Aberrant resting-state connectivity in non-psychotic individuals with auditory hallucinations

Background Although auditory verbal hallucinations (AVH) are a core symptom of schizophrenia, they also occur in non-psychotic individuals, in the absence of other psychotic, affective, cognitive and negative symptoms. AVH have been hypothesized to result from deviant integration of inferior frontal, parahippocampal and superior temporal brain areas. However, a direct link between dysfunctional connectivity and AVH has not yet been established. To determine whether hallucinations are indeed related to aberrant connectivity, AVH should be studied in isolation, for example in non-psychotic individuals with AVH. Method Resting-state connectivity was investigated in 25 non-psychotic subjects with AVH and 25 matched control subjects using seed regression analysis with the (1) left and (2) right inferior frontal, (3) left and (4) right superior temporal and (5) left parahippocampal areas as the seed regions. To correct for cardiorespiratory (CR) pulsatility rhythms in the functional magnetic resonance imaging (fMRI) data, heartbeat and respiration were monitored during scanning and the fMRI data were corrected for these rhythms using the image-based method for retrospective correction of physiological motion effects RETROICOR. Results In comparison with the control group, non-psychotic individuals with AVH showed increased connectivity between the left and the right superior temporal regions and also between the left parahippocampal region and the left inferior frontal gyrus. Moreover, this group did not show a negative correlation between the left superior temporal region and the right inferior frontal region, as was observed in the healthy control group. Conclusions Aberrant connectivity of frontal, parahippocampal and superior temporal brain areas can be specifically related to the predisposition to hallucinate in the auditory domain.

[1]  A. Aleman,et al.  Abnormal connectivity between attentional, language and auditory networks in schizophrenia , 2012, Schizophrenia Research.

[2]  J. Fleiss,et al.  The global assessment scale. A procedure for measuring overall severity of psychiatric disturbance. , 1976, Archives of general psychiatry.

[3]  C. Frith,et al.  Disordered functional connectivity in schizophrenia , 1996, Psychological Medicine.

[4]  Erno J. Hermans,et al.  Enhanced resting-state connectivity of amygdala in the immediate aftermath of acute psychological stress , 2010, NeuroImage.

[5]  A. Tien,et al.  Distributions of hallucinations in the population. , 1991, Social psychiatry and psychiatric epidemiology.

[6]  N. Andreasen,et al.  COMPREHENSIVE ASSESSMENT OF SYMPTOMS AND HISTORY (CASH) , 2000 .

[7]  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.

[8]  D. Garza.  Hallucinations: The Science of Idiosyncratic Perception , 2009 .

[9]  Judith M Ford,et al.  Relationship of imprecise corollary discharge in schizophrenia to auditory hallucinations. , 2007, Archives of general psychiatry.

[10]  Functional anatomy of verbal fluency in people with schizophrenia and those at genetic risk , 2000, Schizophrenia Research.

[11]  M Davies,et al.  The Structured Clinical Interview for DSM-III-R (SCID). II. Multisite test-retest reliability. , 1992 .

[12]  Derek K. Jones,et al.  A diffusion tensor imaging study of fasciculi in schizophrenia. , 2007, The American journal of psychiatry.

[13]  S. Petersen,et al.  Memory's echo: vivid remembering reactivates sensory-specific cortex. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[14]  Karl J. Friston,et al.  Regional Brain Activity in Chronic Schizophrenic Patients during the Performance of a Verbal Fluency Task , 1995, British Journal of Psychiatry.

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

[16]  K. Diederen,et al.  Neuroimaging of Voice Hearing in Non-Psychotic Individuals: A Mini Review , 2012, Front. Hum. Neurosci..

[17]  Kevin Murphy,et al.  The impact of global signal regression on resting state correlations: Are anti-correlated networks introduced? , 2009, NeuroImage.

[18]  Vinod Menon,et al.  Functional connectivity in the resting brain: A network analysis of the default mode hypothesis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[19]  Philip K. McGuire,et al.  The hallucinating brain: A review of structural and functional neuroimaging studies of hallucinations , 2008, Neuroscience & Biobehavioral Reviews.

[20]  Peter A. Bandettini,et al.  Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI , 2006, NeuroImage.

[21]  A. Raine.  The SPQ: a scale for the assessment of schizotypal personality based on DSM-III-R criteria. , 1991, Schizophrenia bulletin.

[22]  R. S. Kahn,et al.  Microstructural alterations of the arcuate fasciculus in schizophrenia patients with frequent auditory verbal hallucinations , 2011, Schizophrenia Research.

[23]  Stephen M. Smith,et al.  Advances and Pitfalls in the Analysis and Interpretation of Resting-State FMRI Data , 2010, Front. Syst. Neurosci..

[24]  Erno J. Hermans,et al.  Enhanced sensitivity with fast three‐dimensional blood‐oxygen‐level‐dependent functional MRI: comparison of SENSE–PRESTO and 2D‐EPI at 3 T , 2008, NMR in biomedicine.

[25]  N C Andreasen,et al.  The Comprehensive Assessment of Symptoms and History (CASH). An instrument for assessing diagnosis and psychopathology. , 1992, Archives of general psychiatry.

[26]  Matthijs Vink,et al.  Cardiorespiratory effects on default‐mode network activity as measured with fMRI , 2009, Human brain mapping.

[27]  Karl J. Friston,et al.  Functional anatomy of verbal fluency in people with schizophrenia and those at genetic risk , 2000, Schizophrenia Research.

[28]  G. Ojemann.  Cortical organization of language , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[29]  Catie Chang,et al.  Effects of model-based physiological noise correction on default mode network anti-correlations and correlations , 2009, NeuroImage.

[30]  R. Kahn,et al.  Increased psychophysiological parameters of attention in non-psychotic individuals with auditory verbal hallucinations , 2010, Schizophrenia Research.

[31]  Sukhwinder S Shergill,et al.  Auditory hallucinations: a review of psychological treatments , 1998, Schizophrenia Research.

[32]  Jeffrey D. Johnson,et al.  Recollection and the reinstatement of encoding-related cortical activity. , 2007, Cerebral cortex.

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

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

[35]  J. Haxby,et al.  Localization of Cardiac-Induced Signal Change in fMRI , 1999, NeuroImage.

[36]  E. Bullmore,et al.  Differences in frontal cortical activation by a working memory task after substitution of risperidone for typical antipsychotic drugs in patients with schizophrenia. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[37]  R. Kahn,et al.  The same or different? A phenomenological comparison of auditory verbal hallucinations in healthy and psychotic individuals. , 2011, The Journal of clinical psychiatry.

[38]  Judith M Ford,et al.  Synch before you speak: auditory hallucinations in schizophrenia. , 2007, The American journal of psychiatry.

[39]  M. First,et al.  The Structured Clinical Interview for DSM-III-R (SCID). I: History, rationale, and description. , 1992, Archives of general psychiatry.

[40]  G. V. Hoesen,et al.  The parahippocampal gyrus: New observations regarding its cortical connections in the monkey , 1982, Trends in Neurosciences.

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

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

[43]  G H Glover,et al.  Image‐based method for retrospective correction of physiological motion effects in fMRI: RETROICOR , 2000, Magnetic resonance in medicine.

[44]  H. Eichenbaum,et al.  The medial temporal lobe and recognition memory. , 2007, Annual review of neuroscience.

[45]  Thomas E. Nichols,et al.  Non-white noise in fMRI: Does modelling have an impact? , 2006, NeuroImage.

[46]  G. Egan,et al.  Cortical activation associated with the experience of auditory hallucinations and perception of human speech in schizophrenia: a PET correlation study , 2003, Psychiatry Research: Neuroimaging.

[47]  R. Kahn,et al.  Aberrations in the arcuate fasciculus are associated with auditory verbal hallucinations in psychotic and in non‐psychotic individuals , 2011, Human brain mapping.

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

[49]  R. Hoffman,et al.  Time course of regional brain activity accompanying auditory verbal hallucinations in schizophrenia , 2011, British Journal of Psychiatry.

[50]  H Eichenbaum,et al.  Functional organization of the hippocampal memory system. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[51]  A. Anderson,et al.  Time course of regional brain activation associated with onset of auditory/verbal hallucinations , 2008, British Journal of Psychiatry.

[52]  Walter Schneider,et al.  Theory, simulation, and compensation of physiological motion artifacts in functional MRI , 1994, Proceedings of 1st International Conference on Image Processing.

[53]  Karl J. Friston,et al.  Unified segmentation , 2005, NeuroImage.

[54]  Richard S. J. Frackowiak,et al.  A functional neuroanatomy of hallucinations in schizophrenia , 1995, Nature.

[55]  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.

[56]  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.

[57]  K. Diederen,et al.  Auditory hallucinations elicit similar brain activation in psychotic and nonpsychotic individuals. , 2012, Schizophrenia bulletin.

[58]  H. Eichenbaum.  A cortical–hippocampal system for declarative memory , 2000, Nature Reviews Neuroscience.

[59]  Rutger Goekoop,et al.  Deactivation of the parahippocampal gyrus preceding auditory hallucinations in schizophrenia. , 2010, The American journal of psychiatry.

[60]  Sebastiaan F W Neggers,et al.  Decreased language lateralization is characteristic of psychosis, not auditory hallucinations. , 2010, Brain : a journal of neurology.

[61]  Paul Allen,et al.  Neural correlates of the misattribution of speech in schizophrenia , 2007, British Journal of Psychiatry.

[62]  G H Glover,et al.  Motion Artifacts in fMRI: Comparison of 2DFT with PR and Spiral Scan Methods , 1995, Magnetic resonance in medicine.

[63]  A. Tien.  Distribution of hallucinations in the population , 1991, Social Psychiatry and Psychiatric Epidemiology.

[64]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.