Behavioural Brain Research 238 (2013) 200–205
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Behavioural Brain Research
j ourna l ho me pa ge: www.elsevier.com/locate/bbr
Short communication
Social modulation in extinction of aversive memories
Aleksandra Nowak, Tomasz Werka, Ewelina Knapska
∗
Department of Neurophysiology, Nencki Institute of Experimental Biology, Polish Academy of Science, 3 Pasteur St., 02-093 Warsaw, Poland
h i g h l i g h t s
◮ We propose two models of social modulation of extinction memory retrieval.
◮ Extinguished fear response renews in the presence of a fearful conspecific.
◮ Extinguished avoidance response renews in the presence of a fearful conspecific.
a r t i c l e i n f o
Article history:
Received 13 June 2012
Received in revised form 16 October 2012
Accepted 18 October 2012
Available online 26 October 2012
Keywords:
Fear conditioning
Place avoidance
Extinction
Renewal
Empathy
Anxiety disorders
a b s t r a c t
Return of fear after extinction is a considerable challenge for the efficacy of exposure-based therapies.
Fear recovery is most often modeled in the laboratory by changing the experimental context and studied
in isolated animals. Since social context is an important factor affecting behavior, the question arises
how it influences the recovery of extinguished fear. Here we present two novel behavioral models that
allow studying social modulation of extinction memory retrieval. We show that the presence of a fearful
cage mate results in a robust renewal of freezing as well as avoidance responses that were previously
successfully extinguished.
© 2012 Elsevier B.V. All rights reserved.
Fear-eliciting properties of a stimulus acquired through con-
ditioning can be extinguished by a repeated presentation of the
conditioned stimulus (CS) in the absence of the unconditioned stim-
ulus [1]. Similarly, extinction of learned place avoidance behavior
occurs when visiting the place is no longer punished [2]. However,
such extinction process does not reflect unlearning of the original
association, but results in a transient inhibition of fear. For example,
extinguished fear responses may return after a change of context
(renewal phenomenon) [3].
In recent years, increased interest in mechanisms underlying
fear extinction has emerged, partly because it is a useful model
for exposure-based therapies for the treatment of human anxi-
ety disorders, such as phobias and post-traumatic stress disorder
[4]. The return of fear after extinction is a considerable challenge
for maintaining long-lasting fear suppression after exposure-based
therapies [5]. Until recently, the fear extinction and recovery
phenomena were studied only in isolated animals. However, since
vicarious experience accounts of both etiology and extinction of
phobias have been shown in humans [6,7], social modulation seems
∗
Corresponding author. Tel.: +48 22 5892 257; fax: +48 22 5892 490.
E-mail address: e.knapska@nencki.gov.pl (E. Knapska).
to be an important factor that can affect the efficacy of exposure
based therapies.
Social modulation of fear and avoidance learning in animal
models was shown before [8–11]; however until now there were
no animal models allowing for studying vicarious modulation of
aversive memories extinction. In the present study, we examined
influence of a fearful conspecific’s presence on the rate of retrieval
of fear and place avoidance extinction memory.
In the first experiment we tested retrieval of fear extinction
memory in the presence of a fearful conspecific. Male 2–3-month-
old C57BL/6 male mice were housed in pairs, extensively handled
for 3 weeks in order to minimize stress caused by an experimenter’s
presence and habituated to transport to experimental room and
to experimental cage (in three 10-min sessions). Then, the mice
were subjected to fear conditioning and extinction in the Panlab
shuttle-box for mice (LE918), which was divided by a perforated
transparent partition allowing the mice to see, hear and smell the
neighbor, but not to contact him physically. The mice were trained
and tested in the left or right part of the shuttle-box cage (for
every animal the side of the cage was the same through the whole
behavioral procedure). Sensory stimuli were adjusted to generate
two distinct contexts (context A: room lights on, the cage cleaned
with a 1% acid solution, the mice transported to this context in
0166-4328/$ – see front matter © 2012 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.bbr.2012.10.031