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Perceived stress modulates the activity between the amygdala and the cortex

Molecular Psychiatry volume 27, pages 4939–4947 (2022)Cite this article

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Abstract

The significant link between stress and psychiatric disorders has prompted research on stress’s impact on the brain. Interestingly, previous studies on healthy subjects have demonstrated an association between perceived stress and amygdala volume, although the mechanisms by which perceived stress can affect brain function remain unknown. To better understand what this association entails at a functional level, herein, we explore the association of perceived stress, measured by the PSS10 questionnaire, with disseminated functional connectivity between brain areas. Using resting-state fMRI from 252 healthy subjects spanning a broad age range, we performed both a seed-based amygdala connectivity analysis (static connectivity, with spatial resolution but no temporal definition) and a whole-brain data-driven approach to detect altered patterns of phase interactions between brain areas (dynamic connectivity with spatiotemporal information). Results show that increased perceived stress is directly associated with increased amygdala connectivity with frontal cortical regions, which is driven by a reduced occurrence of an activity pattern where the signals in the amygdala and the hippocampus evolve in opposite directions with respect to the rest of the brain. Overall, these results not only reinforce the pathological effect of in-phase synchronicity between subcortical and cortical brain areas but also demonstrate the protective effect of counterbalanced (i.e., phase-shifted) activity between brain subsystems, which are otherwise missed with correlation-based functional connectivity analysis.

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Fig. 1: Results from the static connectivity: Positive association of right amygdala seed-based connectivity with PSS10 scores.
Fig. 2: Lower perceived stress relates to more counterbalanced activity between amygdala-hippocampus and the rest of the brain.

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Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

Code availability

FSL software is available by the authors at https://fsl.fmrib.ox.ac.uk/fsl/fslwiki/FslInstallation and LEiDA scripts at GitHub (https://github.com/juanitacabral/LEiDA).

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Acknowledgements

This work was funded by National funds, through the Foundation for Science and Technology (FCT) [projects UIDB/50026/2020, UIDP/50026/2020, PTDC/MED-NEU/29071/2017]; by BIAL foundation [grants PT/FB/BL-2016-206, BIAL 30-16]; Fundação Calouste Gulbenkian [contract grant P-139977]; and the European Commission (FP7) [contract HEALTH-F2-2010-259772]. Fellowship grants supported IC, LA, and AC through the FCT [grants number SFRH/BD/133006/2017, SFRH/BD/101398/2014, NORTE-08-5369-FSE-000041] from the Health Science program. JC is funded by FCT grant CEECIND/03325/2017.

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Authors and Affiliations

  1. Life and Health Sciences Research Institute (ICVS), School of Medicine, University of Minho, 4710-057, Braga, Portugal

    Inês Caetano, Sónia Ferreira, Ana Coelho, Liliana Amorim, Teresa Costa Castanho, Carlos Portugal-Nunes, José Miguel Soares, Nuno Gonçalves, Rui Sousa, Joana Reis, Catarina Lima, Paulo Marques, Pedro Silva Moreira, Ana João Rodrigues, Nadine Correia Santos, Pedro Morgado, Ricardo Magalhães, Maria Picó-Pérez, Joana Cabral & Nuno Sousa

  2. ICVS/3B’s, PT Government Associate Laboratory, 4710-057, Braga/Guimarães, Portugal

    Inês Caetano, Sónia Ferreira, Ana Coelho, Liliana Amorim, Teresa Costa Castanho, Carlos Portugal-Nunes, José Miguel Soares, Nuno Gonçalves, Rui Sousa, Joana Reis, Catarina Lima, Paulo Marques, Pedro Silva Moreira, Ana João Rodrigues, Nadine Correia Santos, Pedro Morgado, Ricardo Magalhães, Maria Picó-Pérez, Joana Cabral & Nuno Sousa

  3. Clinical Academic Center—Braga (2CA), 4710-243, Braga, Portugal

    Inês Caetano, Sónia Ferreira, Ana Coelho, Liliana Amorim, Teresa Costa Castanho, Carlos Portugal-Nunes, José Miguel Soares, Nuno Gonçalves, Rui Sousa, Joana Reis, Catarina Lima, Paulo Marques, Pedro Silva Moreira, Ana João Rodrigues, Nadine Correia Santos, Pedro Morgado, Ricardo Magalhães, Maria Picó-Pérez, Joana Cabral & Nuno Sousa

  4. Association P5 Digital Medical Center (ACMP5), 4710-057, Braga, Portugal

    Liliana Amorim, Teresa Costa Castanho & Nuno Sousa

  5. CECAV—Veterinary and Animal Science Research Centre, Quinta de Prados, 5000-801, Vila Real, Portugal

    Carlos Portugal-Nunes

  6. Departamento de Psiquiatria e Saúde Mental, Centro Hospitalar Tondela-Viseu, 3500-228, Viseu, Portugal

    Rui Sousa

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  1. Inês Caetano
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Contributions

Conceptualization: IC, NS. Methodology: IC, SF, JC, NS. Software: IC, SF, JC. Validation: IC, LA, TCC, CL, MPP, JC. Formal analysis: IC, SF, JC. Investigation: LA, TCC, AC, SF, CPN, JMS, NG, RS, JR, PMarques, PSM, AJR, PM, RM, MPP. Resources: AJR, NCS, PM, NS. Data Curation: AC, RM. Writing - Original Draft: IC. Writing—Review & Editing: JC, NS. Visualization: IC, JC, NS. Supervision: NS. Project administration: NS. Funding acquisition: AJR, NCS, PM, NS.

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Correspondence to Nuno Sousa.

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Caetano, I., Ferreira, S., Coelho, A. et al. Perceived stress modulates the activity between the amygdala and the cortex. Mol Psychiatry 27, 4939–4947 (2022). https://doi.org/10.1038/s41380-022-01780-8

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