Auditory gating deficit to human voices in schizophrenia: A MEG study

BACKGROUND Patients with schizophrenia have auditory gating deficits; however, little is known about P50 auditory gating to human voices and its association with clinical symptoms. We examined the functioning of auditory gating and its relationship with the clinical symptoms in schizophrenia. METHODS Auditory evoked magnetoencephalography responses to the first and the second voices stimuli were recorded in 22 schizophrenia patients and 28 normal control subjects. The auditory gating ratios of P50m and N100m were investigated and P50m-symptom correlations were also investigated. RESULTS Patients showed significantly higher P50m gating ratios to human voices specifically in the left hemisphere. Moreover, patients with higher left P50m gating ratios showed more severe auditory hallucinations, while patients with higher right P50m gating ratios showed more severe negative symptoms. CONCLUSIONS The present study suggests that schizophrenia patients have auditory gating deficits to human voices, specifically in the left hemisphere and auditory hallucinations of schizophrenia may be associated with sensory overload to human voices in the auditory cortex.

[1]  N. Andreasen,et al.  Schizophrenia: the characteristic symptoms. , 1991, Schizophrenia bulletin.

[2]  M. Myles-Worsley,et al.  P50 sensory gating in multiplex schizophrenia families from a Pacific island isolate. , 2002, The American journal of psychiatry.

[3]  P. Woodruff,et al.  Auditory hallucinations: Insights and questions from neuroimaging , 2004, Cognitive neuropsychiatry.

[4]  R. Freedman,et al.  Lack of relationship of auditory gating defects to negative symptoms in schizophrenia , 1990, Schizophrenia Research.

[5]  B. Langguth,et al.  Cortical excitability in neuroleptic-naive first-episode schizophrenic patients , 2004, Schizophrenia Research.

[6]  Gregory A. Miller,et al.  M50 sensory gating predicts negative symptoms in schizophrenia , 2005, Schizophrenia Research.

[7]  Robert Freedman,et al.  Varied effects of atypical neuroleptics on P50 auditory gating in schizophrenia patients. , 2004, The American journal of psychiatry.

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

[9]  R. Freedman,et al.  Input dysfunction, schizotypy, and genetic models of schizophrenia , 2002, Schizophrenia Research.

[10]  D L Braff,et al.  Sensory gating deficits in schizophrenia: new results. , 1992, The American journal of psychiatry.

[11]  D. Hubl,et al.  Competition for neuronal resources: how hallucinations make themselves heard , 2007, British Journal of Psychiatry.

[12]  N. Boutros,et al.  Range of sensory gating values and test-retest reliability in normal subjects. , 2007, Psychophysiology.

[13]  David Keator,et al.  A PET study of the pathophysiology of negative symptoms in schizophrenia. Positron emission tomography. , 2002, The American journal of psychiatry.

[14]  D. Boatman.  Cortical bases of speech perception:evidence from functional lesion studies , 2004, Cognition.

[15]  E. Bramon,et al.  Meta-analysis of the P300 and P50 waveforms in schizophrenia , 2004, Schizophrenia Research.

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

[17]  G. A. Miller,et al.  Predicting EEG responses using MEG sources in superior temporal gyrus reveals source asynchrony in patients with schizophrenia , 2003, Clinical Neurophysiology.

[18]  R. Ilmoniemi,et al.  Magnetoencephalography-theory, instrumentation, and applications to noninvasive studies of the working human brain , 1993 .

[19]  W. Dement,et al.  Quantification of sleepiness: a new approach. , 1973, Psychophysiology.

[20]  Robert Freedman,et al.  Elementary phenotypes in the neurobiological and genetic study of schizophrenia , 1999, Biological Psychiatry.

[21]  Gregory A Miller,et al.  Improved test-retest reliability of 50-ms paired-click auditory gating using magnetoencephalography source modeling. , 2007, Psychophysiology.

[22]  A. Fallgatter,et al.  Sensory gating deficit in a subtype of chronic schizophrenic patients , 2004, Psychiatry Research.

[23]  G. Carey,et al.  Codistribution of a sensory gating deficit and schizophrenia in multi-affected families , 1991, Psychiatry Research.

[24]  D. Braff.  Information processing and attention dysfunctions in schizophrenia. , 1993, Schizophrenia bulletin.

[25]  K. Heilman,et al.  The role of the right hemisphere in emotional communication. , 1991, Brain : a journal of neurology.

[26]  R Freedman,et al.  Inhibitory gating of an evoked response to repeated auditory stimuli in schizophrenic and normal subjects. Human recordings, computer simulation, and an animal model. , 1996, Archives of general psychiatry.

[27]  B. Christensen,et al.  The role of cortical inhibition in the pathophysiology and treatment of schizophrenia , 2007, Brain Research Reviews.

[28]  G. A. Miller,et al.  Lateralization of auditory sensory gating and neuropsychological dysfunction in schizophrenia. , 2003, The American journal of psychiatry.

[29]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[30]  M. Pell.  Recognition of prosody following unilateral brain lesion: influence of functional and structural attributes of prosodic contours , 1998, Neuropsychologia.

[31]  C. Levitan,et al.  Superior temporal gyral volumes and laterality correlates of auditory hallucinations in schizophrenia , 1999, Biological Psychiatry.

[32]  Xu-Feng Huang,et al.  Increased density of GABAA receptors in the superior temporal gyrus in schizophrenia , 2005, Experimental Brain Research.

[33]  A. Korten,et al.  Early manifestations and first-contact incidence of schizophrenia in different cultures: A preliminary report on the initial evaluation phase of the WHO Collaborative Study on Determinants of Outcome of Severe Mental Disorders , 1986, Psychological Medicine.

[34]  A. Kring,et al.  Flat affect in schizophrenia: a test of neuropsychological models. , 1994, Schizophrenia bulletin.

[35]  J. M. Ollinger,et al.  Positron Emission Tomography , 2018, Handbook of Small Animal Imaging.

[36]  R Freedman,et al.  Neurophysiological evidence for a defect in neuronal mechanisms involved in sensory gating in schizophrenia. , 1982, Biological psychiatry.

[37]  R. Freedman,et al.  Deficits in sensory gating in schizophrenic patients and their relatives. Evidence obtained with auditory evoked responses. , 1984, Archives of general psychiatry.

[38]  Ann Summerfelt,et al.  Review of clinical correlates of P50 sensory gating abnormalities in patients with schizophrenia. , 2005, Schizophrenia bulletin.

[39]  R. Kikinis,et al.  Middle and inferior temporal gyrus gray matter volume abnormalities in chronic schizophrenia: an MRI study. , 2004, The American journal of psychiatry.

[40]  G. A. Miller,et al.  Interpreting abnormality: an EEG and MEG study of P50 and the auditory paired-stimulus paradigm , 2003, Biological Psychology.

[41]  T. Onitsuka,et al.  The effect of interstimulus intervals and between-block rests on the auditory evoked potential and magnetic field: is the auditory P50 in humans an overlapping potential? , 2000, Clinical Neurophysiology.

[42]  Robert Freedman,et al.  Neurophysiological and neuropsychological evidence for attentional dysfunction in schizophrenia , 1993, Schizophrenia Research.

[43]  Brett A. Clementz,et al.  P50 Suppression among schizophrenia and normal comparison subjects: A methodological analysis , 1997, Biological Psychiatry.

[44]  Idil Cavus,et al.  Slow transcranial magnetic stimulation, long-term depotentiation, and brain hyperexcitability disorders. , 2002, The American journal of psychiatry.

[45]  M. Geyer,et al.  Poor P50 suppression among schizophrenia patients and their first-degree biological relatives. , 1998, The American journal of psychiatry.

[46]  N. Andreasen.  Methods for assessing positive and negative symptoms. , 1990, Modern problems of pharmacopsychiatry.

[47]  M. E. Spencer,et al.  A Study of Dipole Localization Accuracy for MEG and EEG using a Human Skull Phantom , 1998, NeuroImage.

[48]  M. E. Spencer,et al.  A Study of Dipole Localization Accuracy for MEG and EEG using a Human Skull Phantom , 1998, NeuroImage.

[49]  D. Campion,et al.  P50 inhibitory gating deficit is correlated with the negative symptomatology of schizophrenia , 2005, Psychiatry Research.

[50]  P. Bickford,et al.  Inhibitory neurophysiological deficit as a phenotype for genetic investigation of schizophrenia. , 2000, American journal of medical genetics.

[51]  August B. Hollingshead,et al.  Two Factor Index of Social Position , 1957 .

[52]  平野 昭吾.  Abnormal neural oscillatory activity to speech sounds in schizophrenia : a magnetoencephalography study , 2009 .

[53]  B. Maher,et al.  Progress in experimental personality research , 1964 .

[54]  Robert Freedman,et al.  Elementary neuronal dysfunctions in schizophrenia , 1991, Schizophrenia Research.

[55]  P. Venables,et al.  INPUT DYSFUNCTION IN SCHIZOPHRENIA. , 1964, Progress in experimental personality research.

[56]  R. Kikinis,et al.  Middle and inferior temporal gyrus gray matter volume abnormalities in first-episode schizophrenia: an MRI study. , 2006, The American journal of psychiatry.

[57]  R. Heinrichs,et al.  Meta-analysis and the science of schizophrenia: variant evidence or evidence of variants? , 2004, Neuroscience & Biobehavioral Reviews.

[58]  K M Heilman,et al.  Comprehension of affective and nonaffective prosody , 1984, Neurology.