Neurobiology of Learning and Memory 87 (2007) 209–217
www.elsevier.com/locate/ynlme
1074-7427/$ - see front matter © 2006 Elsevier Inc. All rights reserved.
doi:10.1016/j.nlm.2006.08.009
Methylene blue facilitates the extinction of fear in an animal
model of susceptibility to learned helplessness
Kathryn M. Wrubel, Douglas Barrett, Jason Shumake,
S. Elizabeth Johnson, F. Gonzalez-Lima
¤
Department of Psychology and Institute for Neuroscience, University of Texas at Austin, Austin, TX 78712, USA
Received 29 June 2006; revised 22 August 2006; accepted 23 August 2006
Available online 2 October 2006
Abstract
The objectives were to (1) extend previous Wndings on fear extinction deWcits in male congenitally helpless rats (a model for susceptibil-
ity to learned helplessness) to female congenitally helpless rats, and (2) attempt a therapeutic intervention with methylene blue, a meta-
bolic enhancer that improves memory retention, to alleviate the predicted extinction deWcits. In the Wrst experiment, fear acquisition (four
tone-shock pairings in operant chamber) was followed by extinction training (60 tones in open Weld). Congenitally helpless rats showed
fear acquisition similar to controls but had dramatic extinction deWcits, and did not display the gradual extinction curves observed in con-
trols. Congenitally helpless rats demonstrated greater tone-evoked freezing as compared to controls in both the acquisition and extinction
contexts one week after extinction training, and also in the extinction probe conducted one month later. In the second experiment (which
began one month after the Wrst experiment) congenitally helpless subjects were further exposed to tones for 5 days, each followed by 4 mg/kg
methylene blue or saline IP, and had a fear renewal test in the acquisition context. Methylene blue administration improved retention of
the extinction memory as demonstrated by signiWcant decreases in fear renewal as compared to saline-administered congenitally helpless
subjects. The impaired ability to extinguish fear to a traumatic memory in congenitally helpless rats supports the validity of this strain as
an animal model for vulnerability to post-traumatic stress disorder, and this study further suggests that methylene blue may facilitate fear
extinction as an adjunct to exposure therapy.
© 2006 Elsevier Inc. All rights reserved.
Keywords: Extinction; Post-traumatic stress disorder; Congenitally helpless rats; Methylene blue; Fear conditioning; Metabolic enhancer; Animal model;
Disease susceptibility; Memory retention; Exposure therapy; Cytochrome oxidase
1. Introduction
Inescapable electric shock prevents animals from subse-
quently learning an escape response, a phenomenon termed
learned helplessness (Overmier & Seligman, 1967). Vulnera-
bility to learned helplessness is hereditable and can be
enhanced through selective breeding, as evidenced by the
creation of a strain of congenitally helpless rats (Henn &
Vollmayr, 2005). Studies show that up to 95% of the con-
genitally helpless oVspring typically show the learned
helpless phenotype, as opposed to the 5–20% of randomly
bred rats (Henn, Johnson, Edwards, & Anderson, 1985;
Lachman et al., 1992). Since epidemiological studies show
that 40–50% of the risk of susceptibility to depression and
30% of the risk of susceptibility to post-traumatic stress
disorder (PTSD) is genetic (Fava & Kendler, 2000; Sanders,
Detera-Wadleigh, & Gershon, 1999; True et al., 1993), an
appropriate animal model of congenital vulnerability to
these disorders could be very useful, especially in the devel-
opment of therapeutic treatments.
A recent paper reported behavioral characteristics of
male rats predisposed to learned helplessness (Shumake,
Barrett, & Gonzalez-Lima, 2005). Compared to normal
rats, congenitally helpless rats demonstrated reduced
*
Corresponding author. Fax: +1 512 471 4728.
E-mail address: gonzalez-lima@mail.utexas.edu (F. Gonzalez-Lima).