Citation for Published Item: Use Policy Neuroscience and Biobehavioral Reviews Hearing Voices in the Resting Brain: a Review of Intrinsic Functional Connectivity Research on Auditory Verbal Hallucinations

Resting state networks (RSNs) are thought to reflect the intrinsic functional connectivity of brain regions. Alterations to RSNs have been proposed to underpin various kinds of psychopathology, including the occurrence of auditory verbal hallucinations (AVH). This review outlines the main hypotheses linking AVH and the resting state, and assesses the evidence for alterations to intrinsic connectivity provided by studies of resting fMRI in AVH. The influence of hallucinations during data acquisition, medication confounds, and movement are also considered. Despite a large variety of analytic methods and designs being deployed, it is possible to conclude that resting connectivity in the left temporal lobe in general and left superior temporal gyrus in particular are disrupted in AVH. There is also preliminary evidence of atypical connectivity in the default mode network and its interaction with other RSNs. Recommendations for future research include the adoption of a common analysis protocol to allow for more overlapping datasets and replication of intrinsic functional connectivity alterations.

[1]  T. Whitford,et al.  Reduced integrity of the left arcuate fasciculus is specifically associated with auditory verbal hallucinations in schizophrenia , 2015, Schizophrenia Research.

[2]  Lars T. Westlye,et al.  Network-specific effects of age and in-scanner subject motion: A resting-state fMRI study of 238 healthy adults , 2012, NeuroImage.

[3]  André Aleman,et al.  Auditory Hallucinations in Schizophrenia Are Associated with Reduced Functional Connectivity of the Temporo-Parietal Area , 2010, Biological Psychiatry.

[4]  E. Rolls,et al.  Computational models of schizophrenia and dopamine modulation in the prefrontal cortex , 2008, Nature Reviews Neuroscience.

[5]  Mark Mühlau,et al.  Aberrant dependence of default mode/central executive network interactions on anterior insular salience network activity in schizophrenia. , 2014, Schizophrenia bulletin.

[6]  Georg Northoff,et al.  How can the brain's resting state activity generate hallucinations? A ‘resting state hypothesis’ of auditory verbal hallucinations , 2011, Schizophrenia Research.

[7]  C. Schönfeldt-Lecuona,et al.  Dysconnectivity of multiple resting-state networks in patients with schizophrenia who have persistent auditory verbal hallucinations. , 2011, Journal of psychiatry & neuroscience : JPN.

[8]  S. Kay,et al.  The positive and negative syndrome scale (PANSS) for schizophrenia. , 1987, Schizophrenia bulletin.

[9]  M. Alpert,et al.  Imagery vividness, reality testing, and schizophrenic hallucinations. , 1972, Journal of abnormal psychology.

[10]  K. Vogeley,et al.  Resting-state functional network correlates of psychotic symptoms in schizophrenia , 2010, Schizophrenia Research.

[11]  R. S. Kahn,et al.  Aberrant resting-state connectivity in non-psychotic individuals with auditory hallucinations , 2012, Psychological Medicine.

[12]  Michelle Hampson,et al.  Elevated Functional Connectivity Along a Corticostriatal Loop and the Mechanism of Auditory/Verbal Hallucinations in Patients with Schizophrenia , 2011, Biological Psychiatry.

[13]  Peter F. Liddle,et al.  Structural correlates of auditory hallucinations in schizophrenia: A meta-analysis , 2012, Schizophrenia Research.

[14]  D. Hubl,et al.  Structural Analysis of Heschl’s Gyrus in Schizophrenia Patients with Auditory Hallucinations , 2009, Neuropsychobiology.

[15]  M. Greicius,et al.  Resting-state functional connectivity reflects structural connectivity in the default mode network. , 2009, Cerebral cortex.

[16]  Mert R. Sabuncu,et al.  The influence of head motion on intrinsic functional connectivity MRI , 2012, NeuroImage.

[17]  T. Stompe,et al.  Culture and the prevalence of hallucinations in schizophrenia. , 2011, Comprehensive psychiatry.

[18]  W. Singer,et al.  Activation of Heschl’s Gyrus during Auditory Hallucinations , 1999, Neuron.

[19]  A. Aleman,et al.  Report on the inaugural meeting of the International Consortium on Hallucination Research: a clinical and research update and 16 consensus-set goals for future research. , 2012, Schizophrenia bulletin.

[20]  S. Eickhoff,et al.  Aberrant connectivity of areas for decoding degraded speech in patients with auditory verbal hallucinations , 2013, Brain Structure and Function.

[21]  Wei Deng,et al.  Short-term effects of antipsychotic treatment on cerebral function in drug-naive first-episode schizophrenia revealed by "resting state" functional magnetic resonance imaging. , 2010, Archives of general psychiatry.

[22]  G. Egan,et al.  Reduced connectivity of the auditory cortex in patients with auditory hallucinations: a resting state functional magnetic resonance imaging study , 2009, Psychological Medicine.

[23]  D. Pins,et al.  The neurodynamic organization of modality-dependent hallucinations. , 2013, Cerebral cortex.

[24]  C. Fernyhough,et al.  Report on the 2nd International Consortium on Hallucination Research: evolving directions and top-10 "hot spots" in hallucination research. , 2014, Schizophrenia bulletin.

[25]  I D Wilkinson,et al.  Neural activity in speech-sensitive auditory cortex during silence. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[26]  Renaud Jardri,et al.  The arcuate fasciculus in auditory-verbal hallucinations: A meta-analysis of diffusion-tensor-imaging studies , 2014, Schizophrenia Research.

[27]  Yufeng Zang,et al.  Individual Differences in Impulsivity Predict Head Motion during Magnetic Resonance Imaging , 2014, PloS one.

[28]  I Feinberg,et al.  Efference copy and corollary discharge: implications for thinking and its disorders. , 1978, Schizophrenia bulletin.

[29]  Abraham Z. Snyder,et al.  Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion , 2012, NeuroImage.

[30]  C. Price The anatomy of language: a review of 100 fMRI studies published in 2009 , 2010, Annals of the New York Academy of Sciences.

[31]  S. Kühn,et al.  Quantitative meta-analysis on state and trait aspects of auditory verbal hallucinations in schizophrenia. , 2012, Schizophrenia bulletin.

[32]  M. Stephane,et al.  Better Than Mermaids and Stray Dogs? Subtyping Auditory Verbal Hallucinations and Its Implications for Research and Practice , 2014, Schizophrenia bulletin.

[33]  R. Cho,et al.  Mechanisms of Auditory Verbal Hallucination in Schizophrenia , 2013, Front. Psychiatry.

[34]  Todd S. Woodward,et al.  Aberrant connectivity during self–other source monitoring in schizophrenia , 2011, Schizophrenia Research.

[35]  Renaud Jardri,et al.  Cortical activations during auditory verbal hallucinations in schizophrenia: a coordinate-based meta-analysis. , 2011, The American journal of psychiatry.

[36]  Daniel P. Kennedy,et al.  Largely typical patterns of resting-state functional connectivity in high-functioning adults with autism. , 2014, Cerebral cortex.

[37]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[38]  S. Debener,et al.  Default-mode brain dysfunction in mental disorders: A systematic review , 2009, Neuroscience & Biobehavioral Reviews.

[39]  S. Bressler,et al.  Large-scale brain networks in cognition: emerging methods and principles , 2010, Trends in Cognitive Sciences.

[40]  V. Menon Large-Scale Brain Networks in Cognition: Emerging Principles , 2010 .

[41]  Mark A. Elliott,et al.  Impact of in-scanner head motion on multiple measures of functional connectivity: Relevance for studies of neurodevelopment in youth , 2012, NeuroImage.

[42]  Willem M Otte,et al.  Network analysis of auditory hallucinations in nonpsychotic individuals , 2014, Human brain mapping.

[43]  Mark S. Bolding,et al.  Antipsychotic Drugs Alter Functional Connectivity between the Medial Frontal Cortex, Hippocampus, and Nucleus Accumbens as Measured by H215O PET , 2012, Front. Psychiatry.

[44]  J. Pillai Functional Connectivity. , 2017, Neuroimaging clinics of North America.

[45]  Leonard M. Freeman,et al.  A set of measures of centrality based upon betweenness , 1977 .

[46]  Ann K. Shinn,et al.  Default mode network abnormalities in bipolar disorder and schizophrenia , 2010, Psychiatry Research: Neuroimaging.

[47]  Greg G. Brown,et al.  Dysregulation of working memory and default‐mode networks in schizophrenia using independent component analysis, an fBIRN and MCIC study , 2009, Human brain mapping.

[48]  Remo Guidieri Res , 1995, RES: Anthropology and Aesthetics.

[49]  R. Hoffman,et al.  Neuroimaging auditory hallucinations in schizophrenia: from neuroanatomy to neurochemistry and beyond. , 2012, Schizophrenia bulletin.

[50]  D. Hubl,et al.  Resting-state EEG in schizophrenia: Auditory verbal hallucinations are related to shortening of specific microstates , 2011, Clinical Neurophysiology.

[51]  Justin T. Baker,et al.  Functional connectivity of left Heschl's gyrus in vulnerability to auditory hallucinations in schizophrenia , 2013, Schizophrenia Research.

[52]  R. Bluhm,et al.  Spontaneous low-frequency fluctuations in the BOLD signal in schizophrenic patients: anomalies in the default network. , 2007, Schizophrenia bulletin.

[53]  John H Krystal,et al.  Transcranial magnetic stimulation of left temporoparietal cortex and medication-resistant auditory hallucinations. , 2003, Archives of general psychiatry.

[54]  R. Baldessarini,et al.  Hallucinations in bipolar disorder: characteristics and comparison to unipolar depression and schizophrenia. , 2005, Bipolar disorders.

[55]  J. Ford,et al.  Schizophrenia, myelination, and delayed corollary discharges: a hypothesis. , 2012, Schizophrenia bulletin.

[56]  Fabio Sambataro,et al.  Treatment with Olanzapine is Associated with Modulation of the Default Mode Network in Patients with Schizophrenia , 2010, Neuropsychopharmacology.

[57]  P. McGuire,et al.  Neuroanatomy of auditory verbal hallucinations in schizophrenia: A quantitative meta-analysis of voxel-based morphometry studies , 2013, Cortex.

[58]  K. Diederen,et al.  Healthy individuals with auditory verbal hallucinations; who are they? Psychiatric assessments of a selected sample of 103 subjects. , 2010, Schizophrenia bulletin.

[59]  Cynthia G. Wible,et al.  From Tones in Tinnitus to Sensed Social Interaction in Schizophrenia: How Understanding Cortical Organization Can Inform the Study of Hallucinations and Psychosis , 2014, Schizophrenia bulletin.

[60]  J. McGrath,et al.  The cognitive neuropsychology of schizophrenia. , 1997 .

[61]  Simon B. Eickhoff,et al.  Resting State Functional Connectivity in Patients with Chronic Hallucinations , 2012, PloS one.

[62]  James G. Scott,et al.  Auditory Verbal Hallucinations in Persons With and Without a Need for Care , 2014, Schizophrenia bulletin.

[63]  N. Tarrier,et al.  Scales to measure dimensions of hallucinations and delusions: the psychotic symptom rating scales (PSYRATS) , 1999, Psychological Medicine.

[64]  Paul M. Thompson,et al.  Anxiety Modulates Insula Recruitment in Resting-State Functional Magnetic Resonance Imaging in Youth and Adults , 2011, Brain Connect..

[65]  J. Gabrieli,et al.  Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia , 2009, Proceedings of the National Academy of Sciences.

[66]  J. Ford,et al.  Default mode network activity and connectivity in psychopathology. , 2012, Annual review of clinical psychology.

[67]  M. Coltheart The neuropsychology of delusions , 2010, Annals of the New York Academy of Sciences.

[68]  J. Ford,et al.  Reduced communication between frontal and temporal lobes during talking in schizophrenia , 2002, Biological Psychiatry.

[69]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[70]  Matthew J. Brookes,et al.  Measuring functional connectivity using MEG: Methodology and comparison with fcMRI , 2011, NeuroImage.

[71]  Yuan Zhou,et al.  Functional disintegration in paranoid schizophrenia using resting-state fMRI , 2007, Schizophrenia Research.

[72]  Peter Williamson,et al.  Are anticorrelated networks in the brain relevant to schizophrenia? , 2007, Schizophrenia bulletin.

[73]  J. Ford,et al.  Electrophysiological and diffusion tensor imaging evidence of delayed corollary discharges in patients with schizophrenia , 2010, Psychological Medicine.

[74]  T. Eichele,et al.  Increased Intrinsic Brain Activity in the Striatum Reflects Symptom Dimensions in Schizophrenia , 2012, Schizophrenia bulletin.

[75]  R. Kahn,et al.  Auditory verbal hallucinations predominantly activate the right inferior frontal area. , 2008, Brain : a journal of neurology.

[76]  R. Salvador,et al.  Failure to deactivate in the prefrontal cortex in schizophrenia: dysfunction of the default mode network? , 2008, Psychological Medicine.

[77]  宁北芳,et al.  疟原虫var基因转换速率变化导致抗原变异[英]/Paul H, Robert P, Christodoulou Z, et al//Proc Natl Acad Sci U S A , 2005 .