Extinction and subsequent updating of innate fear responses to a visual looming stimulus rely on hippocampus-dependent mechanisms
Animals rely on innate and learned behavior to respond to their environment, but how the brain balances hardwired responses with adaptive flexibility remains unclear. Here, we demonstrate that innate looming stimulus responses in Mus musculus can be attenuated via repeated unreinforced presentation. This attenuation is long-lasting and generalizing, but is rapidly recovered when the stimulus is paired with an electric foot-shock. Fiber photometry recordings reveal attenuation of responses to visual looming stimuli in the SC and PAG, which do not recover following recovery of behavioral responses. Analysis of c-Fos expression uncovered a ventral CA1 (vCA1) ensemble that is active during both innate and learned looming fear responses. We report that this vCA1 engram is not necessary for innate defensive behavior but is necessary for learned fear responses. These findings reveal a novel role of the hippocampus in adapting to looming stimuli, and provide a platform for understanding the interaction of memory and instinct.
Authors
- Paul Conway (ORCID: https://orcid.org/0000-0003-0802-4245)
- Gisella Vetere (ORCID: https://orcid.org/0000-0002-4595-4284)
- Tomás J. Ryan (ORCID: https://orcid.org/0000-0003-0121-8514)
- James D. O’Leary (ORCID: https://orcid.org/0000-0001-9801-5312)
- Stephen M. Winston (ORCID: https://orcid.org/0000-0002-8809-9900)
- Clara Ortega‐de San Luis (ORCID: https://orcid.org/0000-0002-8365-2762)
- Livia Autore
- Andrea Zamora (ORCID: https://orcid.org/0000-0002-6260-2862)
- Antoine Harel (ORCID: https://orcid.org/0000-0002-9972-0491)
- Mark A. Brimble (ORCID: https://orcid.org/0000-0001-7182-9818)
- Zijun Wang (ORCID: https://orcid.org/0000-0002-2095-2151)
- Armn A. Tavallaei
Institutions
- Canadian Institute for Advanced Research (CA)
- Centre National de la Recherche Scientifique (FR)
- St. Jude Children's Research Hospital (US)
- The University of Melbourne (AU)
- Georgetown University (US)
- Universidad de Jaén (ES)
- Trinity College Dublin (IE)
- Florey Institute of Neuroscience and Mental Health (AU)
- Université Paris Sciences et Lettres (FR)
- Georgetown University Medical Center (US)
- ESPCI Paris (FR)
Publication Details
- Journal
- PLoS Biology
- Published
- 2025-09-24
- DOI
- https://doi.org/10.1371/journal.pbio.3003391
- Citations
- 1
- Primary Topic
- Memory and Neural Mechanisms
- Type
- article
- Field-Weighted Citation Impact
- 1.43