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

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 unde...

Full description

Bibliographic Details
Main Authors: Jeremy M Trott, Ann N Hoffman, Irina Zhuravka, Michael S Fanselow
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2022-05-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/75663
_version_ 1818018393310101504
author Jeremy M Trott
Ann N Hoffman
Irina Zhuravka
Michael S Fanselow
author_facet Jeremy M Trott
Ann N Hoffman
Irina Zhuravka
Michael S Fanselow
author_sort Jeremy M Trott
collection DOAJ
description 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.
first_indexed 2024-04-14T07:38:35Z
format Article
id doaj.art-8f7f6204c9f349cd96cd0b50cb9518c0
institution Directory Open Access Journal
issn 2050-084X
language English
last_indexed 2024-04-14T07:38:35Z
publishDate 2022-05-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj.art-8f7f6204c9f349cd96cd0b50cb9518c02022-12-22T02:05:34ZengeLife Sciences Publications LtdeLife2050-084X2022-05-011110.7554/eLife.75663Conditional and unconditional components of aversively motivated freezing, flight and darting in miceJeremy M Trott0https://orcid.org/0000-0002-7875-3446Ann N Hoffman1Irina Zhuravka2Michael S Fanselow3https://orcid.org/0000-0002-3850-5966Staglin Center for Brain and Behavioral Health, Department of Psychology, Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, United StatesStaglin Center for Brain and Behavioral Health, Department of Psychology, Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, United StatesStaglin Center for Brain and Behavioral Health, Department of Psychology, Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, United StatesStaglin Center for Brain and Behavioral Health, Department of Psychology, Department of Psychiatry and Biobehavioral Sciences, University of California, Los Angeles, Los Angeles, United StatesFear 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.https://elifesciences.org/articles/75663mousedefensive behaviorfear conditioningdartinglearningmemory
spellingShingle Jeremy M Trott
Ann N Hoffman
Irina Zhuravka
Michael S Fanselow
Conditional and unconditional components of aversively motivated freezing, flight and darting in mice
eLife
mouse
defensive behavior
fear conditioning
darting
learning
memory
title Conditional and unconditional components of aversively motivated freezing, flight and darting in mice
title_full Conditional and unconditional components of aversively motivated freezing, flight and darting in mice
title_fullStr Conditional and unconditional components of aversively motivated freezing, flight and darting in mice
title_full_unstemmed Conditional and unconditional components of aversively motivated freezing, flight and darting in mice
title_short Conditional and unconditional components of aversively motivated freezing, flight and darting in mice
title_sort conditional and unconditional components of aversively motivated freezing flight and darting in mice
topic mouse
defensive behavior
fear conditioning
darting
learning
memory
url https://elifesciences.org/articles/75663
work_keys_str_mv AT jeremymtrott conditionalandunconditionalcomponentsofaversivelymotivatedfreezingflightanddartinginmice
AT annnhoffman conditionalandunconditionalcomponentsofaversivelymotivatedfreezingflightanddartinginmice
AT irinazhuravka conditionalandunconditionalcomponentsofaversivelymotivatedfreezingflightanddartinginmice
AT michaelsfanselow conditionalandunconditionalcomponentsofaversivelymotivatedfreezingflightanddartinginmice