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γ-Band Auditory Steady-State Responses Are Impaired in First Episode Psychosis

      Background

      In chronic schizophrenia and chronic bipolar disorder, γ band (30–100 Hz) auditory steady-state electroencephalogram responses (ASSRs) are reduced in power and phase locking, likely reflecting neural circuit dysfunction. Here we examined whether γ ASSR deficits are also present at first hospitalization for psychosis.

      Methods

      Subjects were 16 first episode schizophrenia patients (SZ), 16 first episode affective disorder patients (AFF) (13 with bipolar disorder), and 33 healthy control subjects (HC). Stimuli were 20-, 30-, and 40-Hz binaural click trains. The ASSR phase locking and evoked power were analyzed with the Morlet wavelet transform.

      Results

      At 40-Hz stimulation, SZ and AFF had significantly reduced phase locking compared with HC. This deficit was more pronounced over the left hemisphere in SZ. Evoked power at 40 Hz was also reduced in the patients compared with HC. At 30-Hz stimulation phase locking and evoked power were reduced in both patient groups. The 20-Hz ASSR did not differ between groups, but phase locking and evoked power of the 40-Hz harmonic of the 20-Hz ASSR were reduced in both SZ and AFF. Phase locking of this 40-Hz harmonic was correlated with total positive symptoms in SZ.

      Conclusions

      The γ ASSR deficit is present at first hospitalization for both schizophrenia and affective disorder but shows a left hemisphere bias in first hospitalized SZ. Some of the neural circuitry abnormalities underlying the γ ASSR deficit might be common to psychoses in general, whereas others might be specific to particular disorders.

      Key Words

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      References

        • Singer W.
        Neuronal synchrony: A versatile code for the definition of relations?.
        Neuron. 1999; 24: 49-65
        • Lewis D.A.
        • Hashimoto T.
        • Volk D.W.
        Cortical inhibitory neurons and schizophrenia.
        Nat Rev Neurosci. 2005; 6: 312-324
        • Spencer K.M.
        • Nestor P.G.
        • Perlmutter R.
        • Niznikiewicz M.A.
        • Klump M.C.
        • Frumin M.
        • et al.
        Neural synchrony indexes disordered perception and cognition in schizophrenia.
        Proc Natl Acad Sci U S A. 2004; 101: 17288-17293
        • Uhlhaas P.J.
        • Singer W.
        Neural synchrony in brain disorders: Relevance for cognitive dysfunctions and pathophysiology.
        Neuron. 2006; 52: 155-168
        • Galambos R.
        • Makeig S.
        • Talmachoff J.
        A 40 Hz auditory potential recorded from the human scalp.
        Proc Natl Acad Sci U S A. 1981; 78: 2643-2647
        • Pastor M.A.
        • Artieda J.
        • Arbizu J.
        • Marti-Climent J.M.
        • Peñuelas I.
        • Masdeu J.C.
        Activation of human cerebral and cerebellar cortex by auditory stimulation at 40 Hz.
        J Neurosci. 2002; 22: 10501-10506
        • Brenner C.A.
        • Sporns O.
        • Lysaker P.H.
        • O'Donnell B.F.
        EEG synchronization to modulated auditory tones in schizophrenia, schizoaffective disorder, and schizotypal personality disorder.
        Am J Psychiatry. 2003; 160: 2238-2240
        • Hong L.E.
        • Summerfelt A.
        • McMahon R.
        • Adami H.
        • Francis G.
        • Elliott A.
        • et al.
        Evoked gamma band synchronization and the liability for schizophrenia.
        Schizophr Res. 2004; 70: 293-302
        • Kwon J.S.
        • O'Donnell B.F.
        • Wallenstein G.V.
        • Greene R.W.
        • Hirayasu Y.
        • Nestor P.G.
        • et al.
        Gamma frequency-range abnormalities to auditory stimulation in schizophrenia.
        Arch Gen Psychiatry. 1999; 56: 1001-1005
        • Light G.A.
        • Hsu J.L.
        • Hsieh M.H.
        • Meyer-Gomes K.
        • Sprock J.
        • Swerdlow N.R.
        • Braff D.L.
        Gamma band EEG oscillations reveal neural network cortical coherence dysfunction in schizophrenia patients.
        Biol Psychiatry. 2006; 60: 1231-1240
        • O'Donnell B.F.
        • Hetrick W.P.
        • Bodkins M.
        • Vohs J.L.
        • Bismark A.
        • Skosnik P.D.
        Event-related potential abnormalities in bipolar disorder: Relationship to symptoms, medication, and substance disorders.
        in: Kotlar B.M. New Developments in Mania Research. Nova Science Press, Hauppauge, New York2006: 115-133
        • O'Donnell B.F.
        • Hetrick W.P.
        • Vohs J.L.
        • Krishnan G.P.
        • Carroll C.A.
        • Shekhar A.
        Neural synchronization deficits to auditory stimulation in bipolar disorder.
        NeuroReport. 2004; 15: 1369-1372
        • Wilson T.W.
        • Hernandez O.
        • Asherin R.M.
        • Teale P.D.
        • Reite M.L.
        • Rojas D.C.
        Cortical gamma generators suggest abnormal auditory circuitry in early-onset psychosis.
        Cereb Cortex. 2008; 18: 371-378
        • Salisbury D.F.
        • Kuroki N.
        • Kasai K.
        • Shenton M.E.
        • McCarley R.W.
        Progressive and interrelated functional and structural evidence of post-onset brain reduction in schizophrenia.
        Arch Gen Psychiatry. 2007; 64: 521-529
        • Spitzer R.L.
        • Williams J.B.W.
        • Gibbon M.
        • First M.B.
        Structured Clinical Interview for DSM-III-R Non-Patient Edition (SCID-NP, Version 1.0).
        American Psychiatric Press, Washington DC1990
        • First M.B.
        • Gibbon M.
        • Spitzer R.L.
        • Williams J.B.W.
        Structured Clinical Interview for DSM-IV Axis II Personality Disorders (SCID-II).
        American Psychiatric Press, Washington DC1997
        • First M.B.
        • Spitzer R.L.
        • Gibbon M.
        • Williams J.B.W.
        Structured Clinical Interview for DSM-IV Axis I Disorders – Patient Edition.
        New York State Psychiatric Institute, New York1995
        • Oldfield R.C.
        The assessment and analysis of handedness: The Edinburgh inventory.
        Neuropsychologia. 1971; 9: 97-113
        • Hollingshead A.B.
        Two Factor Index of Social Position.
        Yale University Press, New Haven, Connecticut1965
        • Endicott J.
        • Spitzer R.L.
        • Fleiss J.L.
        • Cohen J.
        The Global Assessment Scale: A procedure for measuring overall severity of psychiatric disturbance.
        Arch Gen Psychiatry. 1976; 33: 766-771
        • Kay S.R.
        • Fiszbein A.
        • Opler L.A.
        The positive and negative syndrome scale (PANSS) for schizophrenia.
        Schizophr Bull. 1987; 13: 261-276
        • Stoll A.L.
        The Psychopharmacology Reference Card.
        McLean Hospital, Belmont, Massachusetts2001
        • Woods S.W.
        Chlorpromazine equivalent doses for the newer atypical antipsychotics.
        J Clin Psychiatry. 2003; 64: 663-667
        • Gratton G.
        • Coles M.G.H.
        • Donchin E.
        A new method for off-line removal of ocular artifact.
        Electroencephalogr Clin Neurophysiol. 1983; 75: 468-484
        • Tallon-Baudry C.
        • Bertrand O.
        Oscillatory gamma activity in humans and its role in object representation.
        Trends Cogn Sci. 1999; 3: 151-162
        • Keselman H.J.
        • Rogan J.C.
        Repeated measures F tests and psychophysiological research: Controlling the number of false positives.
        Psychophysiology. 1980; 17: 499-503
        • Salisbury D.F.
        • Shenton M.E.
        • Sherwood A.R.
        • Fischer I.A.
        • Yurgelun-Todd D.A.
        • Tohen M.
        • McCarley R.W.
        First episode schizophrenic psychosis differs from first episode affective psychosis and controls in P300 amplitude over left temporal lobe.
        Arch Gen Psychiatry. 1998; 55: 173-180
        • Salisbury D.F.
        • Shenton M.E.
        • McCarley R.W.
        P300 topography differs in schizophrenia and manic psychosis.
        Biol Psychiatry. 1999; 45: 99-106
        • Bruder G.
        • Kayser J.
        • Tenke C.
        • Amador X.
        • Friedman M.
        • Sharif Z.
        • Gorman J.
        Left temporal lobe dysfunction in schizophrenia: Event-related potential and behavioral evidence from phonetic and tonal dichotic listening tasks.
        Arch Gen Psychiatry. 1999; 56: 267-276
        • Shenton M.E.
        • Dickey C.C.
        • Frumin M.
        • McCarley R.W.
        A review of MRI findings in schizophrenia.
        Schizophr Res. 2001; 49: 1-52
        • Sommer I.
        • Aleman A.
        • Ramsey N.
        • Bouma A.
        • Kahn R.
        Handedness, language lateralisation and anatomical asymmetry in schizophrenia: Meta-analysis.
        Brit J Psychiatry. 2001; 178: 344-351
        • Spencer K.M.
        • McCarley R.W.
        Visual hallucinations, attention, and neural circuitry: Perspectives from schizophrenia research.
        Behav Brain Sci. 2005; 28: 774
        • Akbarian S.
        • Huang H.-S.
        Molecular and cellular mechanisms of altered GAD1/GAD67 expression in schizophrenia and related disorders.
        Brain Res Rev. 2006; 52: 293-304
        • Benes F.M.
        • Berretta S.
        GABAergic interneurons: Implications for understanding schizophrenia and bipolar disorder.
        Neuropsychopharmacol. 2001; 25: 1-27
        • Benes F.M.
        • Lim B.
        • Matzilevich D.
        • Walsh J.P.
        • Subburaju S.
        • Minns M.
        Regulation of the GABA cell phenotype in hippocampus of schizophrenics and bipolars.
        Proc Natl Acad Sci U S A. 2007; 104: 10164-10169
        • Torrey E.F.
        • Barci B.M.
        • Webster M.J.
        • Bartko J.J.
        • Meador-Woodruff J.H.
        • Knable M.B.
        Neurochemical markers for schizophrenia, bipolar disorder, and major depression in postmortem brains.
        Biol Psychiatry. 2005; 57: 252-260
        • Woo T.-U.
        • Walsh J.P.
        • Benes F.M.
        Density of glutamic acid decarboxylase 67 messenger RNA-containing neurons that express the N-methyl-D-aspartate receptor subunit NR2A in the anterior cingulate cortex in schizophrenia and bipolar disorder.
        Arch Gen Psychiatry. 2004; 61: 649-657
        • Gallinat J.
        • Winterer G.
        • Herrmann C.S.
        • Senkowski D.
        Reduced oscillatory gamma-band responses in unmedicated schizophrenic patients indicate impaired frontal network processing.
        Clin Neurophysiol. 2004; 115: 1863-1874
        • Symond M.B.
        • Harris A.W.F.
        • Gordon E.
        • Williams L.M.
        “Gamma synchrony” in first-episode schizophrenia: A disorder of temporal connectivity?.
        Am J Psychiatry. 2005; 162: 459-465
        • Lee K.-H.
        • Williams L.M.
        • Haig A.
        • Gordon E.
        Gamma (40 Hz) phase synchronicity and symptom dimensions in schizophrenia.
        Cognit Neuropsychiatry. 2003; 8: 57-71