Conditional and unconditional components of aversively motivated freezing, flight and darting in mice

Abstract
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Abstract

Fear conditioning is one of the most frequently used laboratory procedures for modeling learning and memory generally, and anxiety disorders in particular. The conditional response (CR) used in the majority of fear conditioning studies in rodents is freezing. Recently, it has been reported that under certain conditions, running, jumping or darting replaces freezing as the dominant CR. These findings raise both a critical methodological problem and an important theoretical issue. If only freezing is measured but rodents express their learning with a different response, then significant instances of learning, memory, or fear may be missed. In terms of theory, whatever conditions lead to these different behaviors may be a key to how animals transition between different defensive responses and different emotional states. In mice, we replicated these past results but along with several novel control conditions. Contrary to the prior conclusions, running and darting were primarily a result of nonassociative processes and were actually suppressed by associative learning. Darting and flight were taken to be analogous to nonassociative startle or alpha responses that are potentiated by fear. Additionally, associative processes had some impact on the topography of flight behavior. On the other hand, freezing was the purest reflection of associative learning. We also uncovered a rule that describes when these movements replace freezing: When afraid, freeze until there is a sudden novel change in stimulation, then burst into vigorous flight attempts. This rule may also govern the change from fear to panic.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting files.R code to extract darts and produce velocity traces is uploaded as Source Code 1Source Data Files have been provided for Figures 2, 3, 4, 5, 6, 7, 8, 9, 10, 11 as well as Figure 1-figure supplement 1, Figure 2-figure supplement 1, Figure 4-figure supplement 1, Figure 8-figure supplement 1

Article and author information

Author details

Jeremy M Trott

Department of Psychology, University of California, Los Angeles, Los Angeles, United States

Competing interests
No competing interests declared.

"This ORCID iD identifies the author of this article:" 0000-0002-7875-3446
Ann N Hoffman

Department of Psychology, University of California, Los Angeles, Los Angeles, United States

Competing interests
No competing interests declared.
Irina Zhuravka

Department of Psychology, University of California, Los Angeles, Los Angeles, United States

Competing interests
No competing interests declared.
Michael S Fanselow

Department of Psychology, University of California, Los Angeles, Los Angeles, United States

For correspondence
fanselow@psych.ucla.edu

Competing interests
Michael S Fanselow, is a founding board member of Neurovation, Inc..

"This ORCID iD identifies the author of this article:" 0000-0002-3850-5966

Funding

National Institutes of Health (R01MH062122)

Michael S Fanselow

Staglin Center for Brain And Behavioral Health (MSF Award)

Michael S Fanselow

National Institute on Drug Abuse (T32DA024635)

Jeremy M Trott

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 subjects in each reported study were treated in accordance with an approved protocol (#09-107) from the Institutional Animal Care and Use Committee at the University of California-Los Angeles following recommendations in the Guide for the Care and Use of Laboratory Animals established by the National Institute of Health.

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.