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Gamma oscillations of visual cortex underlying emotion and cognition deficits associated with suicide attempt in major depressive disorder

Nature Mental Health volume 2, pages 924–934 (2024)Cite this article

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Abstract

Altered neural oscillations in response to negative or positive emotional stimuli may be related to severe clinical symptoms in patients with major depressive disorder, particularly high suicidality. However, the underlying neurobiological mechanisms of this aberrant oscillatory activity and its potential emotional and cognitive functions remain unclear. Here we conducted a cross-sectional study of 107 participants, including 40 healthy controls and 67 patients with major depressive disorder (33 with suicide attempts and 34 without). All participants underwent an emotional expression recognition task during the magnetoencephalography scanning and completed neurocognitive assessments. Time–frequency characteristics and phase connections were analysed and compared between groups in sensor and source space using cluster-based permutation tests. The association between abnormal oscillatory features and neurocognitive performance was also evaluated. We found that increased gamma oscillations (50–70 Hz) of the visual cortices were considerably associated with suicide attempts in depression. Moreover, gamma-band source power in happy or sad conditions could predict individualized suicide risk. Gamma-band phase connections under the happy or sad condition were related to deficits in large-scale cognitive functions. Overall, gamma oscillations of the visual areas induced by the emotional stimuli were reliable biomarkers for identifying suicide attempts in depressive patients. Abnormal gamma-band connection involving visual cortex under both happy and sad expressions were significantly correlated with broad cognitive deficits.

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Fig. 1: Task paradigm and a flowchart of data analysis.
Fig. 2: Behavior data and neurocognitive assessments.
Fig. 3: Gamma oscillations at the sensor level across the SA, NSA and HC groups.
Fig. 4: Gamma oscillations at the source level across the SA, NSA and HC groups.
Fig. 5: Statistical analyses related to SA and neurocognitive function.

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Data availability

The data that support the key findings are available from the Open Science Framework (https://osf.io/q5zyg/). For any inquiries regarding the data, requests can be made to the corresponding authors.

Code availability

MEG data were preprocessed and analysed with the MATLAB r2016b based Fieldtrip (v.2017) toolbox (https://github.com/fieldtrip/fieldtrip)55. The sample size was estimated with G*Power_3.1.9.7 software (https://www.psychologie.hhu.de/arbeitsgruppen/allgemeine-psychologie-und-arbeitspsychologie/gpower)47. The statistical comparisons involving demographic variables, behavioral data were conducted with SPSS software (v.22)59. The data distribution plots were conducted with GraphPad Prism software (8.0.2)60. The brain maps were plotted with the BrainNet Viewer (v.2017) toolbox (https://github.com/mingruixia/BrainNet-Viewer)32. The custom codes are available from the Open Science Framework (https://osf.io/q5zyg/).

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Acknowledgements

This research received support from the National Natural Science Foundation of China (grants 81871066, 81571639 and 81701784) awarded to Q.L.; the Fundamental Research Funds for the Central Universities (2242021k30014, 2242021k30059) awarded to Q.L.; the Jiangsu Provincial Medical Innovation Team of the Project of Invigorating Health Care through Science, Technology, and Education (grant CXTDC2016004) awarded to Z.Y.; and the Jiangsu Provincial key research and development program (grant BE2018609) awarded to Z.Y.; Z.D. was supported by the Chinese Scholarship Council. We are grateful to O. Jensen from the University of Birmingham and H. Jiang from Zhejiang University for their valuable comments on this work. We would also like to express our appreciation to Y. Pan and T. Ghafari from the University of Birmingham for their helpful suggestions. Additionally, we acknowledge the editing and proofreading services provided by American Journal Experts, which substantially contributed to improving the clarity and language of this paper.

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Authors and Affiliations

  1. School of Biological Sciences and Medical Engineering, Child Development and Learning Science, Key Laboratory of Child Development and Learning Science, Ministry of Education, Research Center for Learning Science, Southeast University, Nanjing, China

    Zhongpeng Dai, Wei Zhang, Zhijian Yao & Qing Lu

  2. Centre for Human Brain Health, School of Psychology, University of Birmingham, Birmingham, UK

    Zhongpeng Dai

  3. Department of Psychiatry, Affiliated Brain Hospital of Nanjing Medical University, Nanjing, China

    Hongliang Zhou, Zhilu Chen & Zhijian Yao

  4. Institutes Sciences Cognitives Marc Jeannerod, CNRS UMR 5229, Lyon, France

    Siqi Zhang

  5. Nanjing Brain Hospital, Medical School of Nanjing University, Nanjing, China

    Zhijian Yao

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Contributions

Q.L. and Z.Y. were responsible for conceptualization. Z.D., W.Z. and S.Z. were responsible for methodology. Z.D., H.Z. and W.Z. were responsible for formal analysis. Z.D., H.Z., Z.C. and W.Z. were responsible for investigation. Z.D. wrote the orignal draft; Z.D., Q.L., H.Z. and S.Z. reviewed and edited the paper. Z.D. was responsible for visualization. Q.L. and Z.Y. supervised the project and acquired funding.

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Correspondence to Zhijian Yao or Qing Lu.

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Dai, Z., Zhang, W., Zhou, H. et al. Gamma oscillations of visual cortex underlying emotion and cognition deficits associated with suicide attempt in major depressive disorder. Nat. Mental Health 2, 924–934 (2024). https://doi.org/10.1038/s44220-024-00269-3

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