Extinction recall of fear memories formed before stress is not affected despite higher theta activity in the amygdala

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Abstract

Stress is known to exert its detrimental effects not only by enhancing fear, but also by impairing its extinction. However, in earlier studies stress exposure preceded both processes. Thus, compared to unstressed animals, stressed animals had to extinguish fear memories that were strengthened by prior exposure to stress. Here we dissociate the two processes to examine if stress specifically impairs the acquisition and recall of fear extinction. Strikingly, when fear memories were formed before stress exposure, thereby allowing animals to initiate extinction from comparable levels of fear, recall of fear extinction was unaffected. Despite this we observed a persistent increase in theta activity in the BLA. Theta activity in the mPFC, by contrast, was normal. Stress also disrupted mPFC-BLA theta-frequency synchrony and directional coupling. Thus, in the absence of the fear-enhancing effects of stress, the expression of fear during and after extinction reflects normal regulation of theta activity in the mPFC, not theta hyperactivity in the amygdala.

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Data generated or analysed during this study are included in the manuscript and supporting files. Source data files have been provided for all the Figures.

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Mohammed Mostafizur Rahman

National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, India

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0002-9355-4867
Ashutosh Shukla

National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, India

Competing interests
The authors declare that no competing interests exist.
Sumantra Chattarji

National Centre for Biological Sciences, Tata Institute of Fundamental Research, Bangalore, India

For correspondence
shona@ncbs.res.in

Competing interests
The authors declare that no competing interests exist.

"This ORCID iD identifies the author of this article:" 0000-0001-9962-3635

Funding

Department of Atomic Energy, Government of India

Mohammed Mostafizur Rahman
Ashutosh Shukla
Sumantra Chattarji

Department of Biotechnology , Ministry of Science and Technology

Sumantra Chattarji

Madan and Usha Sethi Fellowship

Sumantra Chattarji

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Ethics

Animal experimentation: All animal care and experimentation procedures were approved by the Institutional Animal Ethics Committee, National Centre for Biological Sciences (Approval No: SC-5/2009) and Committee for the Purpose of Control and Supervision of Experiments on Animals, Government of India (Registration No: 109/CPCSEA).

Copyright

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.