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Abstract

Objective:

Brain oscillations play a pivotal role in synchronizing responses of local and global ensembles of neurons. Patients with schizophrenia exhibit impairments in oscillatory response, which are thought to stem from abnormal maturation during critical developmental stages. Studying individuals at genetic risk for psychosis, such as 22q11.2 deletion carriers, from childhood to adulthood may provide insights into developmental abnormalities.

Methods:

The authors acquired 106 consecutive T1-weighted MR images and 40-Hz auditory steady-state responses (ASSRs) with high-density (256 channel) EEG in a group of 58 22q11.2 deletion carriers and 48 healthy control subjects. ASSRs were analyzed with 1) time-frequency analysis using Morlet wavelet decomposition, 2) intertrial phase coherence (ITPC), and 3) theta-gamma phase-amplitude coupling estimated in the source space between brain regions activated by the ASSRs. Additionally, volumetric analyses were performed with FreeSurfer. Subanalyses were conducted in deletion carriers who endorsed psychotic symptoms and in subgroups with different age bins.

Results:

Deletion carriers had decreased theta and late-latency 40-Hz ASSRs and phase synchronization compared with control subjects. Deletion carriers with psychotic symptoms displayed a further reduction of gamma-band response, decreased ITPC, and decreased top-down modulation of gamma-band response in the auditory cortex. Reduced gamma-band response was correlated with the atrophy of auditory cortex in individuals with psychotic symptoms. In addition, a linear increase of theta and gamma power from childhood to adulthood was found in control subjects but not in deletion carriers.

Conclusions:

The results suggest that while all deletion carriers exhibit decreased gamma-band response, more severe local and long-range communication abnormalities are associated with the emergence of psychotic symptoms and gray matter loss. Additionally, the lack of age-related changes in deletion carriers indexes a potential developmental impairment in circuits underlying the maturation of neural oscillations during adolescence. The progressive disruption of gamma-band response in 22q11.2 deletion syndrome supports a developmental perspective toward understanding and treating psychotic disorders.

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Information & Authors

Information

Published In

Go to American Journal of Psychiatry
Go to American Journal of Psychiatry
American Journal of Psychiatry
Pages: 204 - 215
PubMed: 35236117

History

Received: 19 February 2021
Revision received: 14 June 2021
Revision received: 29 July 2021
Revision received: 15 September 2021
Accepted: 29 September 2021
Published in print: March 2022
Published online: 3 March 2022

Keywords

  1. Gamma-Band Oscillations
  2. Theta-Band Oscillations
  3. Psychosis
  4. Phase-Amplitude Coupling
  5. Adolescence
  6. 22q11DS

Authors

Details

Valentina Mancini, M.D. [email protected]
Developmental Imaging and Psychopathology Laboratory (Mancini, Schneider, Eliez) and Department of Genetic Medicine and Development (Eliez), University of Geneva School of Medicine, Geneva; Functional Brain Mapping Laboratory, Department of Basic Neurosciences, University of Geneva, Geneva (Rochas, Seeber, Roehri, Rihs, Ferat, Michel); Clinical Psychology Unit for Intellectual and Developmental Disabilities, Faculty of Psychology and Educational Sciences, University of Geneva, Geneva (Schneider); Institute of Neuroscience and Psychology, University of Glasgow, Glasgow, Scotland (Uhlhaas); Department of Child and Adolescent Psychiatry, Psychosomatic Medicine and Psychotherapy, Charité Universitätsmedizin, Berlin (Uhlhaas); Center for Biomedical Imaging (CIBM) of Lausanne and Geneva (Michel).
Vincent Rochas, Ph.D.
Developmental Imaging and Psychopathology Laboratory (Mancini, Schneider, Eliez) and Department of Genetic Medicine and Development (Eliez), University of Geneva School of Medicine, Geneva; Functional Brain Mapping Laboratory, Department of Basic Neurosciences, University of Geneva, Geneva (Rochas, Seeber, Roehri, Rihs, Ferat, Michel); Clinical Psychology Unit for Intellectual and Developmental Disabilities, Faculty of Psychology and Educational Sciences, University of Geneva, Geneva (Schneider); Institute of Neuroscience and Psychology, University of Glasgow, Glasgow, Scotland (Uhlhaas); Department of Child and Adolescent Psychiatry, Psychosomatic Medicine and Psychotherapy, Charité Universitätsmedizin, Berlin (Uhlhaas); Center for Biomedical Imaging (CIBM) of Lausanne and Geneva (Michel).
Martin Seeber, Ph.D.
Developmental Imaging and Psychopathology Laboratory (Mancini, Schneider, Eliez) and Department of Genetic Medicine and Development (Eliez), University of Geneva School of Medicine, Geneva; Functional Brain Mapping Laboratory, Department of Basic Neurosciences, University of Geneva, Geneva (Rochas, Seeber, Roehri, Rihs, Ferat, Michel); Clinical Psychology Unit for Intellectual and Developmental Disabilities, Faculty of Psychology and Educational Sciences, University of Geneva, Geneva (Schneider); Institute of Neuroscience and Psychology, University of Glasgow, Glasgow, Scotland (Uhlhaas); Department of Child and Adolescent Psychiatry, Psychosomatic Medicine and Psychotherapy, Charité Universitätsmedizin, Berlin (Uhlhaas); Center for Biomedical Imaging (CIBM) of Lausanne and Geneva (Michel).
Nicolas Roehri, Ph.D.
Developmental Imaging and Psychopathology Laboratory (Mancini, Schneider, Eliez) and Department of Genetic Medicine and Development (Eliez), University of Geneva School of Medicine, Geneva; Functional Brain Mapping Laboratory, Department of Basic Neurosciences, University of Geneva, Geneva (Rochas, Seeber, Roehri, Rihs, Ferat, Michel); Clinical Psychology Unit for Intellectual and Developmental Disabilities, Faculty of Psychology and Educational Sciences, University of Geneva, Geneva (Schneider); Institute of Neuroscience and Psychology, University of Glasgow, Glasgow, Scotland (Uhlhaas); Department of Child and Adolescent Psychiatry, Psychosomatic Medicine and Psychotherapy, Charité Universitätsmedizin, Berlin (Uhlhaas); Center for Biomedical Imaging (CIBM) of Lausanne and Geneva (Michel).
Tonia A. Rihs, Ph.D.
Developmental Imaging and Psychopathology Laboratory (Mancini, Schneider, Eliez) and Department of Genetic Medicine and Development (Eliez), University of Geneva School of Medicine, Geneva; Functional Brain Mapping Laboratory, Department of Basic Neurosciences, University of Geneva, Geneva (Rochas, Seeber, Roehri, Rihs, Ferat, Michel); Clinical Psychology Unit for Intellectual and Developmental Disabilities, Faculty of Psychology and Educational Sciences, University of Geneva, Geneva (Schneider); Institute of Neuroscience and Psychology, University of Glasgow, Glasgow, Scotland (Uhlhaas); Department of Child and Adolescent Psychiatry, Psychosomatic Medicine and Psychotherapy, Charité Universitätsmedizin, Berlin (Uhlhaas); Center for Biomedical Imaging (CIBM) of Lausanne and Geneva (Michel).
Victor Ferat, M.S.
Developmental Imaging and Psychopathology Laboratory (Mancini, Schneider, Eliez) and Department of Genetic Medicine and Development (Eliez), University of Geneva School of Medicine, Geneva; Functional Brain Mapping Laboratory, Department of Basic Neurosciences, University of Geneva, Geneva (Rochas, Seeber, Roehri, Rihs, Ferat, Michel); Clinical Psychology Unit for Intellectual and Developmental Disabilities, Faculty of Psychology and Educational Sciences, University of Geneva, Geneva (Schneider); Institute of Neuroscience and Psychology, University of Glasgow, Glasgow, Scotland (Uhlhaas); Department of Child and Adolescent Psychiatry, Psychosomatic Medicine and Psychotherapy, Charité Universitätsmedizin, Berlin (Uhlhaas); Center for Biomedical Imaging (CIBM) of Lausanne and Geneva (Michel).
Maude Schneider, Ph.D.
Developmental Imaging and Psychopathology Laboratory (Mancini, Schneider, Eliez) and Department of Genetic Medicine and Development (Eliez), University of Geneva School of Medicine, Geneva; Functional Brain Mapping Laboratory, Department of Basic Neurosciences, University of Geneva, Geneva (Rochas, Seeber, Roehri, Rihs, Ferat, Michel); Clinical Psychology Unit for Intellectual and Developmental Disabilities, Faculty of Psychology and Educational Sciences, University of Geneva, Geneva (Schneider); Institute of Neuroscience and Psychology, University of Glasgow, Glasgow, Scotland (Uhlhaas); Department of Child and Adolescent Psychiatry, Psychosomatic Medicine and Psychotherapy, Charité Universitätsmedizin, Berlin (Uhlhaas); Center for Biomedical Imaging (CIBM) of Lausanne and Geneva (Michel).
Peter J. Uhlhaas, Ph.D.
Developmental Imaging and Psychopathology Laboratory (Mancini, Schneider, Eliez) and Department of Genetic Medicine and Development (Eliez), University of Geneva School of Medicine, Geneva; Functional Brain Mapping Laboratory, Department of Basic Neurosciences, University of Geneva, Geneva (Rochas, Seeber, Roehri, Rihs, Ferat, Michel); Clinical Psychology Unit for Intellectual and Developmental Disabilities, Faculty of Psychology and Educational Sciences, University of Geneva, Geneva (Schneider); Institute of Neuroscience and Psychology, University of Glasgow, Glasgow, Scotland (Uhlhaas); Department of Child and Adolescent Psychiatry, Psychosomatic Medicine and Psychotherapy, Charité Universitätsmedizin, Berlin (Uhlhaas); Center for Biomedical Imaging (CIBM) of Lausanne and Geneva (Michel).
Stephan Eliez, M.D.
Developmental Imaging and Psychopathology Laboratory (Mancini, Schneider, Eliez) and Department of Genetic Medicine and Development (Eliez), University of Geneva School of Medicine, Geneva; Functional Brain Mapping Laboratory, Department of Basic Neurosciences, University of Geneva, Geneva (Rochas, Seeber, Roehri, Rihs, Ferat, Michel); Clinical Psychology Unit for Intellectual and Developmental Disabilities, Faculty of Psychology and Educational Sciences, University of Geneva, Geneva (Schneider); Institute of Neuroscience and Psychology, University of Glasgow, Glasgow, Scotland (Uhlhaas); Department of Child and Adolescent Psychiatry, Psychosomatic Medicine and Psychotherapy, Charité Universitätsmedizin, Berlin (Uhlhaas); Center for Biomedical Imaging (CIBM) of Lausanne and Geneva (Michel).
Christoph M. Michel, Ph.D.
Developmental Imaging and Psychopathology Laboratory (Mancini, Schneider, Eliez) and Department of Genetic Medicine and Development (Eliez), University of Geneva School of Medicine, Geneva; Functional Brain Mapping Laboratory, Department of Basic Neurosciences, University of Geneva, Geneva (Rochas, Seeber, Roehri, Rihs, Ferat, Michel); Clinical Psychology Unit for Intellectual and Developmental Disabilities, Faculty of Psychology and Educational Sciences, University of Geneva, Geneva (Schneider); Institute of Neuroscience and Psychology, University of Glasgow, Glasgow, Scotland (Uhlhaas); Department of Child and Adolescent Psychiatry, Psychosomatic Medicine and Psychotherapy, Charité Universitätsmedizin, Berlin (Uhlhaas); Center for Biomedical Imaging (CIBM) of Lausanne and Geneva (Michel).

Notes

Send correspondence to Dr. Mancini ([email protected]).

Author Contributions

The last two authors contributed equally.

Funding Information

Supported by research grants from the Swiss National Science Foundation (grants 324730-144260 and 320030-179404 to Dr. Eliez and grant 320030-184677 to Dr. Michel) and a National Center of Competence in Research Synapsy grant (grant 51NF40-185897 to Dr. Eliez and Dr. Michel).Dr. Uhlhaas has received research support from Eli Lilly and Lundbeck. The other authors report no financial relationships with commercial interests.

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