Decreased Resting-State Interhemispheric Functional Connectivity Correlated with Neurocognitive Deficits in Drug-Naive First-Episode Adolescent-Onset Schizophrenia

Abstract Background Given that adolescence is a critical epoch in the onset of schizophrenia, studying aberrant brain changes in adolescent-onset schizophrenia, particularly in patients with drug-naive first-episode schizophrenia, is important to understand the biological mechanism of this disorder. Previous resting-state functional magnetic resonance imaging studies have shown abnormal functional connectivity in separate hemispheres in patients with adult-onset schizophrenia. Our aim to study adolescent-onset schizophrenia can provide clues for the early aetiology of schizophrenia. Method A total of 48 drug-naïve, first-episode, adolescent-onset schizophrenia outpatients and 31 healthy controls underwent resting-state functional magnetic resonance imaging scans. Data were subjected to voxel-mirrored homotopic connectivity and support vector machine analyses. Results Compared with the healthy controls, the adolescent-onset schizophrenia group showed significantly lower voxel-mirrored homotopic connectivity values in different brain regions, including the fusiform gyrus, superior temporal gyrus/insula, precentral gyrus, and precuneus. Decreased voxel-mirrored homotopic connectivity values in the superior temporal gyrus/insula were significantly correlated with Trail-Making Test: Part A performance (r = −0.437, P = .002). A combination of the voxel-mirrored homotopic connectivity values in the precentral gyrus and precuneus may be used to discriminate patients with adolescent-onset schizophrenia from controls with satisfactory classification results, which showed sensitivity of 100%, specificity of 87.09%, and accuracy of 94.93%. Conclusion Our findings highlight resting-state interhemispheric FC abnormalities within the sensorimotor network of patients with adolescent-onset schizophrenia and confirm the relationship between adolescent-onset schizophrenia and adult-onset schizophrenia. These findings suggest that reduced interhemispheric connectivity within the sensorimotor network has a pivotal role in the pathogenesis of schizophrenia.

[1]  Huafu Chen,et al.  Treatment effects of olanzapine on homotopic connectivity in drug-free schizophrenia at rest , 2018, The world journal of biological psychiatry : the official journal of the World Federation of Societies of Biological Psychiatry.

[2]  Dov B. Lerman-Sinkoff,et al.  Transdiagnostic Associations Between Functional Brain Network Integrity and Cognition , 2017, JAMA psychiatry.

[3]  Feng Liu,et al.  Family-based case-control study of homotopic connectivity in first-episode, drug-naive schizophrenia at rest , 2017, Scientific Reports.

[4]  C. Arango,et al.  Progressive brain changes in children and adolescents with early-onset psychosis: A meta-analysis of longitudinal MRI studies , 2016, Schizophrenia Research.

[5]  Feng Liu,et al.  Decreased interhemispheric functional connectivity in insula and angular gyrus/supramarginal gyrus: Significant findings in first-episode, drug-naive somatization disorder , 2016, Psychiatry Research: Neuroimaging.

[6]  M. Hoptman,et al.  Homotopic connectivity in drug-naïve, first-episode, early-onset schizophrenia. , 2015, Journal of child psychology and psychiatry, and allied disciplines.

[7]  Wenbin Guo,et al.  Decreased resting-state interhemispheric functional connectivity in unaffected siblings of schizophrenia patients , 2014, Schizophrenia Research.

[8]  Wenbin Guo,et al.  Decreased resting-state interhemispheric coordination in first-episode, drug-naive paranoid schizophrenia , 2014, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[9]  A. Aleman,et al.  Voxel-based gray and white matter morphometry correlates of hallucinations in schizophrenia: The superior temporal gyrus does not stand alone , 2013, NeuroImage: Clinical.

[10]  Huafu Chen,et al.  Decreased Interhemispheric Coordination in Treatment-Resistant Depression: A Resting-State fMRI Study , 2013, PloS one.

[11]  Ming Song,et al.  Aberrant Default Mode Functional Connectivity in Early Onset Schizophrenia , 2013, PloS one.

[12]  Huafu Chen,et al.  Decreased interhemispheric resting-state functional connectivity in first-episode, drug-naive major depressive disorder , 2013, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[13]  D. Javitt,et al.  Decreased interhemispheric coordination in schizophrenia: A resting state fMRI study , 2012, Schizophrenia Research.

[14]  Muriel Walshe,et al.  Prefrontal deviations in function but not volume are putative endophenotypes for schizophrenia. , 2012, Brain : a journal of neurology.

[15]  Hang Joon Jo,et al.  Trouble at Rest: How Correlation Patterns and Group Differences Become Distorted After Global Signal Regression , 2012, Brain Connect..

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

[17]  T. Crow,et al.  The relationship between callosal axons and cortical neurons in the planum temporale: Alterations in schizophrenia , 2011, Neuroscience Research.

[18]  M. Brannick,et al.  Psychometrics of Mayer-Salovey-Caruso Emotional Intelligence Test (MSCEIT) Scores , 2011, Psychological reports.

[19]  Alan C. Evans,et al.  Growing Together and Growing Apart: Regional and Sex Differences in the Lifespan Developmental Trajectories of Functional Homotopy , 2010, The Journal of Neuroscience.

[20]  M. Keshavan,et al.  Assessing social-cognitive deficits in schizophrenia with the Mayer-Salovey-Caruso Emotional Intelligence Test. , 2010, Schizophrenia bulletin.

[21]  Justin L. Vincent,et al.  Precuneus shares intrinsic functional architecture in humans and monkeys , 2009, Proceedings of the National Academy of Sciences.

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

[23]  M. E. Shenton,et al.  Reduced interhemispheric connectivity in schizophrenia-tractography based segmentation of the corpus callosum , 2008, Schizophrenia Research.

[24]  M. Corballis,et al.  Bilateral disadvantage: Lack of interhemispheric cooperation in schizophrenia , 2007, Consciousness and Cognition.

[25]  J. Rapoport,et al.  Longitudinal brain changes in early-onset psychosis. , 2007, Schizophrenia bulletin.

[26]  William Stafford Noble,et al.  Support vector machine , 2013 .

[27]  John J. Foxe,et al.  Visual white matter integrity in schizophrenia. , 2006, The American journal of psychiatry.

[28]  I. Tendolkar,et al.  Neurocognitive Functioning in Subjects at Risk for a First Episode of Psychosis Compared with First- and Multiple-episode Schizophrenia , 2006, Journal of clinical and experimental neuropsychology.

[29]  J. Lieberman.  Neurobiology and the natural history of schizophrenia. , 2006, The Journal of clinical psychiatry.

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

[31]  M. Desco,et al.  Structural neuroimaging in adolescents with a first psychotic episode. , 2005, Journal of the American Academy of Child and Adolescent Psychiatry.

[32]  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.

[33]  Derek K. Jones,et al.  Perisylvian language networks of the human brain , 2005, Annals of neurology.

[34]  William Stafford Noble,et al.  Support vector machine classification on the web , 2004, Bioinform..

[35]  R. Kikinis,et al.  Uncinate fasciculus findings in schizophrenia: a magnetic resonance diffusion tensor imaging study. , 2002, The American journal of psychiatry.

[36]  Li Liao,et al.  Combining pairwise sequence similarity and support vector machines for remote protein homology detection , 2002, RECOMB '02.

[37]  S. James,et al.  Evidence for non-progressive changes in adolescent-onset schizophrenia: follow-up magnetic resonance imaging study. , 2002, The British journal of psychiatry : the journal of mental science.

[38]  Brigitte Rockstroh,et al.  Reduced interhemispheric transmission in schizophrenia patients: evidence from event-related potentials , 2002, Neuroscience Letters.

[39]  R. Kahn,et al.  Language lateralization in schizophrenia, an fMRI study , 2001, Schizophrenia Research.

[40]  F Pulvermüller,et al.  Functional asymmetry in schizophrenic patients during auditory speech processing , 2001, Schizophrenia Research.

[41]  Chris H. Q. Ding,et al.  Multi-class protein fold recognition using support vector machines and neural networks , 2001, Bioinform..

[42]  C. Hollis.  Adult outcomes of child- and adolescent-onset schizophrenia: diagnostic stability and predictive validity. , 2000, The American journal of psychiatry.

[43]  Gunnar Rätsch,et al.  Engineering Support Vector Machine Kerneis That Recognize Translation Initialion Sites , 2000, German Conference on Bioinformatics.

[44]  J. Lieberman,et al.  Neuropsychology of first-episode schizophrenia: initial characterization and clinical correlates. , 2000, The American journal of psychiatry.

[45]  Rob Nicolson,et al.  Childhood-onset schizophrenia: rare but worth studying , 1999, Biological Psychiatry.

[46]  A. Toga,et al.  In vivo evidence for post-adolescent brain maturation in frontal and striatal regions , 1999, Nature Neuroscience.

[47]  A. L. Wolff,et al.  Motor deficits and schizophrenia: the evidence from neuroleptic-naïve patients and populations at risk. , 1999, Journal of psychiatry & neuroscience : JPN.

[48]  Jane S. Paulsen,et al.  Generalized cognitive deficits in schizophrenia: a study of first-episode patients. , 1999, Archives of general psychiatry.

[49]  J. Rapoport,et al.  Progressive cortical change during adolescence in childhood-onset schizophrenia. A longitudinal magnetic resonance imaging study. , 1999, Archives of general psychiatry.

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

[51]  T. Crow.  Schizophrenia as failure of hemispheric dominance for language. , 1997, Trends in neurosciences.

[52]  I. C. Wright,et al.  Corpus callosum size and inter-hemispheric function in schizophrenia , 1997, Schizophrenia Research.

[53]  J. Waddington,et al.  Developmental trajectory and disease progression in schizophrenia: the conundrum, and insights from a 12-year prospective study in the Monaghan 101 , 1997, Schizophrenia Research.

[54]  T. J. Crow,et al.  Cerebral lateralization is delayed in children who later develop schizophrenia , 1996, Schizophrenia Research.

[55]  S. W. Davies,et al.  Exon 1 of the HD Gene with an Expanded CAG Repeat Is Sufficient to Cause a Progressive Neurological Phenotype in Transgenic Mice , 1996, Cell.

[56]  H. Bracha,et al.  Prenatal growth markers in schizophrenia: a monozygotic co-twin control study. , 1996, The American journal of psychiatry.

[57]  P. Williamson,et al.  Aberrant interhemispheric alpha coherence on electroencephalography in schizophrenic patients during activation tasks , 1996, Psychological Medicine.

[58]  Jane S. Paulsen,et al.  Neuropsychological deficits in schizophrenics. Relationship to age, chronicity, and dementia. , 1994, Archives of general psychiatry.

[59]  Bettina Mohr,et al.  Lexical decision after left, right and bilateral presentation of function words, content words and non-words: Evidence for interhemispheric interaction , 1994, Neuropsychologia.

[60]  M. Banich,et al.  The sum of the parts does not equal the whole: evidence from bihemispheric processing. , 1992, Journal of experimental psychology. Human perception and performance.

[61]  L. DeLisi,et al.  Neuropsychological functioning of first-episode schizophreniform patients. , 1992, The American journal of psychiatry.

[62]  Armin Raznahan,et al.  Disrupted sensorimotor and social-cognitive networks underlie symptoms in childhood-onset schizophrenia. , 2016, Brain : a journal of neurology.

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

[64]  S. Luck,et al.  CNTRICS final task selection: control of attention. , 2009, Schizophrenia bulletin.

[65]  Li Liao,et al.  Combining Pairwise Sequence Similarity and Support Vector Machines for Detecting Remote Protein Evolutionary and Structural Relationships , 2003, J. Comput. Biol..

[66]  N C Andreasen,et al.  Thought, language, and communication in schizophrenia: diagnosis and prognosis. , 1986, Schizophrenia bulletin.

[67]  P. Magaro,et al.  Information processing and lateralization in schizophrenia. , 1983, Biological psychiatry.

[68]  Magaro Pa,et al.  Information processing and lateralization in schizophrenia. , 1983 .

[69]  R. Gur.  Motoric laterality imbalance in schizophrenia. A possible concomitant of left hemisphere dysfunction. , 1977, Archives of general psychiatry.