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

Author

Ai Koizumi and Kaoru Amano and Aurelio Cortese and Kazuhisa Shibata and Wako Yoshida and Ben Seymour and Mitsuo Kawato and Hakwan Lau

Abstract

Fear conditioning is a fundamentally important and preserved process across species1,2. In humans it is linked to fear-related disorders such as phobias and post-traumatic stress disorder (PTSD)3,4. Fear memories can be reduced by counter-conditioning, in which fear conditioned stimuli (CS+s) are repeatedly reinforced with reward5 or with novel non-threatening stimuli6. 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 settings7. It also raises the fundamental question as to whether explicit presentations of feared objects is necessary for fear reduction1,8. Although learning without explicit stimulus presentation has been previously demonstrated9–12, 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) signals13–15 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)13,15). 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 representations13. 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.