Facing emotions: real-time fMRI-based neurofeedback using dynamic emotional faces to modulate amygdala activity

Apurva Watve; Amelie Haugg; Nada Frei; Yury Koush; David Willinger; Annette Beatrix Bruehl; Philipp Stämpfli; Frank Scharnowski; Ronald Sladky

doi:10.3389/fnins.2023.1286665

Facing emotions: real-time fMRI-based neurofeedback using dynamic emotional faces to modulate amygdala activity

Front Neurosci. 2024 Jan 11:17:1286665. doi: 10.3389/fnins.2023.1286665. eCollection 2023.

Authors

Apurva Watve¹, Amelie Haugg², Nada Frei², Yury Koush³, David Willinger^{2

4

5}, Annette Beatrix Bruehl^{1

6}, Philipp Stämpfli¹, Frank Scharnowski^{1

5

7

8}, Ronald Sladky^{1

9}

Affiliations

¹ Department of Psychiatry, Psychotherapy, and Psychosomatics, Psychiatric University Hospital, University of Zürich, Zürich, Switzerland.
² Department of Child and Adolescent Psychiatry, Psychiatric Hospital, University of Zürich, Zürich, Switzerland.
³ Magnetic Resonance Research Center (MRRC), Department of Radiology and Biomedical Imaging, Yale University, New Haven, CT, United States.
⁴ Division of Psychodynamics, Department of Psychology and Psychodynamics, Karl Landsteiner University of Health Sciences, Krems an der Donau, Lower Austria, Austria.
⁵ Neuroscience Center Zürich, University of Zürich and Swiss Federal Institute of Technology, Zürich, Switzerland.
⁶ Center for Affective, Stress and Sleep Disorders, Psychiatric University Hospital Basel, Basel, Switzerland.
⁷ Zurich Center for Integrative Human Physiology, Faculty of Medicine, University of Zürich, Zürich, Switzerland.
⁸ Department of Cognition, Emotion, and Methods in Psychology, Faculty of Psychology, University of Vienna, Vienna, Austria.
⁹ Social, Cognitive and Affective Neuroscience Unit, Department of Basic Psychological Research and Research Methods, Faculty of Psychology, University of Vienna, Vienna, Austria.

Abstract

Introduction: Maladaptive functioning of the amygdala has been associated with impaired emotion regulation in affective disorders. Recent advances in real-time fMRI neurofeedback have successfully demonstrated the modulation of amygdala activity in healthy and psychiatric populations. In contrast to an abstract feedback representation applied in standard neurofeedback designs, we proposed a novel neurofeedback paradigm using naturalistic stimuli like human emotional faces as the feedback display where change in the facial expression intensity (from neutral to happy or from fearful to neutral) was coupled with the participant's ongoing bilateral amygdala activity.

Methods: The feasibility of this experimental approach was tested on 64 healthy participants who completed a single training session with four neurofeedback runs. Participants were assigned to one of the four experimental groups (n = 16 per group), i.e., happy-up, happy-down, fear-up, fear-down. Depending on the group assignment, they were either instructed to "try to make the face happier" by upregulating (happy-up) or downregulating (happy-down) the amygdala or to "try to make the face less fearful" by upregulating (fear-up) or downregulating (fear-down) the amygdala feedback signal.

Results: Linear mixed effect analyses revealed significant amygdala activity changes in the fear condition, specifically in the fear-down group with significant amygdala downregulation in the last two neurofeedback runs as compared to the first run. The happy-up and happy-down groups did not show significant amygdala activity changes over four runs. We did not observe significant improvement in the questionnaire scores and subsequent behavior. Furthermore, task-dependent effective connectivity changes between the amygdala, fusiform face area (FFA), and the medial orbitofrontal cortex (mOFC) were examined using dynamic causal modeling. The effective connectivity between FFA and the amygdala was significantly increased in the happy-up group (facilitatory effect) and decreased in the fear-down group. Notably, the amygdala was downregulated through an inhibitory mechanism mediated by mOFC during the first training run.

Discussion: In this feasibility study, we intended to address key neurofeedback processes like naturalistic facial stimuli, participant engagement in the task, bidirectional regulation, task congruence, and their influence on learning success. It demonstrated that such a versatile emotional face feedback paradigm can be tailored to target biased emotion processing in affective disorders.

Keywords: amygdala; dynamic faces; emotion regulation; neurofeedback; real-time fMRI.

Grants and funding

The author(s) declare financial support was received for the research, authorship, and/or publication of this article. This study was supported by the Swiss National Science Foundation (BSSG10_155915, 100014_178841, and 32003B_166566), the Foundation for Research in Science and the Humanities at the University of Zurich (STWF-17-012), and the Baugarten Stiftung.