Fear in action: Fear conditioning and alleviation through body movements

Maria Alemany-González; Martijn E Wokke; Toshinori Chiba; Takuji Narumi; Naotsugu Kaneko; Hiraku Yokoyama; Katsumi Watanabe; Kimitaka Nakazawa; Hiroshi Imamizu; Ai Koizumi

doi:10.1016/j.isci.2024.109099

Fear in action: Fear conditioning and alleviation through body movements

iScience. 2024 Feb 6;27(3):109099. doi: 10.1016/j.isci.2024.109099. eCollection 2024 Mar 15.

Authors

Maria Alemany-González¹, Martijn E Wokke^{1

2

3}, Toshinori Chiba^{4

5

6}, Takuji Narumi⁷, Naotsugu Kaneko⁸, Hiraku Yokoyama⁹, Katsumi Watanabe^{10

11}, Kimitaka Nakazawa⁸, Hiroshi Imamizu^{12

13

14}, Ai Koizumi¹

Affiliations

¹ Sony Computer Science Laboratories, Inc., Tokyo, Japan.
² Centre for Mind, Brain and Behavior, University of Granada, Granada, Spain.
³ Neuroscience Institute, New York University Grossman School of Medicine, New York, NY, USA.
⁴ The Department of Decoded Neurofeedback, Computational Neuroscience Laboratories, Advanced Telecommunications Research Institute International, Kyoto, Japan.
⁵ The Department of Psychiatry, Self-Defense Forces Hanshin Hospital, Kawanishi, Japan.
⁶ The Department of Psychiatry, Kobe University Graduate School of Medicine, Kobe, Japan.
⁷ Graduate School of Information Science and Technology, The University of Tokyo, Tokyo, Japan.
⁸ Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Tokyo, Japan.
⁹ Institute of Engineering, Tokyo University of Agriculture and Technology, Tokyo, Japan.
¹⁰ Faculty of Science and Engineering, Waseda University, Tokyo, Japan.
¹¹ Department of Psychology, University of New South Wales, Sydney, NSW, Australia.
¹² Research Into Artifacts, Center for Engineering, Graduate School of Engineering, The University of Tokyo, Tokyo, Japan.
¹³ Department of Psychology, Graduate School of Humanities and Sociology, The University of Tokyo, Tokyo, Japan.
¹⁴ Department of Cognitive Neuroscience, Cognitive Mechanisms Laboratories, Advanced Telecommunications Research Institute International, Kyoto, Japan.

Abstract

Fear memories enhance survival especially when the memories guide defensive movements to minimize harm. Accordingly, fear memories and body movements have tight relationships in animals: Fear memory acquisition results in adapting reactive defense movements, while training active defense movements reduces fear memory. However, evidence in humans is scarce because their movements are typically suppressed in experiments. Here, we tracked adult participants' body motions while they underwent ecologically valid fear conditioning in a 3D virtual space. First, with body motion tracking, we revealed that distinct spatiotemporal body movement patterns emerge through fear conditioning. Second, subsequent training to actively avoid threats with naturalistic defensive actions led to a long-term (24 h) reduction of physiological and embodied conditioned responses, while extinction or vicarious training only transiently reduced the responses. Together, our results highlight the role of body movements in human fear memory and its intervention.

Keywords: Biological sciences; behavioral neuroscience; neuroscience.

Associated data

Dryad/10.5061/dryad.bcc2fqzj3