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Fear reduction without fear through reinforcement of neural activity that bypasses conscious exposure

Accepted version
Peer-reviewed

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Authors

Koizumi, A 
Amano, K 
Cortese, A 
Shibata, K 
Yoshida, W 

Abstract

Fear conditioning is a fundamentally important and preserved process across species. In humans it is linked to fear-related disorders such as phobias and post-traumatic stress disorder (PTSD). Fear memories can be reduced by counter-conditioning, in which fear conditioned stimuli (CS+s) are repeatedly reinforced with reward or with novel non-threatening stimuli. However, this procedure involves explicit presentations of CS+s, which is itself aversive before fear is successfully reduced. This aversiveness may be a problem when trying to translate such experimental paradigms into clinical settings. It also raises the fundamental question as to whether explicit presentations of feared objects is necessary for fear reduction. Although learning without explicit stimulus presentation has been previously demonstrated whether fear can be reduced while avoiding explicit exposure to CS+s remains largely unknown. One recently developed approach employs an implicit method to induce learning by reinforcing stimulus-specific neural representations using real-time decoding of multivariate functional magnetic resonance imaging (fMRI) signals in the absence of stimulus presentation; that is, pairing rewards with the occurrences of multi-voxel brain activity patterns matching a specific stimulus (decoded fMRI neurofeedback (DecNef). It has been shown that participants exhibit perceptual learning for a specific visual stimulus feature through DecNef, without being given any strategy for the induction of specific neural representations, and without awareness of the content of reinforced neural representations. Here we examined whether a similar approach could be applied to counter-conditioning of fear. We show that we can reduce fear towards CS+s by pairing rewards with the activation patterns in visual cortex representing a CS+, while participants remain unaware of the content and purpose of the procedure. This procedure may be an initial step towards novel treatments for fear-related disorders such as phobia and PTSD, via unconscious processing.

Description

Keywords

Fear extinction, Multi-voxel decoding, Post-traumatic stress disorder, fMRI decoded neurofeedback

Journal Title

Nature Human Behaviour

Conference Name

Journal ISSN

2397-3374
2397-3374

Volume Title

1

Publisher

Nature Publishing Group
Sponsorship
This work was partially supported by ‘Brain Machine Interface Development’ under the Strategic Research Program for Brain Sciences supported by the Japan Agency for Medical Research and Development (AMED), the ATR entrust research contract from the National Institute of Information and Communications Technology, and the US National Institute of Neurological Disorders and Stroke of the National Institutes of Health (grant no. R01NS088628 to H.L.). B.S. is funded by the Wellcome Trust, UK.