Sexually divergent expression of active and passive conditioned fear responses in rats

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Abstract

Traditional rodent models of Pavlovian fear conditioning assess the strength of learning by quantifying freezing responses. However, sole reliance on this measure includes the de facto assumption that any locomotor activity reflects an absence of fear. Consequently, alternative expressions of associative learning are rarely considered. Here we identify a novel, active fear response ('darting') that occurs primarily in female rats. In females, darting exhibits the characteristics of a learned fear behavior, appearing during the CS period as conditioning proceeds and disappearing from the CS period during extinction. This finding motivates a reinterpretation of rodent fear conditioning studies, particularly in females, and it suggests that conditioned fear behavior is more diverse than previously appreciated. Moreover, rats that darted during initial fear conditioning exhibited lower freezing during the second day of extinction testing, suggesting that females employ distinct and adaptive fear response strategies that improve long-term outcomes.

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Tina M Gruene

Department of Psychology, Northeastern University, Boston, United States

Competing interests
The authors declare that no competing interests exist.
Katelyn Flick

Department of Psychology, Northeastern University, Boston, United States

Competing interests
The authors declare that no competing interests exist.
Alexis Stefano

Department of Psychology, Northeastern University, Boston, United States

Competing interests
The authors declare that no competing interests exist.
Stephen D Shea

Cold Spring Harbor Laboratory, Cold Spring Harbor, United States

Competing interests
The authors declare that no competing interests exist.
Rebecca M Shansky

Department of Psychology, Northeastern University, Boston, United States

For correspondence
r.shansky@neu.edu

Competing interests
The authors declare that no competing interests exist.

Ethics

Animal experimentation: All procedures were conducted in accordance with the National Institutes of Health Guide for the Care and Use of Laboratory Animals and were approved by the Northeastern University Institutional Animal Care and Use Committee protocol # 12-0102R.

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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.