Background
Functional neuroimaging supports the hypothesis that auditory verbal hallucinations
(AVH) in schizophrenia result from altered functional connectivity between perisylvian
language regions, although the extent to which AVH are also associated with an altered
tract anatomy is less clear.
Methods
Twenty-eight patients with schizophrenia subdivided into 17 subjects with a history
of AVH and 11 without a history of hallucinations and 59 age- and IQ-matched healthy
controls were recruited. The number of streamlines, fractional anisotropy (FA), and
mean diffusivity were measured along the length of the arcuate fasciculus and its
medial and lateral components.
Results
Patients with schizophrenia had bilateral reduction of FA relative to controls in
the arcuate fasciculi (p < .001). Virtual dissection of the subcomponents of the arcuate fasciculi revealed
that these reductions were specific to connections between posterior temporal and
anterior regions in the inferior frontal and parietal lobe. Also, compared with controls,
the reduction in FA of these tracts was highest, and bilateral, in patients with AVH,
but in patients without AVH, this reduction was reported only on the left.
Conclusions
These findings point toward a supraregional network model of AVH in schizophrenia.
They support the hypothesis that there may be selective vulnerability of specific
anatomical connections to posterior temporal regions in schizophrenia and that extensive
bilateral damage is associated with a greater vulnerability to AVH. If confirmed by
further studies, these findings may advance our understanding of the anatomical factors
that are protective against AVH and predictive of a treatment response.
Key Words
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References
- Grundrisse der Psychiatrie.Thieme, Leipzig, Germany1906
- Dementia praecox. E. and S. Livingstone, Edinburgh1919
- Schizophrenia: a disconnection syndrome?.Clin Neurosci. 1995; 3: 89-97
- Synaptic plasticity and dysconnection in schizophrenia.Biol Psychiatry. 2006; 59: 929-939
- Abnormal monitoring of inner speech: a physiological basis for auditory hallucinations.Lancet. 1995; 346: 596-600
- Increased superior temporal activation associated with external misattributions of self-generated speech in schizophrenia.Schizophr Res. 2008; 100: 361-363
- Modulation of activity in temporal cortex during generation of inner speech.Hum Brain Mapp. 2002; 16: 219-227
- Reduced frontotemporal functional connectivity in schizophrenia associated with auditory hallucinations.Biol Psychiatry. 2002; 51: 1008-1011
- Functional anatomy of auditory verbal imagery in schizophrenic patients with auditory hallucinations.Am J Psychiatry. 2000; 157: 1691-1693
- Reduced communication between frontal and temporal lobes during talking in schizophrenia.Biol Psychiatry. 2002; 51: 485-492
- Inner speech models of auditory verbal hallucinations: evidence from behavioural and neuroimaging studies.Int Rev Psychiatry. 2007; 19: 407-415
- The functional anatomy of auditory hallucinations in schizophrenia.Psychiatry Res. 2000; 100: 13-20
- Increased blood flow in Broca's area during auditory hallucinations in schizophrenia.Lancet. 1993; 342: 703-706
- Mapping auditory hallucinations in schizophrenia using functional magnetic resonance imaging.Arch Gen Psychiatry. 2000; 57: 1033-1038
- Perisylvian language networks of the human brain.Ann Neurol. 2005; 57: 8-16
- Symmetries in human brain language pathways correlate with verbal recall.Proc Natl Acad Sci USA. 2007; 104: 17163-17168
- A review of diffusion tensor imaging studies in schizophrenia.J Psychiatr Res. 2007; 41: 15-30
- Diffusion MRI in psychiatric disorders.in: Jones D.K. Diffusion MRI. Oxford University Press, Oxford, United Kingdom2010
- MRI white matter diffusion anisotropy and PET metabolic rate in schizophrenia.Neuroreport. 1998; 9: 425-430
- Structural disconnectivity in schizophrenia: a diffusion tensor magnetic resonance imaging study.Br J Psychiatry. 2003; 182: 439-443
- Pathways that make voices: white matter changes in auditory hallucinations.Arch Gen Psychiatry. 2004; 61: 658-668
- DTI and MTR abnormalities in schizophrenia: analysis of white matter integrity.Neuroimage. 2005; 26: 1109-1118
- A diffusion tensor imaging study of fasciculi in schizophrenia.Am J Psychiatry. 2007; 164: 467-473
- Abnormal brain white matter in schizophrenia: a diffusion tensor imaging study.Neuroreport. 2001; 12: 2251-2254
- Compromised white matter tract integrity in schizophrenia inferred from diffusion tensor imaging.Arch Gen Psychiatry. 1999; 56: 367-374
- Diffusion tensor imaging of frontal lobe white matter tracts in schizophrenia.Ann Gen Psychiatry. 2006; 5: 19
- Investigating regional white matter in schizophrenia using diffusion tensor imaging.Neuroreport. 2002; 13: 333-336
- Tract-specific anisotropy measurements in diffusion tensor imaging.Psychiatry Res. 2006; 146: 73-82
- Diffusion tensor magnetic resonance imaging tractography in cognitive disorders.Curr Opin Neurol. 2006; 19: 599-606
- A diffusion tensor magnetic resonance imaging study of frontal cortex connections in very-late-onset schizophrenia-like psychosis.Am J Geriatr Psychiatry. 2005; 13: 1092-1099
- Age effects on diffusion tensor magnetic resonance imaging tractography measures of frontal cortex connections in schizophrenia.Hum Brain Mapp. 2006; 27: 230-238
- Altered connections on the road to psychopathy.Mol Psychiatry. 2009; 14: 946-953
- White matter tractography in bipolar disorder and schizophrenia.Biol Psychiatry. 2008; 64: 1088-1092
Voineskos AN, Lobaugh NJ, Bouix S, Rajji TK, Miranda D, Kennedy JL, et al. Diffusion tensor tractography findings in schizophrenia across the adult lifespan. Brain 133:1494–1504.
- Corpus callosum abnormalities and their association with psychotic symptoms in patients with schizophrenia.Biol Psychiatry. 2010; 68: 70-77
- National Adult Reading Test (NART): Test Manual.2nd ed. Nfer-Nelson, Windsor, Berkshire, United Kingdom1991
- Diagnostic and Statistical Manual of Mental Disorders.4th ed. American Psychiatic Association, Washington, DC1994
- Negative v positive schizophrenia.Arch Gen Psychiatry. 1982; 39: 789-794
- Isotropic resolution diffusion tensor imaging with whole brain acquisition in a clinically acceptable time.Hum Brain Mapp. 2002; 15: 216-230
- MR diffusion tensor spectroscopy and imaging.Biophys J. 1994; 66: 259-267
- Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI.J Magn Reson B. 1996; 111: 209-219
- In vivo fiber tractography using DT-MRI data.Magn Reson Med. 2000; 44: 625-632
- Virtual in vivo interactive dissection of white matter fasciculi in the human brain.Neuroimage. 2002; 17: 77-94
- Spatial normalization and averaging of diffusion tensor MRI data sets.Neuroimage. 2002; 17: 592-617
- Atlasing location, asymmetry and inter-subject variability of white matter tracts in the human brain with MR diffusion tractography.Neuroimage. 2011; 54: 49-59
- A diffusion tensor imaging tractography atlas for virtual in vivo dissections.Cortex. 2008; 44: 1105-1132
- Regional deficits in brain volume in schizophrenia: a meta-analysis of voxel-based morphometry studies.Am J Psychiatry. 2005; 162: 2233-2245
- Anatomically related grey and white matter abnormalities in adolescent-onset schizophrenia.Brain. 2007; 130: 2375-2386
- Chronic schizophrenia as a brain misconnection syndrome: a white matter voxel-based morphometry study.Schizophr Res. 2003; 64: 15-23
- Neural synchrony indexes disordered perception and cognition in schizophrenia.Proc Natl Acad Sci USA. 2004; 101: 17288-17293
- “Gamma synchrony” in first-episode schizophrenia: a disorder of temporal connectivity?.Am J Psychiatry. 2005; 162: 459-465
- The dysplastic net hypothesis: an integration of developmental and dysconnectivity theories of schizophrenia.Schizophr Res. 1997; 28: 143-156
- Engagement of brain areas implicated in processing inner speech in people with auditory hallucinations.Br J Psychiatry. 2003; 182: 525-531
- Regionally specific disturbance of dorsolateral prefrontal-hippocampal functional connectivity in schizophrenia.Arch Gen Psychiatry. 2005; 62: 379-386
- Aberrant “default mode” functional connectivity in schizophrenia.Am J Psychiatry. 2007; 164: 450-457
- Morphology of the lateral superior temporal gyrus in neuroleptic nai;ve patients with schizophrenia: relationship to symptoms.Schizophr Res. 2003; 60: 173-181
- Brain activation in discourse comprehension: a 3T fMRI study.Neuroimage. 2008; 41: 614-622
- Modulation of the semantic system by word imageability.Neuroimage. 2005; 27: 188-200
- Memory retrieval and the parietal cortex: a review of evidence from a dual-process perspective.Neuropsychologia. 2008; 46: 1787-1799
- What is the relationship between phonological short-term memory and speech processing?.Trends Cogn Sci. 2006; 10: 480-486
- White matter changes in schizophrenia: evidence for myelin-related dysfunction.Arch Gen Psychiatry. 2003; 60: 443-456
- Maldistribution of interstitial neurons in prefrontal white matter of the brains of schizophrenic patients.Arch Gen Psychiatry. 1996; 53: 425-436
- The neuropsychiatry of adult-onset adrenoleukodystrophy.J Neuropsychiatry Clin Neurosci. 1999; 11: 315-327
- Diffusion tensor brain MR imaging in X-linked cerebral adrenoleukodystrophy.Neurology. 2001; 56: 544-547
- Diffusion tensor imaging in cases of adrenoleukodystrophy: preliminary experience as a marker for early demyelination?.Am J Neuroradiol. 2003; 24: 819-824
- Disruption of white matter integrity in the inferior longitudinal fasciculus in adolescents with schizophrenia as revealed by fiber tractography.Arch Gen Psychiatry. 2007; 64: 1270-1280
- Probing the pathophysiology of auditory/verbal hallucinations by combining functional magnetic resonance imaging and transcranial magnetic stimulation.Cereb Cortex. 2007; 17: 2733-2743
- Auditory verbal hallucinations predominantly activate the right inferior frontal area.Brain. 2008; 131: 3169-3177
- Predicting inter-hemispheric transfer time from the diffusion properties of the corpus callosum in healthy individuals and schizophrenia patients: a combined ERP and DTI study.Neuroimage. 2011; 54: 2318-2329
- The role of the corpus callosum in transcranial magnetic stimulation induced interhemispheric signal propagation.Biol Psychiatry. 2010; 68: 825-831
- Fiber tractography reveals disruption of temporal lobe white matter tracts in schizophrenia.Schizophr Res. 2009; 107: 30-38
- Altered cerebellar feedback projections in Asperger syndrome.Neuroimage. 2008; 41: 1184-1191
- The anatomy of extended limbic pathways in Asperger syndrome: a preliminary diffusion tensor imaging tractography study.Neuroimage. 2009; 47: 427-434
- Microstructural organization of cerebellar tracts in schizophrenia.Biol Psychiatry. 2009; 66: 1067-1069
- Morbid risk of schizophrenia for relatives of patients with cannabis-associated psychosis.Schizophr Res. 1995; 15: 277-281
- Modality specific neural correlates of auditory and somatic hallucinations.J Neurol Neurosurg Psychiatry. 2001; 71: 688-690
- Effectiveness of a second deep TMS in depression: a brief report.Prog Neuropsychopharmacol Biol Psychiatry. 2011; 35: 1041-1044
- Slow transcranial magnetic stimulation can rapidly reduce resistant auditory hallucinations in schizophrenia.Biol Psychiatry. 2005; 57: 188-191
- Transcranial magnetic stimulation of left temporoparietal cortex and medication-resistant auditory hallucinations.Arch Gen Psychiatry. 2003; 60: 49-56
- Successful use of maintenance rTMS for 8 months in a patient with antipsychotic-refractory auditory hallucinations.Schizophr Res. 2008; 100: 351-352
Article info
Publication history
Published online: July 28, 2011
Accepted:
June 6,
2011
Received in revised form:
May 17,
2011
Received:
November 12,
2010
Footnotes
Authors MC and MCC contributed equally to this work.
Identification
Copyright
© 2011 Society of Biological Psychiatry. Published by Elsevier Inc. All rights reserved.
