connectivity Fronto-temporal connectivity 

Abbreviations

ACC

Anterior cingulate cortex

ACR

Anterior corona radiata

AF

Anterior fasciculus

ATR

Anterior thalamic radiation

AVH

Auditory verbal hallucinations

DTI

Diffusion tensor imaging

IFG

Inferior frontal gyrus

IFOF

Inferior fronto-occipital fasciculus

ILF

Inferior longitudinal fasciculus

FA

Fractional anisotropy

ROI

Region of interest

SLF

Superior longitudinal fasciculus

TBSS

Tract-based spatial statistics

TFCE

Threshold-free cluster enhancement

UF

Uncinate fasciculus

Notes

Acknowledgments

The authors thank G.R. Blake for his comments on earlier versions of the manuscript. We thank psychiatrists Dr. R. Bruggeman and Dr. H. Knegtering for their help with patient inclusion. Our thanks are due especially to A. de Vos and J. van der Velde for help with data sorting and to S. Chalavi for discussions on analysis. L. Cerliani is supported by an NWO MaGW Open competition grant (grant number 400-08-089) and by an NIHC grant (grant number 056-13-017). This research was supported by a EURYI Award from the European Science Foundation (No. 044035001) awarded to A.A.

Conflict of interest

The authors declare that they have no competing financial interests in relation to the work described.

Supplementary material

429_2013_663_MOESM1_ESM.xlsx (21 kb)
Supplementary material 1 (XLSX 21 kb)
429_2013_663_MOESM2_ESM.xlsx (17 kb)
Supplementary material 2 (XLSX 16 kb)

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Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Branislava Ćurčić-Blake
    • 1
  • Luca Nanetti
    • 1
  • Lisette van der Meer
    • 1
    • 2
    • 5
  • Leonardo Cerliani
    • 1
    • 3
  • Remco Renken
    • 1
  • Gerdina H. M. Pijnenborg
    • 1
    • 4
    • 6
  • André Aleman
    • 1
  1. 1.Department of Neuroscience, Neuroimaging Center (NIC)University Medical Center Groningen, University of GroningenGroningenThe Netherlands
  2. 2.Department of RehabilitationLentisZuidlarenThe Netherlands
  3. 3.Netherlands Institute for NeuroscienceRoyal Netherlands Academy of Arts and Sciences (KNAW)AmsterdamThe Netherlands
  4. 4.Department of Clinical Psychology & Experimental PsychopathalogyUniversity of GroningenGroningenThe Netherlands
  5. 5.Rob Giel Research Centrum University of Groningen, University Medical Center GroningenGroningenThe Netherlands
  6. 6.Department of Psychotic DisordersGGZ-DrentheAssenThe Netherlands

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