Altered Fronto-Temporal Functional Connectivity in Individuals at Ultra-High-Risk of Developing Psychosis

Background The superior temporal gyrus (STG) is one of the key regions implicated in psychosis, given that abnormalities in this region are associated with an increased risk of conversion from an at-risk mental state to psychosis. However, inconsistent results regarding the functional connectivity strength of the STG have been reported, and the regional heterogeneous characteristics of the STG should be considered. Methods To investigate the distinctive functional connection of each subregion in the STG, we parcellated the STG of each hemisphere into three regions: the planum temporale, Heschl’s gyrus, and planum polare. Resting-state functional magnetic resonance imaging was obtained from 22 first-episode psychosis (FEP) patients, 41 individuals at ultra-high-risk for psychosis (UHR), and 47 demographically matched healthy controls. Results Significant group differences (in seed-based connectivity) were demonstrated in the left planum temporale and from both the right and left Heschl’s gyrus seeds. From the left planum temporale seed, the FEP and UHR groups exhibited increased connectivity to the bilateral dorsolateral prefrontal cortex. In contrast, the FEP and UHR groups demonstrated decreased connectivity from the bilateral Heschl’s gyrus seeds to the dorsal anterior cingulate cortex. The enhanced connectivity between the left planum temporale and right dorsolateral prefrontal cortex was positively correlated with positive symptom severity in individuals at UHR (r = .34, p = .03). Conclusions These findings corroborate the fronto-temporal connectivity disruption hypothesis in schizophrenia by providing evidence supporting the altered fronto-temporal intrinsic functional connection at earlier stages of psychosis. Our data indicate that subregion-specific aberrant fronto-temporal interactions exist in the STG at the early stage of psychosis, thus suggesting that these aberrancies are the neural underpinning of proneness to psychosis.

[1]  Klaus Willmes,et al.  Auditory mismatch impairments are characterized by core neural dysfunctions in schizophrenia. , 2015, Brain : a journal of neurology.

[2]  Mary Beth Nebel,et al.  Reduction of motion-related artifacts in resting state fMRI using aCompCor , 2014, NeuroImage.

[3]  Tae Young Lee,et al.  Symptomatic and functional remission of subjects at clinical high risk for psychosis: A 2-year naturalistic observational study , 2014, Schizophrenia Research.

[4]  Jimmy Lee,et al.  Altered striatal functional connectivity in subjects with an at-risk mental state for psychosis. , 2014, Schizophrenia bulletin.

[5]  Paul Allen,et al.  Auditory Verbal Hallucinations and Brain Dysconnectivity in the Perisylvian Language Network: A Multimodal Investigation , 2013, Schizophrenia bulletin.

[6]  Peter B. Jones,et al.  Functional dysconnectivity of corticostriatal circuitry as a risk phenotype for psychosis. , 2013, JAMA psychiatry.

[7]  R. Kahn,et al.  Schizophrenia is a cognitive illness: time for a change in focus. , 2013, JAMA psychiatry.

[8]  F. Darvas,et al.  Corrigendum to “Spatio-temporal source imaging reveals subcomponents of the human auditory mismatch negativity in the cingulum and right inferior temporal gyrus” [Neurosci. Lett. 308 (2001) 107–110] , 2013, Neuroscience Letters.

[9]  D. Prvulovic,et al.  Reduced functional connectivity and asymmetry of the planum temporale in patients with schizophrenia and first-degree relatives , 2013, Schizophrenia Research.

[10]  Kenji Kirihara,et al.  Neural substrates of normal and impaired preattentive sensory discrimination in large cohorts of nonpsychiatric subjects and schizophrenia patients as indexed by MMN and P3a change detection responses , 2013, NeuroImage.

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

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

[13]  Joaquim Radua,et al.  Neuroanatomical maps of psychosis onset: voxel-wise meta-analysis of antipsychotic-naive VBM studies. , 2012, Schizophrenia bulletin.

[14]  J. Kwon,et al.  Aberrant auditory processing in schizophrenia and in subjects at ultra-high-risk for psychosis. , 2012, Schizophrenia bulletin.

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

[16]  Philip K. McGuire,et al.  Alterations in White Matter Evident Before the Onset of Psychosis , 2012, Schizophrenia bulletin.

[17]  Tae Young Lee,et al.  Early intervention in psychosis: Insights from Korea. , 2012, Asian journal of psychiatry.

[18]  M. L. Le Pelley,et al.  Attention to Irrelevant Cues Is Related to Positive Symptoms in Schizophrenia , 2012, Schizophrenia bulletin.

[19]  A. Belger,et al.  In Search of Psychosis Biomarkers in High-risk Populations: Is the Mismatch Negativity the One We've Been Waiting for? , 2012, Biological Psychiatry.

[20]  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.

[21]  Peter F. Liddle,et al.  Aberrant salience network (bilateral insula and anterior cingulate cortex) connectivity during information processing in schizophrenia , 2010, Schizophrenia Research.

[22]  Anders M. Dale,et al.  Automatic parcellation of human cortical gyri and sulci using standard anatomical nomenclature , 2010, NeuroImage.

[23]  J. A. Boer,et al.  Auditory Hallucinations in Schizophrenia Are Associated with Reduced Functional Connectivity of the Temporo-Parietal Area , 2010, Biological Psychiatry.

[24]  Alex Fornito,et al.  What can spontaneous fluctuations of the blood oxygenation-level-dependent signal tell us about psychiatric disorders? , 2010, Current opinion in psychiatry.

[25]  A. Caspi,et al.  Static and dynamic cognitive deficits in childhood preceding adult schizophrenia: a 30-year study. , 2010, The American journal of psychiatry.

[26]  Philip K. McGuire,et al.  Cingulate activity and fronto-temporal connectivity in people with prodromal signs of psychosis , 2010, NeuroImage.

[27]  E. Bramon,et al.  Superior temporal lobe dysfunction and frontotemporal dysconnectivity in subjects at risk of psychosis and in first‐episode psychosis , 2009, Human brain mapping.

[28]  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.

[29]  K. Davis,et al.  Two systems of resting state connectivity between the insula and cingulate cortex , 2009, Human brain mapping.

[30]  Jun Soo Kwon,et al.  Pre-Attentive Auditory Processing in Ultra-High-Risk for Schizophrenia with Magnetoencephalography , 2009, Biological Psychiatry.

[31]  C. Pantelis,et al.  Progressive gray matter reduction of the superior temporal gyrus during transition to psychosis. , 2009, Archives of general psychiatry.

[32]  P. Mcguire,et al.  Duration of untreated prodromal symptoms and 12-month functional outcome of individuals at risk of psychosis. , 2009, The British journal of psychiatry : the journal of mental science.

[33]  Karl J. Friston,et al.  Dysconnection in Schizophrenia: From Abnormal Synaptic Plasticity to Failures of Self-monitoring , 2009, Schizophrenia bulletin.

[34]  Paul Allen,et al.  Misattribution of speech and impaired connectivity in patients with auditory verbal hallucinations , 2007, Human brain mapping.

[35]  M. Fox,et al.  Spontaneous fluctuations in brain activity observed with functional magnetic resonance imaging , 2007, Nature Reviews Neuroscience.

[36]  Thomas T. Liu,et al.  A component based noise correction method (CompCor) for BOLD and perfusion based fMRI , 2007, NeuroImage.

[37]  Philip K. McGuire,et al.  Regional Gray Matter Volume Abnormalities in the At Risk Mental State , 2007, Biological Psychiatry.

[38]  Yuan Zhou,et al.  Functional dysconnectivity of the dorsolateral prefrontal cortex in first-episode schizophrenia using resting-state fMRI , 2007, Neuroscience Letters.

[39]  J. Ragland,et al.  Alterations of fronto-temporal connectivity during word encoding in schizophrenia , 2007, Psychiatry Research: Neuroimaging.

[40]  W. McMahon,et al.  Superior Temporal Gyrus, Language Function, and Autism , 2007, Developmental neuropsychology.

[41]  Karl J. Friston,et al.  Synaptic Plasticity and Dysconnection in Schizophrenia , 2006, Biological Psychiatry.

[42]  Jill Harkavy-Friedman,et al.  Resting neural activity distinguishes subgroups of schizophrenia patients , 2004, Biological Psychiatry.

[43]  D. Poeppel,et al.  Dorsal and ventral streams: a framework for understanding aspects of the functional anatomy of language , 2004, Cognition.

[44]  Ulrich Schall,et al.  Functional neuroanatomy of auditory mismatch processing: an event-related fMRI study of duration-deviant oddballs , 2003, NeuroImage.

[45]  S. Dehaene,et al.  Functional Neuroimaging of Speech Perception in Infants , 2002, Science.

[46]  T. McGlashan,et al.  Prospective diagnosis of the initial prodrome for schizophrenia based on the Structured Interview for Prodromal Syndromes: preliminary evidence of interrater reliability and predictive validity. , 2002, The American journal of psychiatry.

[47]  Felix Darvas,et al.  Spatio-temporal source imaging reveals subcomponents of the human auditory mismatch negativity in the cingulum and right inferior temporal gyrus , 2001, Neuroscience Letters.

[48]  R Tandon,et al.  Superior temporal gyrus in schizophrenia: a volumetric magnetic resonance imaging study , 2000, Schizophrenia Research.

[49]  J. Kaas,et al.  Auditory processing in primate cerebral cortex , 1999, Current Opinion in Neurobiology.

[50]  Karl J. Friston The disconnection hypothesis , 1998, Schizophrenia Research.

[51]  S. Clarke,et al.  Cytochrome Oxidase, Acetylcholinesterase, and NADPH-Diaphorase Staining in Human Supratemporal and Insular Cortex: Evidence for Multiple Auditory Areas , 1997, NeuroImage.

[52]  D. Pandya,et al.  Anatomy of the auditory cortex. , 1995, Revue neurologique.

[53]  M. LeMay,et al.  Abnormalities of the left temporal lobe and thought disorder in schizophrenia. A quantitative magnetic resonance imaging study. , 1992, The New England journal of medicine.

[54]  A M Galaburda,et al.  The intrinsic architectonic and connectional organization of the superior temporal region of the rhesus monkey , 1983, The Journal of comparative neurology.

[55]  A. Galaburda,et al.  Cytoarchitectonic organization of the human auditory cortex , 1980, The Journal of comparative neurology.

[56]  B. Maher,et al.  Delusional thinking and perceptual disorder. , 1974, Journal of individual psychology.

[57]  P. Liddle,et al.  Does the salience network play a cardinal role in psychosis? An emerging hypothesis of insular dysfunction. , 2012, Journal of psychiatry & neuroscience : JPN.

[58]  R. Hoffman,et al.  Symptom Assessment in Schizophrenic Prodromal States , 2004, Psychiatric Quarterly.

[59]  L. Parsons,et al.  Interregional connectivity to primary motor cortex revealed using MRI resting state images , 1999, Human brain mapping.

[60]  M. First,et al.  Structured Clinical Interview for DSM-IV Axis I Disorders , 1997 .

[61]  Y. Lee,et al.  The Manual of Korean-Wechsler Adult Intelligence Scale , 1992 .

[62]  G D Pearlson,et al.  Auditory hallucinations and smaller superior temporal gyral volume in schizophrenia. , 1990, The American journal of psychiatry.

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

[64]  J. Kwon,et al.  OPEN ACCESS The Reliability and Validity of the Korean Version of the Structured Interview for Prodromal Syndrome , 2022 .