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Cited by 253Neural dynamics and brain functionSchizophrenia research and treatmentHallucinations in medical conditions

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Left auditory cortex gamma synchronization and auditory hallucination symptoms in schizophrenia

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Spencer, Kevin M, Niznikiewicz, Margaret A, Nestor, Paul G, Shenton, Martha E, McCarley, Robert W·2009·BMC Neuroscience
DOI 10.1186/1471-2202-10-85PMC PMC2719648
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Abstract

BACKGROUND: Oscillatory electroencephalogram (EEG) abnormalities may reflect neural circuit dysfunction in neuropsychiatric disorders. Previously we have found positive correlations between the phase synchronization of beta and gamma oscillations and hallucination symptoms in schizophrenia patients. These findings suggest that the propensity for hallucinations is associated with an increased tendency for neural circuits in sensory cortex to enter states of oscillatory synchrony. Here we tested this hypothesis by examining whether the 40 Hz auditory steady-state response (ASSR) generated in the left primary auditory cortex is positively correlated with auditory hallucination symptoms in schizophrenia. We also examined whether the 40 Hz ASSR deficit in schizophrenia was associated with cross-frequency interactions. Sixteen healthy control subjects (HC) and 18 chronic schizophrenia patients (SZ) listened to 40 Hz binaural click trains. The EEG was recorded from 60 electrodes and average-referenced offline. A 5-dipole model was fit from the HC grand average ASSR, with 2 pairs of superior temporal dipoles and a deep midline dipole. Time-frequency decomposition was performed on the scalp EEG and source data. RESULTS: Phase locking factor (PLF) and evoked power were reduced in SZ at fronto-central electrodes, replicating prior findings. PLF was reduced in SZ for non-homologous right and left hemisphere sources. Left hemisphere source PLF in SZ was positively correlated with auditory hallucination symptoms, and was modulated by delta phase. Furthermore, the correlations between source evoked power and PLF found in HC was reduced in SZ for the LH sources. CONCLUSION: These findings suggest that differential neural circuit abnormalities may be present in the left and right auditory cortices in schizophrenia. In addition, they provide further support for the hypothesis that hallucinations are related to cortical hyperexcitability, which is manifested by an increased propensity for high-frequency synchronization in modality-specific cortical areas.

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Figure 1 Analyses of scalp EEG data. (A) Time-frequency and topographic maps of phase locking factor (PLF) for healthy controls (HC) and schizophrenia patients (SZ). The time-frequency maps show responses at electrode Fz. Topographic maps are oriented so that the top of the map is anterior and the bottom is posterior. (B) Time-frequency and topographic maps of evoked power for HC and SZ, as in A. (C) Dipole model of the ASSR based on the HC grand average. Labels are for left hemisphere tangential (LH tan), left hemisphere radial (LH rad), right hemisphere tangential (RH tan), right hemisphere radial (RH rad), and Residual (Res) dipoles. (D) Global field power (blue) of the scalp ASSR and percent residual variance (%RV) of the dipole model (red). The period during which the dipole model was fit (30–550 ms) is shaded.
Figure 1 Analyses of scalp EEG data. (A) Time-frequency and topographic maps of phase locking factor (PLF) for healthy controls (HC) and schizophrenia patients (SZ). The time-frequency maps show responses at electrode Fz. Topographic maps are oriented so that the top of the map is anterior and the bottom is posterior. (B) Time-frequency and topographic maps of evoked power for HC and SZ, as in A. (C) Dipole model of the ASSR based on the HC grand average. Labels are for left hemisphere tangential (LH tan), left hemisphere radial (LH rad), right hemisphere tangential (RH tan), right hemisphere radial (RH rad), and Residual (Res) dipoles. (D) Global field power (blue) of the scalp ASSR and percent residual variance (%RV) of the dipole model (red). The period during which the dipole model was fit (30–550 ms) is shaded.CC BY · PubMed Central
Figure 2 PLF time-frequency maps of source activity for HC and SZ.
Figure 2 PLF time-frequency maps of source activity for HC and SZ.CC BY · PubMed Central
Figure 3 Evoked power time-frequency maps of source activity for HC and SZ.
Figure 3 Evoked power time-frequency maps of source activity for HC and SZ.CC BY · PubMed Central
Figure 4 Auditory hallucination correlations and cross-frequency interaction data. (A and B) Scatterplots of LH radial dipole PLF vs. Auditory Hallucination symptom ratings. The HC values are displayed for comparison with the range of SZ values. (A) LH radial dipole PLF over all trials (ρ = 0.541, p < 0.05). (B) LH radial dipole PLF in the 120–180° phase bin for 2 Hz modulation (ρ = 0.617, p < 0.01). (C and D) ASSR PLF plotted as a function of 2 Hz phase for the LH radial (C) and RH tangential (D) dipoles. HC = filled squares, SZ = open circles. In (C), the asterisk indicates the significant reduction of LH radial dipole PLF in SZ for the 120–180° phase bin.
Figure 4 Auditory hallucination correlations and cross-frequency interaction data. (A and B) Scatterplots of LH radial dipole PLF vs. Auditory Hallucination symptom ratings. The HC values are displayed for comparison with the range of SZ values. (A) LH radial dipole PLF over all trials (ρ = 0.541, p < 0.05). (B) LH radial dipole PLF in the 120–180° phase bin for 2 Hz modulation (ρ = 0.617, p < 0.01). (C and D) ASSR PLF plotted as a function of 2 Hz phase for the LH radial (C) and RH tangential (D) dipoles. HC = filled squares, SZ = open circles. In (C), the asterisk indicates the significant reduction of LH radial dipole PLF in SZ for the 120–180° phase bin.CC BY · PubMed Central

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  1. Stoll AL: The Psychopharmacology Reference Card. 2001, Belmont, Massachusetts, McLean Hospital

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Metadata

Authors
Spencer, K. M., Niznikiewicz, M. A., Nestor, P. G., Shenton, M. E., & McCarley, R. W.
Affiliations
  • Harvard University (US)
  • Brigham and Women's Hospital (US)
Corresponding author
Spencer, Kevin M
ORCID
Venue
BMC Neuroscience
Publisher
Springer Science and Business Media LLC
Published
2009-07-20
Volume
10
Issue
1
Pages
85-85
ISSN
1471-2202 (ISSN-L)
DOI
10.1186/1471-2202-10-85
PMC
PMC2719648
OpenAlex
W2124019844
Cited by
253
References
79
Citations by year
2026: 6 · 2025: 6 · 2024: 12 · 2023: 16 · 2022: 17 · 2021: 16 · 2020: 13 · 2019: 11 · 2018: 13 · 2017: 17 · 2016: 16 · 2015: 23 · 2014: 20 · 2013: 22 · 2012: 18
FWCI
7.26
Type
journal article
Language
en
Open access
Licence
Locations
  • BMC Neuroscience (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • U.S. Department of Veterans Affairs (R01 MH080187, I01 CX000154)
  • National Alliance for Research on Schizophrenia and Depression
  • U.S. Public Health Service (R0140799, R03 076760)
  • National Institute of Mental Health (MH080187, R01MH080187)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
  • Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Hallucinations in medical conditions
Keywords
schizophrenia, auditory hallucinations, gamma oscillations, 40 Hz auditory steady-state response, cross-frequency coupling, delta phase, cortical hyperexcitability
MeSH terms
Adult, Auditory Cortex, Brain Mapping, Electroencephalography, Evoked Potentials, Auditory, Hallucinations, Humans, Functional Laterality, Male, Middle Aged, Schizophrenia, Signal Processing, Computer-Assisted

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