An Evolutionarily Threat-Relevant Odor Strengthens Human Fear Memory

Jessica E Taylor; Hakwan Lau; Ben Seymour; Aya Nakae; Hidenobu Sumioka; Mitsuo Kawato; Ai Koizumi

doi:10.3389/fnins.2020.00255

An Evolutionarily Threat-Relevant Odor Strengthens Human Fear Memory

Front Neurosci. 2020 Apr 22:14:255. doi: 10.3389/fnins.2020.00255. eCollection 2020.

Authors

Jessica E Taylor¹, Hakwan Lau^{1

2

3}, Ben Seymour^{4

5

6}, Aya Nakae⁷, Hidenobu Sumioka⁸, Mitsuo Kawato^{1

4}, Ai Koizumi^{1

4

9}

Affiliations

¹ Department of Decoded Neurofeedback (DecNef), Computational Neuroscience Laboratories, Advanced Telecommunications Research Institute International, Kyoto, Japan.
² Department of Psychology, Brain Research Institute, University of California, Los Angeles, Los Angeles, CA, United States.
³ Department of Psychology, University of Hong Kong, Pokfulam, Hong Kong.
⁴ Center for Information and Neural Networks (CiNet), National Institute of Information and Communications Technology (NICT), Osaka, Japan.
⁵ Computational and Biological Learning Lab, Department of Engineering, University of Cambridge, Cambridge, United Kingdom.
⁶ Department of Neural Computation for Decision-Making, Cognitive Mechanisms Laboratories, Advanced Telecommunications Research Institute International, Kyoto, Japan.
⁷ Graduate School of Frontier Biosciences, Osaka University, Osaka, Japan.
⁸ Hiroshi Ishiguro Laboratories, Advanced Telecommunications Research Institute International, Kyoto, Japan.
⁹ Sony Computer Science Laboratories, Inc., Tokyo, Japan.

Abstract

Olfaction is an evolutionary ancient sense, but it remains unclear to what extent it can influence routine human behavior. We examined whether a threat-relevant predator odor (2-methyl-2-thiazoline) would contextually enhance the formation of human fear memory associations. Participants who learned to associate visual stimuli with electric shock in this predator odor context later showed stronger fear responses to the visual stimuli than participants who learned in an aversiveness-matched control odor context. This effect generalized to testing in another odor context, even after extinction training. Results of a separate experiment indicate that a possible biological mechanism for this effect may be increased cortisol levels in a predator odor context. These results suggest that innate olfactory processes can play an important role in human fear learning. Modulatory influences of odor contexts may partly explain the sometimes maladaptive persistence of human fear memory, e.g., in post-traumatic stress disorders.

Keywords: contextual memory modulation; fear memory; human olfaction; innate fear; predator odor.