Auditory M50 and M100 sensory gating deficits in bipolar disorder: a MEG study.

OBJECTIVES Auditory sensory gating deficits have been reported in subjects with bipolar disorder, but the hemispheric and neuronal origins of this deficit are not well understood. Moreover, gating of the auditory evoked components reflecting early attentive stage of information processing has not been investigated in bipolar disorder. The objectives of this study were to investigate the right and left hemispheric auditory sensory gating of the M50 (preattentive processing) and M100 (early attentive processing) in patients diagnosed with bipolar I disorder by utilizing magnetoencephalography (MEG). METHODS Whole-head MEG data were acquired during the standard paired-click paradigm in 20 bipolar I disorder patients and 20 healthy controls. The M50 and the M100 responses were investigated, and dipole source localizations were also investigated. Sensory gating were determined by measuring the strength of the M50 and the M100 response to the second click divided by that of the first click (S2/S1). RESULTS In every subject, M50 and M100 dipolar sources localized to the left and right posterior portion of superior temporal gyrus (STG). Bipolar I disorder patients showed bilateral gating deficits in M50 and M100. The bilateral M50 S2 source strengths were significantly higher in the bipolar I disorder group compared to the control group. LIMITATIONS The sample size was relatively small. More studies with larger sample sizes are warranted. Bipolar subjects were taking a wide range of medications that could not be readily controlled for. CONCLUSIONS These findings suggest that bipolar I disorder patients have auditory gating deficits at both pre-attentive and early attentive levels, which might be related to STG structural abnormality.

[1]  R. Kessler,et al.  Lifetime and 12-month prevalence of bipolar spectrum disorder in the National Comorbidity Survey replication. , 2007, Archives of general psychiatry.

[2]  R Freedman,et al.  Schizophrenia, sensory gating, and nicotinic receptors. , 1998, Schizophrenia bulletin.

[3]  H. Hwu,et al.  More evidence to support the role of S2 in P50 studies , 2010, Schizophrenia Research.

[4]  R. Freedman,et al.  Neurophysiological assessment of sensory gating in psychiatric inpatients: Comparison between schizophrenia and other diagnoses , 1987, Biological Psychiatry.

[5]  David A. Smith,et al.  Reliability of P50 auditory event-related potential indices of sensory gating. , 1994, Psychophysiology.

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

[7]  J. Karhu,et al.  Impaired temporal lobe processing of preattentive auditory discrimination in schizophrenia. , 2002, Schizophrenia bulletin.

[8]  M. Fink.  ECT Has Much to Offer Our Patients: It Should Wot Be Ignored , 2001, The world journal of biological psychiatry : the official journal of the World Federation of Societies of Biological Psychiatry.

[9]  M. Yücel,et al.  Gray matter reduction of the superior temporal gyrus in patients with established bipolar I disorder. , 2010, Journal of affective disorders.

[10]  W. Bunney,et al.  An initial report of a new biological marker for bipolar disorder: P85 evoked brain potential. , 2009, Bipolar disorders.

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

[12]  Mingxiong Huang,et al.  Cognitive abilities and 50- and 100-msec paired-click processes in schizophrenia. , 2010, The American journal of psychiatry.

[13]  Sabine Landau,et al.  Evidence for altered neuronal organisation within the planum temporale in major psychiatric disorders , 2005, Schizophrenia Research.

[14]  R Freedman,et al.  Neurobiological studies of sensory gating in schizophrenia. , 1987, Schizophrenia bulletin.

[15]  H. Fukuyama,et al.  Corticolimbic balance shift of regional glucose metabolism in depressed patients treated with ECT. , 2012, Journal of affective disorders.

[16]  A. Olincy,et al.  Diminished suppression of the P50 auditory evoked potential in bipolar disorder subjects with a history of psychosis. , 2005, The American journal of psychiatry.

[17]  R. Chan,et al.  Neuroleptic effects on P50 sensory gating in patients with first-episode never-medicated schizophrenia , 2009, Schizophrenia Research.

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

[19]  Wen-Pin Chang,et al.  Probing the relative contribution of the first and second responses to sensory gating indices: a meta-analysis. , 2011, Psychophysiology.

[20]  Mingxiong Huang,et al.  Distinct M50 and M100 auditory gating deficits in schizophrenia. , 2005, Psychophysiology.

[21]  L. J. Bour,et al.  A meta-analysis of P50 studies in patients with schizophrenia and relatives: Differences in methodology between research groups , 2007, Schizophrenia Research.

[22]  Michael P. Milham,et al.  Cortical abnormalities in bipolar disorder investigated with MRI and voxel-based morphometry , 2006, NeuroImage.

[23]  Kiyoto Kasai,et al.  Auditory gating deficit to human voices in schizophrenia: A MEG study , 2010, Schizophrenia Research.

[24]  Nash N. Boutros,et al.  Relationships between sensory “gating out” and sensory “gating in” of auditory evoked potentials in schizophrenia: A pilot study , 2010, Schizophrenia Research.

[25]  K. Nuechterlein,et al.  Distinct neural generators of sensory gating in schizophrenia. , 2011, Psychophysiology.

[26]  J M Badier,et al.  Evoked potentials recorded from the auditory cortex in man: evaluation and topography of the middle latency components. , 1994, Electroencephalography and clinical neurophysiology.

[27]  L. J. Chapman,et al.  Progress in experimental personality & psychopathology research , 1992 .

[28]  R P Lesser,et al.  Recording of auditory evoked potentials in man using chronic subdural electrodes. , 1984, Brain : a journal of neurology.

[29]  H. J. Wieringa,et al.  Source localization of EEG versus MEG: Empirical comparison using visually evoked responses and theoretical considerations , 2005, Brain Topography.

[30]  J. Alpert,et al.  Neurophysiological studies of sensory gating in mania: comparison with schizophrenia. , 1983, Biological psychiatry.

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

[32]  A. Barabash,et al.  P50 sensory gating deficit is a common marker of vulnerability to bipolar disorder and schizophrenia , 2008, Acta psychiatrica Scandinavica.

[33]  Thomas Grunwald,et al.  Neuronal substrates of sensory gating within the human brain , 2003, Biological Psychiatry.

[34]  R. Freedman,et al.  Sensory gating and alpha‐7 nicotinic receptor gene allelic variants in schizoaffective disorder, bipolar type , 2007, American journal of medical genetics. Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics.

[35]  A. Barabash,et al.  P50 sensory gating is a trait marker of the bipolar spectrum , 2013, European Neuropsychopharmacology.

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

[37]  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.

[38]  P. Teale,et al.  Sequential source of the M100 exhibits inter‐hemispheric asymmetry , 1998, Neuroreport.

[39]  H. Otsubo,et al.  Neuromagnetic spectral distribution of implicit processing of words , 2001, Neuroreport.

[40]  Oleg Korzyukov,et al.  Sensory gating deficits during the mid-latency phase of information processing in medicated schizophrenia patients , 2004, Psychiatry Research.

[41]  R. Freedman,et al.  Defects in auditory sensory gating and their apparent compensation in relatives of schizophrenics , 1988, Schizophrenia Research.

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

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

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

[45]  A. Barabash,et al.  Sensory gating deficit is associated with catechol-O-methyltransferase polymorphisms in bipolar disorder , 2011, The world journal of biological psychiatry : the official journal of the World Federation of Societies of Biological Psychiatry.

[46]  J. Sweeney,et al.  Affective Neural Circuitry During Facial Emotion Processing in Pediatric Bipolar Disorder , 2007, Biological Psychiatry.

[47]  Aysenil Belger,et al.  Comparison of four components of sensory gating in schizophrenia and normal subjects: a preliminary report , 1999, Psychiatry Research.

[48]  Steven C. R. Williams,et al.  Meta-analysis, database, and meta-regression of 98 structural imaging studies in bipolar disorder. , 2008, Archives of general psychiatry.

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

[50]  Jürgen Gallinat,et al.  Test-retest reliability of P50, N100 and P200 auditory sensory gating in healthy subjects. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[51]  H. C. Cromwell,et al.  Sensory Gating: A Translational Effort from Basic to Clinical Science , 2008, Clinical EEG and neuroscience.

[52]  Association between tobacco smoking and bipolar affective disorder: clinical, epidemiological, cross-sectional, retrospective study in outpatients. , 2012, Comprehensive psychiatry.

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

[54]  E. Bramon,et al.  Further evidence for shared genetic effects between psychotic bipolar disorder and P50 suppression: A combined twin and family study , 2008, American journal of medical genetics. Part B, Neuropsychiatric genetics : the official publication of the International Society of Psychiatric Genetics.

[55]  G. Gerhardt,et al.  Sensory physiology and catecholamines in schizophrenia and mania , 1990, Psychiatry Research.

[56]  E. Bramon,et al.  P50 Auditory Evoked Potential Suppression in Bipolar Disorder Patients With Psychotic Features and Their Unaffected Relatives , 2007, Biological Psychiatry.

[57]  A. Barabash,et al.  CHRNA7 haplotypes are associated with impaired attention in euthymic bipolar disorder. , 2011, Journal of affective disorders.

[58]  Oleg Korzyukov,et al.  Generators of the intracranial P50 response in auditory sensory gating , 2007, NeuroImage.

[59]  B. Clementz,et al.  The gamma band response may account for poor P50 suppression in schizophrenia , 1997, Neuroreport.

[60]  Nash N. Boutros,et al.  Diminished P50, N100 and P200 auditory sensory gating in bipolar I disorder , 2009, Psychiatry Research.

[61]  T. Prentice.  World Health Report , 2013 .

[62]  R. Thoma,et al.  Lateralized abnormalities in auditory M50 sensory gating and cortical thickness of the superior temporal gyrus in post-traumatic stress disorder: Preliminary results , 2011, Psychiatry Research: Neuroimaging.

[63]  B. O’Donnell,et al.  Contributions of spectral frequency analyses to the study of P50 ERP amplitude and suppression in bipolar disorder with or without a history of psychosis. , 2008, Bipolar disorders.

[64]  I. Tendolkar,et al.  Sensory Gating in Schizophrenia: P50 and N100 Gating in Antipsychotic-Free Subjects at Risk, First-Episode, and Chronic Patients , 2008, Biological Psychiatry.

[65]  Andrew C. N. Chen,et al.  Memory impairment and auditory evoked potential gating deficit in schizophrenia , 2004, Psychiatry Research: Neuroimaging.

[66]  Eero Pekkonen,et al.  Delayed auditory processing underlying stimulus detection in Down syndrome , 2007, NeuroImage.

[67]  G. Gerhardt,et al.  Sensory gating deficits in psychiatric impatients: Relation to catecholamine metabolites in different diagnostic groups , 1990, Biological Psychiatry.