Resolving temporal threat uncertainty by observational learning involves the amygdala, hippocampus and anterior insula

By observing others’ experiences, humans learn about threats while avoiding firsthand dangers. Yet, previous neuroscience research has focused on observational threats that are predictable. In firsthand learning, temporally predictable and unpredictable threats can be mechanistically discerned.

In this study, we developed a novel observational paradigm in which participants learned from predictable and unpredictable observational threats, as well as a no-threat condition. Participants encountered the same conditions during an expression phase to investigate how the brain encodes predictive and unpredictive threat cues observed in others. Participants in Experiment 1 (n = 20, 14 female, 6 male) and Experiment 2 (n = 23, 9 female, 1 non-binary, 13 male) successfully learned threat contingencies, showing heightened threat expectations for predictive cues and unpredictable condition-onsets.

Behavioral findings converged with neural (fMRI, Experiment 2) responses in the anterior insula during the expression phase. Reflecting the dynamic process of learning, amygdala activation in response to predictive threat cues displayed a linear decrease across trials. Interestingly, BOLD responses to others’ pain that was predictable, were enhanced within the amygdala, insula and hippocampus, compared to unpredictable conditions.

Our findings suggest that humans can learn to resolve temporal threat uncertainty, through the observation of others. The present work thereby contributes to understanding the social aspects of fear and anxiety disorders. The work was funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) as part of the Research Training Group „Emotional learning and memory” GRK 2753 (L.R and C.B.), Project-ID: 449640848 Project A02, the Collaborative Research Center “Treatment Expectation“ SFB 289 (S.K., L.H.) Project-ID 422744262 - TRR 289 Project A18, and the Research Unit “Contextual influences on dynamic belief updating in volatile environments “ FOR5389 Project-ID: 461947532 all awarded to J.H.

Open Access funding enabled and organized by Projekt DEAL. Department of Systems Neuroscience, University Medical Center Hamburg-Eppendorf, 20246, Hamburg, Germany Simon Knobloch, Theresa Jansen, Lara Caroline Hille, Madeleine Müller, Leonie Rumpf, Christian Francis Lewis Bauer & Jan Haaker Department of General Psychology and Cognitive Neuroscience, Charlotte Fresenius University, 20148, Hamburg, Germany The authors declare no competing interests. Study procedures were in line with the Declaration of Helsinki [22].

The ethics committee of the Hamburg medical chamber approved the study (2023-101155-BO-ff). All participants gave written informed consent to participate in the study. The demonstrator visible in the videos gave written informed consent to the publication of images from the videos.