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Integration of valence and conflict processing through cellular-field interactions in human subgenual cingulate during emotional face processing in treatment-resistant depression

Molecular Psychiatry (2024)Cite this article

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Abstract

The subgenual anterior cingulate cortex (sgACC) has been identified as a key brain area involved in various cognitive and emotional processes. While the sgACC has been implicated in both emotional valuation and emotional conflict monitoring, it is still unclear how this area integrates multiple functions. We characterized both single neuron and local field oscillatory activity in 14 patients undergoing sgACC deep brain stimulation for treatment-resistant depression. During recording, patients were presented with a modified Stroop task containing emotional face images that varied in valence and congruence. We further analyzed spike-field interactions to understand how network dynamics influence single neuron activity in this area. Most single neurons responded to both valence and congruence, revealing that sgACC neuronal activity can encode multiple processes within the same task, indicative of multifunctionality. During peak neuronal response, we observed increased spectral power in low frequency oscillations, including theta-band synchronization (4–8 Hz), as well as desynchronization in beta-band frequencies (13–30 Hz). Theta activity was modulated by current trial congruency with greater increases in spectral power following non-congruent stimuli, while beta desynchronizations occurred regardless of emotional valence. Spike-field interactions revealed that local sgACC spiking was phase-locked most prominently to the beta band, whereas phase-locking to the theta band occurred in fewer neurons overall but was modulated more strongly for neurons that were responsive to task. Our findings provide the first direct evidence of spike-field interactions relating to emotional cognitive processing in the human sgACC. Furthermore, we directly related theta oscillatory dynamics in human sgACC to current trial congruency, demonstrating it as an important regulator during conflict detection. Our data endorse the sgACC as an integrative hub for cognitive emotional processing through modulation of beta and theta network activity.

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Fig. 1: Schematic illustration of the modified emotional faces Stroop task and experimental protocol.
Fig. 2: Summary of single neuron responses.
Fig. 3: Oscillatory dynamics in response to task.
Fig. 4: Spike-field interactions in relation to task.

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Data availability

Data available upon reasonable request.

Code availability

All custom MATLAB R2022b (Mathworks) code used for data analysis is available upon reasonable request.

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Acknowledgements

Authors thank all participants. This project was funded by Alberta Innovates Health Solutions (AIHS, #04126-2017). AJG received funding through Natural Sciences and Engineering Research Council of Canada (NSERC) and New Frontiers in Research Fund (NFRF). DLC and ECB were both AIHS post-doctoral fellows and received additional funding from NSERC-CREATE. APA and NAZ also received funding from NSERC-CREATE. LHK received scholarships from Parkinson Canada, Parkinson Alberta and Eyes High, and MSN was funded by NSERC-CREATE and Parkinson Canada.

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ZHTK and RR: Alberta Innovates Health Solutions (AIHS, #04126-2017).

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Authors and Affiliations

  1. Hotchkiss Brain Institute, University of Calgary, Calgary, Canada

    Nicole A. Zalasky, Feng Luo, Linda H. Kim, M. Sohail Noor, Elliot C. Brown, Ana P. Arantes, Rajamannar Ramasubbu, Zelma H. T. Kiss & Darren L. Clark

  2. Department of Clinical Neurosciences, Cumming School of Medicine, University of Calgary, Calgary, Canada

    Nicole A. Zalasky, Feng Luo, Linda H. Kim, M. Sohail Noor, Elliot C. Brown, Ana P. Arantes, Rajamannar Ramasubbu, Zelma H. T. Kiss & Darren L. Clark

  3. Mathison Centre for Mental Health Research & Education, University of Calgary, Calgary, Canada

    Elliot C. Brown, Rajamannar Ramasubbu, Zelma H. T. Kiss & Darren L. Clark

  4. Department of Psychiatry, Cumming School of Medicine, University of Calgary, Calgary, Canada

    Elliot C. Brown, Rajamannar Ramasubbu, Zelma H. T. Kiss & Darren L. Clark

  5. Canadian Centre for Behavioural Neuroscience, Department of Neuroscience, University of Lethbridge, Lethbridge, Canada

    Aaron J. Gruber

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Contributions

NAZ, AJG, RR, ZHTK, and DLC contributed to study conceptualization and design. FL, LHK, MSN, ECB and DLC participated in data collection. NAZ, APA, AJG, ZHTK and DLC contributed to methodology and software. NAZ and DLC performed formal analysis. NAZ contributed to formal drafting of the original article, and all authors contributed to editing and review. RR, ZHTK and DLC contributed to project administration. ZHTK and DLC supplied resources and supervised all aspects of this study. Study funding was acquired by RR and ZHTK. All authors read and approved the final manuscript.

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Correspondence to Zelma H. T. Kiss.

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Zalasky, N.A., Luo, F., Kim, L.H. et al. Integration of valence and conflict processing through cellular-field interactions in human subgenual cingulate during emotional face processing in treatment-resistant depression. Mol Psychiatry (2024). https://doi.org/10.1038/s41380-024-02667-6

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