Learning and Motivation 43 (2012) 2434

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Learning and Motivation
j our nal homepage: www. el sevi er . com/ l ocat e/ l &m
A modied counterconditioning procedure prevents the renewal of
conditioned fear in rats
Brian L. Thomas

, Marlo Cutler, Cheryl Novak

Department of Psychology, Baldwin-Wallace College, United States
a r t i c l e i n f o
Article history:
Received 6 September 2011
Received in revised form3 January 2012
Available online 13 February 2012
Keywords:
Renewal
Relapse
Fear
Phobias
Extinction
Conditioned suppression
Context dependence
Retrieval
Counterconditioning
Reciprocal inhibition
Systematic desensitization
a b s t r a c t
Two studies using an ABA design examined the Extinction and renewal of conditioned
barpress suppression. Following lights-off and foot shock pairings in Context A, rats were
placed in Context B and were given either a standard counterconditioning procedure where
the lights-off CS was paired with a novel food US delivered freely or a modied counter-
conditioning procedure where CS-US pairings only occurred if the rat earned the US by
performing a required behavior during the CS. Results indicated that the modied counter-
conditioning procedure thwarted ABA renewal but the conventional counterconditioning
procedure did not reduce ABA renewal any more than nonreinforced exposure to the CS
alone. Furthermore, the response required during the modied counterconditioning pro-
cedure could be one used as a baseline response during Acquisition of fear or it could be
a novel response. Implications of the results for theories of Extinction and renewal of fear
are discussed.
2012 Elsevier Inc. All rights reserved.
A considerable amount of research has been conducted over the past 50 years on the treatment of phobias in humans
and on the Extinction of conditioned fears in animal models of phobia. In most cases, the results fromstudies with animals
have been similar to the results fromhuman trials (Thyer, Baum, & Reid, 1988). However, one important exception involves
the process known as counterconditioning where a conditioned stimulus (CS) is rst followed by an aversive unconditioned
stimulus (US) to establish fear and is subsequently paired with an appetitive US in an attempt to decrease fear of the CS. Jones
(1924) rst reported that a child with a phobia could be treated effectively by gradually reducing the distance between the
child and the feared CS (to limit anxiety) while the child ate food. Wolpe (1958) reported analogous results with cats using a
modicationof Massermans (1943) methodfor producing neuroses. Briey, cats were givenanauditory stimulus followed
by shock at randomintervals until a pre-established feeding behavior became inhibited. Next, food was placed on the end of
a rod and gradually moved towards the cats mouth. At rst, the cat would approach the food hesitantly and may refuse to
eat it. However, after several trials, the cat was likely to eat the food readily fromthe rod and eventually fromthe grid oor
that had been the source of the shock earlier in training. Based on these observations, Wolpe (1958) argued that feeding
responses couldbe made toinhibit fear responses (andvice-versa), anexample of a principle he calledreciprocal inhibition.
Wolpe(1952, 1958) usedreciprocal inhibitionas thefoundationfor thebehavioral therapytechniqueknownas systematic
desensitization. Insystematic desensitization, fearful scenarios are arrangedhierarchicallyandare thendescribedtoa person

Corresponding author at: Department of Psychology, 275 Eastland Road, Berea, OH 44017, United States.
E-mail address: bthomas@bw.edu (B.L. Thomas).
0023-9690/$ see front matter 2012 Elsevier Inc. All rights reserved.
doi:10.1016/j.lmot.2012.01.001
B.L. Thomas et al. / Learning and Motivation 43 (2012) 2434 25
while he or she is engaged in relaxation techniques. Wolpe believed that a state of deep relaxation was incompatible with,
and would inhibit, the anxiety normally activated by imagination of a feared scenario. Upon researching the technique in a
randomsample of 36 patients, Wolpe (1969, p. 144) claimed that systematic desensitization markedly ameliorated anxiety
responses in about 90% of the patients. Further studies by Hain, Butcher, and Stevenson (1966), Kraft (1970), Lazarus (1961)
and Paul (1969) reported success rates between 70 and 92% using systematic desensitization.
Given the apparent efcacy of systematic desensitization for treating phobias in humans, it is interesting that laboratory
investigations using non-human animals have only yielded mixed results. For example, Klein (1969) trained rats to fear one
side of a test apparatus and then conned the rats to that side with or without food present. Klein assumed that combining
forced exposure to the feared context with free food would result in counterconditioning and that those rats would be less
likely to avoid the once feared compartment than rats that were given forced connement without food. The results showed
that the presence of food did not reduce avoidance more than simple exposure to the feared context. Similar results were
reported by Moltz (1954), Sermat and Shepard (1959), and Delprato and Jackson (1973). In contrast, several researchers
have reported that counterconditioning treatments reduced fear more effectively than exposure to the feared CS alone. For
example, Reid (1973) described several studies where intracranial stimulation (ICS) of the hypothalamus was given to rats
during or shortly after forced exposure to a feared stimulus. The addition of ICS always reduced fear more effectively than
exposure to the CS alone. Lane (1954), Hall (1955), Dickson, Mellgren, Fountain, and Dyck (1977) and Richardson, Riccio, and
Smoller (1987) found similar results substituting food for ICS. Taken together, these results suggest that counterconditioning
of fear in animals is possible, as it is with human patients, but that further research is needed to determine the training
features required to produce the phenomenon reliably. The rst goal of the present set of studies was to establish a method
that reliably produced counterconditioning of fear in rats.
In addition to the unreliability of counterconditioning in nonhuman animals, Capaldi, Viveiros, and Campbell (1983)
cautioned that the introduction of an appetitive US during counterconditioning could result in context specic Extinction if
the US was not also provided during subsequent phases of testing. Most of the early animal studies of counterconditioning
only compared Extinction rates during counterconditioning with Extinction rates during conventional Extinction (where
only the CS was presented). Capaldi et al. (1983) realized that even if counterconditioning produced a faster reduction of
fear than Extinction, the presence of food during counterconditioning might interfere with its generalization to situations
where food was not present. This implies that any reduction in fear during counterconditioning might be lost outside of
the counterconditioning context or after a forgetting interval. Using the conditioned lick suppression task (Experiment 3),
two groups were given context and shock pairings either with or without food present. In the second phase, each of these
groups was subdivided and half received context Extinction with food present and half without food present. Finally, all four
groups were tested for lick suppression in the context without food present. Since the last phase was conducted without
food present, the authors hypothesized that lick suppression would be stronger following counterconditioning (where food
was present) than conventional Extinction (where food was not present). Moreover, providing food during Acquisition was
expected to reduce the differences between the counterconditioning and Extinction groups during the nal phase because
food could not then be used to predict the absence of the shock. The results conrmed these expectations and showed that
food introduced during counterconditioning increased the context specicity of fear Extinction.
Two additional papers have addressed this issue using fear of a discrete CS rather than contextual fear. First, Peck and
Bouton (1990) trained rats to fear a CS in Context A and then gave CS-food pairings in Context B. Fear was indicated by
defensive freezing behavior and food expectation was indicated by head jerking. After counterconditioning concluded, rats
were given exposure to the CS alone in either Context A or a novel context, C, to assess howwell counterconditioning gen-
eralized to different settings. A modest renewal of the freezing response and a large decrease of the head jerking behavior
occurred when the CS was presented in Context A, but neither of the changes occurred when the CS was presented in Con-
text C. Bouton and Peck (1992) sought to extend their ndings by assessing counterconditioning after a 28-day interval was
imposed between the last counterconditioning session and the nal test of the CS alone. All phases of the experiment were
conducted in a single physical context. Rats that were given CS-food pairings during counterconditioning spontaneously
recovered the freezing response and made fewer head jerks when tested after a 28-day retention interval. Taken together,
these results are consistent with those reported by Capaldi et al. (1983) and showthat the presence of food during counter-
conditioning increased the context specicity of fear reduction. The second goal of the present set of studies was to explore
one strategy for reducing the context specicity of counterconditioning.
A variety of mechanisms have been proposed for counterconditioning including: peripheral response competition, com-
petition between central motivational states and competition between expectancies. More specically, Guthrie (1938)
argued that a stimulus-response association could be replaced if the stimulus became associated with a different response
and Wolpe (1958) required that the newresponse also be incompatible with the original. One difculty with a mechanism
based upon response competition comes fromresearch on superconditioning. For example, Rescorla (1971) showed that a
CS that was established as a conditioned inhibitor of fear actually facilitated fear conditioning of another, neutral CS when
the compound was paired with shock. According to a response competition mechanism, the conditioned inhibitor should
have elicited behaviors that were incompatible with fearful behavior and should have retarded, rather than facilitated, fear
conditioning (i.e., freezing) to the neutral CS. Dickinson (1977) reported a similar result using an appetitive conditioned
exciter in place of the conditioned inhibitor.
Several theorists including Konorski (1967), Mowrer (1960) and Stein (1964) argued that the mechanismof countercon-
ditioning depended upon competing appetitive and aversive motivational states. For example, a foot shock was expected
26 B.L. Thomas et al. / Learning and Motivation 43 (2012) 2434
to simultaneously excite an aversive motivational state and inhibit an appetitive motivational state. In contrast, food was
expected to simultaneously excite appetitive motivation and inhibit aversive motivation. This type of mechanismattributes
successful counterconditioning of fear, in this case, to appetitive motivation outweighing the inuence of aversive motiva-
tion. However, counterconditioning should occur more slowly than Extinction because a feared CS should strongly inhibit
the motivation to eat early in counterconditioning. Additionally, this mechanismsuggests that once appetitive motivation
causes an increase in feeding behavior, the simultaneous inhibition of aversive motivation should cause a corresponding
decrease in fearful responding. Several studies have reported results that are not consistent with this implication (Lovibond
& Dickinson, 1982; Scavio & Gormezano, 1980).
Most recently, Capaldi et al. (1983) suggested that competition may occur between expectations rather than motivational
states. More specically, pairing the CS with shock in Phase 1 and then pairing the same CS with food (and without shock) in
Phase 2 could cause the CS to elicit two distinct expectancies. This ambiguity in the meaning of the CS could be resolved by
usingcontextual stimuli that wereuniquetoeachphaseof training. Inthis view, counterconditioningresembles conventional
Extinction because in each procedure, the CS takes on a second meaning, CS-food or CS-No US, respectively, that make
the CS ambiguous. In studies where the presence or absence of food can be used to disambiguate the meaning of the CS,
generalization of counterconditioning should depend upon whether or not food is present during the nal phase of testing.
If food is present, fear should not be expressed and if food is omitted, fear should reappear. As reported earlier, the results
in Capaldi et al. (1983), Peck and Bouton (1990) and Bouton and Peck (1992) are consistent with this mechanism. One goal
of the present set of studies is to attempt to reduce fear renewal following counterconditioning.
Given the inconsistency in the animal literature on counterconditioning (along with the generally positive results in
humans studies) and the ndings that counterconditioning can be context specic, the primary strategy for the present set
of studies was to search for differences in howcounterconditioning experiments have been conducted in rats and humans.
In animal research, the appetitive US has typically been presented independent of the animals behavior. In contrast, human
studies invariably require the client to engage in a response in order to receive the appetitive US (i.e., relaxation). This
suggests that differences in the animal and human literature might reect the importance of reinforcing an instrumental
response during nonreinforcement of the CS. When Wolpe (1969) extended systematic desensitization into assertiveness
training, he alluded to the importance of the environment selectively providing positive reinforcement for any assertive
behavior that was made. The present set of studies investigated this idea using the conditioned suppression paradigm(Estes
&Skinner, 1941). Rats weregivenfear conditioninginContext Aandwerethengiveneither counterconditioningor Extinction
in Context B. Based on the ndings described earlier, it was expected that Extinction and traditional counterconditioning
would not prevent fear renewal in Context A. However, it was expected that a modied counterconditioning procedure,
where the appetitive US was contingent upon a response made during the CS, might reduce fear renewal and yield results
more consistent with those reported in humans.
Experiment 1
Prior to Experiment 1, a study was conducted to learn if the modied counterconditioning procedure might inuence fear
renewal. In that study, the CS was presented nine times during each of ve sessions. The results showed that requiring the
subject to earn the appetitive US during counterconditioning (in Context B) reduced fear renewal to a level that was midway
between (and not signicantly different) that of subjects that had received either a conventional Extinction procedure in
Context A or a standard counterconditioning procedure in Context B. In Experiment 1, several changes were made to the
procedure in an attempt to clarify the ndings. First, based on the work of Urcelay, Wheeler, and Miller (2009), the number
of CS presentations was reduced from9 to 4 per session to increase the average length of the intertrial intervals (ITIs) from
5min to 13min. Second, the number of Extinction or counterconditioning sessions was increased from 5 to 24 in order to
increase the total number of CS presentations from45 to 96.
Method
Subjects
The subjects were 35 experimentally naive, 90-day-old SpragueDawley rats that were bred at BaldwinWallace College
from stock purchased from Harlan SpragueDawley Inc. (Indianapolis, IN). Each group had 4 males and 3 females. During
the week prior to the start of the study, free feeding weights varied from460 to 642g in males and 268 to 446g in females.
The rats were reduced to and maintained at 85% of those levels throughout the study. Subjects were housed individually in
stainless steel cages with water available continuously. The colony roomwas lighted daily between 06:00 and 22:00h. All
of the training sessions were conducted between 09:00 and 15:00h.
Apparatus
Sixteenoperant chambers were used(inside dimensions =23.2cm20.3cm19.5cm). The chambers were placedinside
sound attenuating cubes (internal dimensions =55.9cm55.9cm48.9cm) that were made of Ultra Plus foam core with
a 1mmPVC facer (United Industries, Bentonville, AR). On each half of the room, eight of the cubes were stacked 22 on a
bench top along a wall, and eight were similarly stacked on the opposite wall. A 2.5cmsheet of foaminsulation separated
top and bottomboxes to further reduce any noise between them. Adjacent cubes were spaced a minimumof 20cmapart.
B.L. Thomas et al. / Learning and Motivation 43 (2012) 2434 27
Table 1
Summary of experimental conditions in Experiments 1 and 2.
Group Acquisition Extinction/counterconditioning Renewal
CC/I (A) LOshock (B) LORmilk (A) LO
CC/I/diff (A) LOshock (B) LOR2milk (A) LO
CC (A) LOshock (B) LOmilk (A) LO
ABA (A) LOshock (B) LO (A) LO
AAA (A) LOshock (A) LO (A) LO
NE (A) LOshock (A or B) No LO (A) LO
Note. (A) or (B) denotes the context where training occurred. LO is the lights-off CS, R indicates the instrumental response reinforced by sucrose during
AcquisitionandRenewal, andR2 indicates aninstrumental response that was not reinforcedby sucrose during AcquisitionandRenewal. During Acquisition,
10 pairings of the LO and foot shock occurred. In Extinction/Counterconditioning, the LO was presented 96 times in each group except for NE which did
not receive any LO presentations. During Renewal, the LO was presented once per day for 4 days.
Three white frosted light bulbs (each 7.5W, 110V) were on the back wall of the sound attenuating cube and provided the
house lighting. Termination of these house lights served as a CS in the study. The work panel and the opposite wall of each
operant chamber were aluminum and the side walls were clear plexiglas. Centered in the work panel was a response bar
(5cm1.5cm). Aweight of 2032g was required to close a microswitch that activated a dipper located to the left and below
the response bar. The oor consisted of 18 stainless steel rods (2mmin diameter, centers spaced 1.3cmapart). Corrugated
squares of cardboard lined the waste tray belowthe rods. On the lid of each operant chamber was a speaker (10-cmdiam.)
that provided a white noise background of 80dB when superimposed on the noise fromthe ventilating fans. Sound intensity
was measured using a Radio Shack sound level meter (catalog number 33-2050; C scale, slowresponse) with its microphone
about 7cm from the dipper tray. The US was a 1-s, 0.6mA scrambled grid shock generated by Grason-Stadler shockers
(Models E1064 or 700; Grason-Stadler Co., West Concord, MA). The peak shock intensity, as measured at the grids using a
Fluke 83 III multimeter (John Fluke Mfg Co Inc., Everett, WA), was equivalent to the nominal shock setting. A computer in
an adjacent roomcontrolled all stimulus events and recorded bar presses.
All 16 chambers were used to create two distinctive contexts. The boxes on one wall had a glass coaster containing 10mL
of 2% anise in water solution (McCormack, Sparks, MD) placed just outside the food magazine. Boxes on the opposite wall
had vertical black stripes on the Plexiglas walls that were 1cmwide and spaced 2cmapart, a slanted aluminumplate that
reduced the distance fromthe work panel to the back wall from23.2 to 12.5cmat oor level, and a glass coaster containing
10mL of undiluted vinegar (Heinz, Pittsburgh, PA) that was also placed next to the magazine. Half the subjects in each group
received fear conditioning and renewal testing in each type of box (hereafter called Context A), and the alternative box
served as Context B.
Procedure
Table 1 illustrates the design of the study. Subjects were randomly assigned to one of 5 groups: counterconditioning
with food contingent upon instrumental leverpressing (CC/I), counterconditioning with food given freely during the CS (CC),
conventional Extinction in Context A (AAA), conventional Extinction in Context B (ABA) and a no Extinction control group
(NE).
Preliminarytraining. Preliminarytrainingincluded2days of magazinetrainingallowingrats todrink32%sucrosefrom0.1mL
dippers, 2 days of shaping where the leverpress response was reinforced with sucrose 100 times per day on a continuous
reinforcement schedule, 2days of leverpress trainingonavariableinterval 60-s schedule(VI-60) and2days of CSpreexposure
where the 60-s long, lights-off CS was presented alone to reduce any neophobia. Training was conducted in Context A on
days 1, 3, 5 and 7 and in Context B on days 2, 4, 6 and 8. Odor cues were not incorporated into Contexts A and B until day 5
when the doors to the sound attenuating chambers were rst closed and remained closed thenceforth. All training sessions
were 60min long in this phase and all the phases that followed.
Fear Acquisition in Context A. All groups received 5 Acquisition sessions in Context A. Two lights-off-shock trials occurred
in each session. Timing of the trials varied daily, but no trials were scheduled during the rst or last 5min of the session.
Leverpressing was reinforced with sucrose on a VI-60 schedule throughout the session.
Fear Extinction/counterconditioning in Context A or B. The Extinction phase occurred over the next 24 daily sessions. For
Groups AAA, ABA and NE, leverpressing was reinforced with sucrose on a VI-60 schedule just as it had been during the
Acquisition phase. For Groups CC and CC/I, sucrose was replaced with chocolate milk (Deans, Sharpsville, PA) that was
only available during the CS. Leverpresses made outside of the CS period were not reinforced. While Group CC received the
chocolate milk freely during the CS, Group CC/I had to leverpress during the CS to earn the chocolate milk. More specically,
in Group CC the dipper was raised for 4s and then lowered for 4s throughout the CS independent of the rats behavior. In
Group CC/I, each leverpress during the CS caused the dipper to be raised for 4s. Additional leverpresses made while the
dipper was raised were counted but did not extend the time that the dipper was raised. After 4s, the dipper was lowered
for 4s before the next dipper could be earned. Chocolate milk was substituted for sucrose because it had proven to be an
28 B.L. Thomas et al. / Learning and Motivation 43 (2012) 2434
Fig. 1. Mean suppression on the last trial of the Acquisition phase (A), the rst (F) and last (L) trials of each session of the extinction phase (gaps indicate
breaks between daily sessions), and the four trials of the Renewal phase (R1R4). In Context A, all groups received lights-off and shock pairings during the
Acquisition phase and lights-off without shock during the renewal phase. Groups were given different procedures during the Extinction phase: Group NE
was placed in either Context A or B to allowfor extinction of the contextual cues, Groups ABA and AAA were placed in Contexts B and A, respectively and
were given nonreinforced exposure to the lights-off CS, Group CC was placed in Context B and given lights-off and chocolate milk pairings and Group CC/I
was placed in Context B and were given lights-off and chocolate milk pairings where the milk was contingent upon leverpressing during the CS.
exceptionally potent reinforcer in other studies in the lab, and it was expected to facilitate learning of the newinstrumental
contingency in Group CC/I. Additionally, it provided a very salient stimulus that was unique to the Extinction context. Some
theories predict that this should increase the likelihood of fear relapse, so nding that it actually reduced relapse might be
particularly important for these theories.
During each Extinction session, the lights-off CS was nonreinforced 4 times for Groups AAA, ABA, CC and CC/I. Groups
AAA and ABA received fear Extinction in Contexts A and B, respectively. Groups CC and CC/I received counterconditioning
in Context B. Half of the rats in Group NE were placed in each context and were allowed to leverpress for sucrose on a VI-60
schedule but were not exposed to the CS.
Fear renewal testing in Context A. Prior to fear renewal testing, all groups were given 1 day of training where leverpressing
was reinforced with sucrose to ensure that leverpressing rates were similar across groups before renewal testing. Over the
next 4 days, the lights-off CS was nonreinforced once per day to measure renewal of suppression.
Results
The suppression ratio (SR, Annau & Kamin, 1961) was used to measure fear levels throughout the study. The ratio was
determined by dividing the number of lever presses that occurred during the CS (D) by the number of responses during the
CS plus the number made during the 1-min period preceding CS onset (D+B). A SR of 0.0, 0.5 and 1.0 indicated maximal
suppression, zero suppression and responding solely during the CS, respectively. SPSS 17.0 was used for signicance testing,
and all tests were conducted with a two-tailed alpha =.05. Throughout this section, wherever group means are reported,
standard error of the mean can be found in parentheses.
Fig. 1 shows suppression on the nal trial of the Acquisition phase (A), on the rst and last trial of sessions 14 and the last
session of the Extinction phase (F and L) and each of the 4 renewal test trials (R1R4). A one-way between groups ANOVA
showed that suppression of leverpressing was similar in all of the groups at the end of the Acquisition phase, F(4,30) =2.3,
p>.07. The grand mean SR was 0.11 (.02) and individual group means varied from .06 (.04) to .16 (.06), indicating strong
suppression in all of the groups.
One-way between groups ANOVAs were also computed for the rst and the last Extinction trial. Rats in Groups NE and CC
were excluded fromthis analysis because the former group did not receive any CS presentations during Extinction and latter
group did not continue to leverpress during counterconditioning in the absence of reinforcement. The remaining groups did
not differ signicantly on the rst Extinction trial, F(2,17) <1.0, but they did differ on the nal Extinction trial, F(2,17) =37.50,
p<.01. Tukeys HSD test (using a familywise signicance level set at 0.05) conrmed that suppression was similar in Groups
AAA and ABA, p>.75 and that suppression was signicantly weaker in Group CC/I than in Group AAA or ABA, ps <.001. A
similar analysis of the pre-CS leverpressing rates revealed that the suppression ratio measure was complicated by group
differences on the nal Extinction trial, F(2,17) =5.01, p<.02. Again, Tukeys results showed that Groups AAA and ABA did
not differ, p>.99, but Group CC/I responded at a signicantly lower rate, ps <.034. The mean number of leverpresses prior to
the nal Extinction trial was 26 (2.6), 26 (3.6) and 2 (1.0) for Groups AAA, ABAand CC/I, respectively. Unlike the other groups,
Group CC/I learned to leverpress almost exclusively during the CS, the only time that a leverpress resulted in reinforcement.
The right side of Fig. 1 shows the 4 renewal test trials labeled R1R4. Recall that the rats in Group NE were divided, with
some rats in each of the two contexts during the Extinction phase. An independent t-test, t (5) =.45, p>.67, conrmed that
providing different amounts of exposure to Context A during the Extinction phase did not inuence suppression on the rst
renewal test trial. Group means were 0.04 (.03) and 0.03 (.01). Based on this result, all of the rats in Group NE were pooled
for all of the additional tests.
B.L. Thomas et al. / Learning and Motivation 43 (2012) 2434 29
A one-way between groups ANOVA indicated that groups differed on the rst renewal trial, F(4, 30) =16.96, p<.001.
Tukeys HSD test indicated that Groups AAA and CC/I did not differ, p>.99, and fear renewal in Groups AAA and CC/I was
signicantly weaker than in each of the other groups, ps <.014. Similarly, Groups ABA and CC did not differ, p>.97 and
suppression in Groups ABA and CC was signicantly reduced when compared with Group NE, ps <.03. Taken together, these
results show that the incorporation of an instrumental contingency prevented the renewal of fear that occurred following
traditional counterconditioning. Without the instrumental contingency, counterconditioning yielded the same level of fear
renewal as a conventional Extinction treatment. Finally, while a signicant amount of fear renewal occurred following
traditional counterconditioning or Extinction, each of these methods decreased fear signicantly when compared with a no
Extinction control.
To ensure that differences in the suppression ratio measure did not result fromdifferences in pre-CS leverpressing rates,
a one-way between groups ANOVA was performed using leverpressing during the 1-min prior to the rst renewal test trial.
The ANOVA failed to reveal any groups differences, F(4,30) <1.0. Mean response rates were 17 (4.6), 18 (4.9), 19 (4.1), 19
(4.4) and 12 (2.4) for Groups FC, AAA, ABA, CC/I and CC, respectively.
Discussion
The goals of Experiment 1 were to conrm the results of Peck and Bouton (1990, Experiment 1) where a traditional
counterconditioning procedure did not prevent fear renewal and to determine if the incorporation of a contingency between
leverpressing and the appetitive US might make the traditional counterconditioning procedure more effective at preventing
fear renewal. The results didconrmthose reportedby Peck andBoutondespite several differences inthe training procedure.
More specically, Peck and Bouton provided six tone and shock pairings on each of three days during Acquisition compared
with two lights-off and shock pairings on each of ve days in Experiment 1. Moreover, Peck and Bouton scheduled the
three Acquisition sessions approximately 72h apart to allowfor context exposure sessions during the intervening days. This
strategy ensured that all of their groups were equally exposed to each context throughout the experiment. In Experiment
1, Acquisition sessions were given in Context A on consecutive days and no attempt was made to equate exposure to each
context during Acquisition. During Extinction, Peck and Bouton delivered six tone and food pairings on each of three days
using the same schedule employed during Acquisition (i.e., one session every 72h with context exposure in between). In
Experiment 1, four lights-off andfoodpairings weredeliveredeachdayfor 24consecutivedays andgroups wereonlyexposed
to their designated Extinction context. Finally, in Renewal, Peck, and Bouton gave four tone presentations during a single
session compared with a single lights-off presentation per day in Experiment 1. In spite of these procedural differences, the
data fromGroup CC in Experiment 1 closely resemble the data reported by Peck and Bouton (called Group B in their paper)
showing that signicant fear renewal occurred following a standard counterconditioning treatment.
The second aimwas to learn if the addition of a contingency (that forced the subject to earn the appetitive US during the
CS) might reduce fear renewal more effectively than the standard counterconditioning procedure. Fear renewal in Group
CC/I was signicantly reduced compared with Group CC, and it did not differ signicantly from Group AAA. This suggests
that requiring the appetitive US to be earned during counterconditioning can prevent relapse more effectively than response
independent pairings of the CS with the appetitive US. The primary goal of Experiment 2 was to examine howrequiring the
US to be earned during counterconditioning might reduce fear renewal.
Experiment 2
The primary aim of Experiment 2 was to determine if the instrumental contingency that was incorporated into the
counterconditioning procedure had to involve the same behavior assessed during the Acquisition and renewal phases (i.e.,
leverpressing) or if requiring another, novel response would prevent fear renewal as completely. Several reports have shown
that providing a discrete CS from the Extinction phase (i.e., a reminder cue) during the renewal test can improve the gen-
eralization of fear Extinction from the Extinction context to the renewal test context (Brooks & Bouton, 1994; Collins &
Brandon, 2002). In Experiment 1, requiring rats in Group CC/I to leverpress during the CS might have increased the amount
of attention directed towards the lever compared with Group CC where leverpressing was inconsequential and extinguished
very quickly. As a result, the presence of the lever during the renewal test might have acted as a potent reminder cue of the
Extinctioncontext for GroupCC/I, but not for GroupCC, resulting inthe differences insuppressionthat were observed. To test
this idea, a second manipulandumwas added to the operant chambers and an additional counterconditioning group, Group
CC/I/diff, was reinforced for making different responses during Acquisition and counterconditioning. If the manipulandum
employed during counterconditioning can serve as a reminder cue during the renewal test, one might expect that requiring
a novel response to a newmanipulandumwould be more effective than requiring the same response to the same manipu-
landumthat was reinforced during the Acquisition phase. In the former case, the manipulanda are associated differentially
with the presence or absence of shock and in the latter case a single manipulandum is associated with the presence and
absence of shock. Additionally, in Experiment 1, Group CC received more appetitive USs during the Extinction phase than
Group CC/I because Group CC received the USs regardless of their behavior and Group CC/I had to earn them. While it is
not clear why a greater number of appetitive USs would reduce the effectiveness of counterconditioning, in Experiment 2, a
30 B.L. Thomas et al. / Learning and Motivation 43 (2012) 2434
Fig. 2. Mean suppression on the last trial of the Acquisition phase (A), the rst (F) and last (L) trials of each session of the Extinction phase (gaps indicate
breaks between daily sessions), and the four trials of the Renewal phase (R1R4). In Context A, all groups received lights-off and shock pairings during the
Acquisition phase and lights-off without shock during the renewal phase. Groups were given different procedures during the Extinction phase: Groups ABA
and AAA were placed in Contexts B and A, respectively and were given nonreinforced exposure to the lights-off CS, Group CC was placed in Context B and
given lights-off and chocolate milk pairings and Groups CC/I and CC/I/diff were placed in Context B and were given lights-off and chocolate milk pairings
where the milk was contingent upon leverpressing or chainpulling during the CS. For Group CC/I, the same response was reinforced during Acquisition and
Extinction. For Group CC/I/diff, the response reinforced during Acquisition differed fromthe response reinforced during Extinction.
yoking procedure was implemented to ensure that the number and timing of appetitive USs given during the feared CS was
equated during the Extinction phase in each of the counterconditioning groups.
Method
Subjects
The subjects were 40 experimentally naive, 90-day-old SpragueDawley rats that were bred at BaldwinWallace College.
Each group had 5 males and 3 females. During the week prior to onset of the study, free feeding weights varied from452 to
639g in males and 264 to 407g in females. All housing and maintenance conditions were the same as in Experiment 1.
Apparatus
The equipment described for Experiment 1 was used in Experiment 2, with one important change. An 11.5cm metal
chain was suspended fromthe center of the lid of the operant chamber. The response lever and the newly added chain were
present throughout the study for all groups. Chainpulling and leverpressing were the dependent variables in this study.
Procedure
The procedure resembledthat of Experiment 1witha fewsignicant exceptions. First, during preliminary training, all rats
were shaped during separate sessions to leverpress and to chainpull on the VI-60 schedule for sucrose. Next, in Acquisition,
the leverpress response was reinforced with sucrose for half of the rats in each group (the chainpull was not) and for the
remaining rats the reverse was true. Third, in Extinction, the effective response did not change for Groups AAA, ABA and CC/I
(they were trained just as they were in Experiment 1), but Group CC/I/diff was required to switch to whichever response had
been ineffective during the Acquisition phase to earn the chocolate milk. Additionally, a yoking procedure was implemented
during the Extinction phase where 4 rats fromGroup CC were yoked to 4 rats (selected randomly) fromGroup CC/I and the
remaining 4 rats fromGroup CC were yoked to 4 rats fromGroup CC/I/diff. When the rat in Group CC/I or CC/I/diff responded
on the effective manipulandumduring the CS, it raised the dipper of chocolate milk in its own box and simultaneously raised
the dipper for its yoked control rat in Group CC. This ensured that each pair of rats received the same total number and timing
of CS-US pairings throughout the Extinction phase. The remaining 4 rats in Groups CC/I and CC/I/diff were not yoked with
another rat. As in Experiment 1, each group in Experiment 2 received four nonreinforced lights-off presentations per session
and 24 Extinction sessions were conducted. Lastly, on the day prior to the renewal phase and throughout the four sessions of
the renewal phase, yoking was eliminated and each rat could respond to either manipulanda to receive sucrose on a single
VI-60 schedule (meaning that rats could not earn more than 60 reinforcers per hour by alternating responses to the lever
and chain). This was the only contingency in place and was intended to resemble the preliminary training and Acquisition
conditions. This also ensured that rats were responding sufciently throughout the session to allow for measurement of
conditioned suppression during the fear renewal test.
Results
Fig. 2 shows suppression on the nal trial of the Acquisition phase (A), on the rst and last trial of sessions 14 and the last
session of the Extinction phase (F and L) and each of the 4 renewal test trials (R1R4). A one-way between groups ANOVA
showed that suppression of responding to the effective manipulandum(i.e., lever or chain) was similar in all of the groups
B.L. Thomas et al. / Learning and Motivation 43 (2012) 2434 31
Fig. 3. Mean change in the number of responses made to the manipulanda that had been effective or ineffective during the Extinction phase. For Groups
CC/I and CC/I/diff, the effective instrumental response had resulted in chocolate milk during the CS, but not in the CS absence. For Group CC, chocolate milk
was given independent of behavior so neither response had been effective during the extinction phase. For the remaining groups, the effective instrumental
response had resulted in sucrose on a VI-60s schedule. Values reect differences between the number of responses made during the CS minus the number
made in an equivalent period immediately prior to CS onset.
at the end of the Acquisition phase, F(4,35) <1. The overall mean SR was 0.07 (.02) and Group means varied from.04 (.02) to
.12 (.06), indicating that suppression was strong in all of the groups.
One-way between groups ANOVAs were also computed for the rst and the last Extinction trial. Again, Group CC was
excluded from this analysis. The remaining groups did not differ signicantly on the rst Extinction trial, F(3,267) =1.04,
p>.35, but they did differ on the nal Extinction trial, F(3,27) =68.62, p<.001. Follow-up Tukeys HSD tests conrmed that
suppression was similar in Groups AAA and ABA, p>.99 and in Groups CC/I and CC/I/diff, p>.57 and that suppression was
signicantly weaker in Groups CC/I and CC/I/diff than in Groups AAA or ABA, ps <.001. A similar analysis of the pre-CS
response rates revealed that the suppression ratio measure was complicated by group differences on the nal Extinction
trial, F(3,27) =16.49, p<.001. The mean number of responses to the effective manipulandumprior to the nal Extinction trial
was 25 (5.7), 28 (4.7), 1 (.01) and 1.4 (.18) for Groups AAA, ABA, CC/I and CC/I/diff, respectively. As in Experiment 1, the rats
in Group CC/I learned to respond predominantly during the CS when the response was reinforced. Group CC/I/diff behaved
similar to CC/I despite the change in the response contingencies.
The right side of Fig. 2 shows the 4 renewal test trials labeled R1R4. Since rats in each group could either leverpress or
chainpull, a suppression ratio was calculated using the total number of responses across both manipulanda. Based on the
results from Experiment 1, signicant fear renewal was expected in Groups ABA and CC but not in Groups AAA and CC/I.
A one-way between groups ANOVA indicated that groups differed on the rst renewal trial, F(4,34) =5.58, p<.01. Tukeys
HSD test showed that suppression was not signicantly different in Groups AAA, CC/I and CC/I/diff, ps >.79. Moreover, fear
renewal was signicantly reduced in Groups AAA, CC/I and CC/I/diff when compared with Groups ABA and CC, ps <.026.
Groups ABA and CC did not differ, p>.98. Taken together, these results replicate and extend the ndings of Experiment
1. More specically, traditional counterconditioning and Extinction procedures resulted in a signicant amount of fear
renewal. However, the modied counterconditioning procedure prevented fear renewal. Furthermore, the similarity of the
data in Groups CC/I and CC/I/diff shows that the instrumental response employed during the modied counterconditioning
treatment could be the same response required during Acquisition in Context A or it could be a novel instrumental response
only required during Extinction in Context B.
Toensurethat differences inthesuppressionratiomeasuredidnot result fromdifferences intherateof pre-CSresponding,
a one-way between groups ANOVA was performed using the total number of responses made during the 1-min prior to the
rst renewal test trial. The ANOVA failed to reveal any group differences, F(4,34) <1.0. Mean response rates were 38 (6.9),
31 (4.4), 36 (7.5), 34 (6.9) and 38 (7.6) for Groups CC/I/diff, CC, AAA, CC/I and ABA, respectively.
Since fear renewal was prevented equally well in Groups CC/I and CC/I/diff, an additional analysis was conducted with
the aimof identifying any differences in howrats in these groups behaved toward each of the two response options before
and during the CS on the rst renewal test trial. Fig. 3 represents how responding was impacted by CS onset. Remember
that for Groups AAA, ABA and CC/I, the effective response was the same during the Acquisition and Extinction phases so it
was expected that nearly all of the pre-CS responding would be directed toward whichever response had been effective. In
contrast, for Group CC/I/diff, the effective response changed between Acquisition and Extinction so responding to either the
chain or lever might be expected. Finally, for Group CC, since neither response was effective during Extinction, whichever
response had been effective during Acquisition was expected to occur during the renewal test. For Group CC, Effective in
Fig. 3 refers to the response that produced reinforcement during the Acquisition phase, but for all other groups, effective
refers to the Extinction phase.
As expected, rats in Groups CC, AAA and ABA responded almost exclusively to the manipulandumthat had been effective
during Acquisition and Extinction. CS onset caused a suppression of that responding in Groups ABA and CC (reected in the
graph as a large negative change in responding), but not in Group AAA. Interestingly, Group CC/I responded similarly to the
effective and ineffective manipulanda before the CS onset and CS onset reduced each response moderately. This is consistent
32 B.L. Thomas et al. / Learning and Motivation 43 (2012) 2434
with the small, but nonsignicant, fear renewal effect shown in Fig. 2. Finally, Group CC/I/diff also responded similarly to
the effective and ineffective manipulanda before the CS onset and CS onset caused a reduction in responding to the manipu-
landumthat had been effective during Acquisition and a smaller increase in responding to the manipulandumthat had been
effective during Extinction. Planned comparisons of the pre-CS and CS response rates of Groups CC/I and CC/I/diff revealed
that CS onset caused signicant suppression of the response that had been ineffective during Extinction, smaller t(7) =2.75,
p<.03, but didnot cause signicant change inthe response that hadbeeneffective during Extinction, larger t(7) =1.53, p>.17.
This suggests that making the appetitive US contingent upon a behavior is necessary for counterconditioning to prevent fear
renewal.
Discussion
Experiment 2 showed that incorporation of a contingency between a response and the appetitive US was necessary for
counterconditioning to prevent fear renewal and that the particular response required during counterconditioning could be
the baseline response that rats had made during Acquisition or an alternative response. Finally, the use of a yoking procedure
eliminated the possibility that differences in the number of pairings of the CS and appetitive US could account for differences
between the standard and modied counterconditioning procedures.
General discussion
A reviewof the literature on counterconditioning of fear in animals revealed a lack of consistency across laboratories and
paradigms. One of the goals of this pair of studies was to establish a training procedure that reliably produced countercondi-
tioning of fear in rats. Two observations were required for counterconditioning to be considered effective. First, the fearful
response to the CS (suppression of behavior) had to be replaced by a food directed response (leverpressing or chainpulling)
to show that a new CS-food association had developed. Second, the CS-food association had to generalize to a context that
differedfromthe counterconditioning context. Capaldi et al. (1983) reasonedthat providing foodduring the Extinctionphase
and then removing that food during the Renewal phase would allowthe learner to use the absence of food as a predictor of
shock and would increase fear renewal. In each of the ABA experiments described here, the physical context was changed
between each phase, as was the type of reinforcer (sucrose or chocolate milk) and in Experiment 2, for Group CC/I/diff, the
response requirement. Yet, both of the experiments suggest that the modied counterconditioning procedure established a
food directed response that generalized fromExtinction Context B to the Acquisition and Renewal Context A. These ndings
seemto challenge the idea that counterconditioning simply increases the ambiguity of the CS and that animals resolve the
ambiguity using contextual stimuli. To our knowledge, this is the rst demonstration that counterconditioning can be used
to prevent fear renewal in any non-human species, and it should be added to a growing list of behavioral strategies that
have been shown to attenuate or thwart fear renewal.
Behavioral strategies that reduce fear renewal generally fall into one of three categories. The most common are strategies
that involve nonreinforcement of the CS alone. For example, Denniston, Chang, andMiller (2003) showedthat nonreinforcing
the CS a very large number of times reduced renewal more than a fewer number of exposures, and Urcelay et al. (2009)
showed that nonreinforcing the CS with longer interstimulus intervals reduced renewal more than an equivalent number
of massed exposures. Both of these studies should be taken with some caution because other researchers have failed to nd
similar results (see Cain, Blouin, & Barad, 2003; Rauhut, Thomas, & Ayres, 2001; Tamai & Nakajima, 2000). In contrast, there
seems to be more widespread agreement that nonreinforcing the CS in a variety of contexts decreases fear renewal more
than nonreinforcement in a single context (Chelonis, Calton, Hart, & Schachtman, 1999; Gunther, Denniston, & Miller, 1998;
Thomas, Vurbic, & Novak, 2009; but see Bouton, Garcia-Gutierrez, Zilski, & Moody, 2006).
The second category involves nonreinforcement of the CS in compound with other feared stimuli. In these studies, the
researcher deliberately establishes fear of either the Extinction context (Rauhut et al., 2001) or a discrete stimulus (Thomas
& Ayres, 2004). The target CS is then nonreinforced in the presence of these additional fear-inducing stimuli with the aimof
deepening extinction of the target CS. Results showed that nonreinforcing a target CS in compound with other fear-inducing
stimuli reduces renewal of fear to the target CS.
The nal category involves pairing the target CS with an appetitive US during extinction. The two experiments presented
here suggest that this strategy can effectively reduce renewal if the appetitive US is earned during the CS rather than
provided freely. While systematic desensitization has been employed extensively in clinical settings with humans (Foa,
Steketee, & Ascher, 1980), prior research with animals made it unclear why systematic desensitization would be effective as
a treatment and how it could prevent relapse of fear outside of the treatment setting. For example, the theoretical work of
Bouton and his associates assumes that circumstances (i.e., physical, temporal, procedural) that are unique to the Extinction
phase of training should increase the likelihood of fear renewal when those circumstances are not in place (Bouton, Woods,
Moody, Sunsay, & Garcia-Gutierrez, 2006). In the present experiments, rats in the modied counterconditioning procedure
experienced changes in the physical environment, the type of reinforcer and the reinforcement schedule, the timing of the
CS exposures and, in one case, had to make an entirely different response to earn the reinforcer. Additionally, these rats were
then placed back into the Acquisition context for renewal testing. All of these features that were distinctive to the Extinction
phase should have greatly increased the probability of fear renewal and instead, they thwarted fear renewal more than
procedures where the conditions were more similar in Acquisition, Extinction and Renewal.
B.L. Thomas et al. / Learning and Motivation 43 (2012) 2434 33
Across the present pair of studies, fear renewal was prevented in Groups CC/I and CC/I/diff, but signicant, comparable
amounts of fear renewal occurred in Groups ABA and CC. Three variables that might account for this pattern of results are:
the presence or absence of a response requirement, the availability of the appetitive US and the type of appetitive US used. To
illustrate, Groups CC/I and CC/I/diff had to earn the appetitive US, but Group CC was given the same appetitive US freely. This
shows that a response requirement was a necessary component of effective counterconditioning. However, the addition of
a response requirement may not be a sufcient condition to prevent fear renewal because Group ABA was also required to
earn reinforcement (sucrose rather than chocolate milk) during the Extinction phase and this did not prevent fear renewal.
Second, Groups CC/I and CC/I/diff were only able to earn the appetitive US during the CS periods, but Group ABA could
earn the appetitive US throughout the session. This shows that restricting the availability of the US to the CS periods may be
a necessary component of effective counterconditioning. However, restricting the US to the CS periods is also not a sufcient
condition because Group CC only received the US during CS periods and fear renewal still occurred.
Finally, the type of appetitive US might have been an important variable. Groups CC/I and CC/I/diff were able to earn
chocolate milk and Group ABA was able to earn sucrose. While chocolate milk may have been a more effective reinforcer of
behavior than sucrose, it is also an insufcient explanation of the results because Group CC also received chocolate milk and
fear renewal occurred.
Experiment 2 also showed that fear renewal was prevented when the response required during counterconditioning
was the same as the baseline response used during Acquisition or an alternative response. However, closer examination
of the rats behavior during the renewal test suggests that reinforcing an alternative response may be a better strategy
than reinforcing the same response that served as a baseline behavior during Acquisition. More specically, Group CC/I
and CC/I/diff responded at similar rates to the effective and ineffective manipulanda prior to CS onset. At CS onset, Group
CC/I showed some suppression of each response (although not as strongly as in Groups ABA or CC). Group CC/I/diff also
suppressed the response that had been ineffective during counterconditioning, but increased slightly the response that
had been effective during counterconditioning. This suggests that residual fear of the CS may be less able to disrupt an
instrumental response that was only reinforced during the Extinction phase.
To summarize, the present set of studies showed that a modied counterconditioning procedure prevented fear renewal
in rats. To our knowledge, this is an original contribution to a growing body of animal research on behavioral strategies for
preventing relapse of fear. The full mechanism of counterconditioning could not be uncovered by these rst two studies,
but it seems that effective counterconditioning requires the appetitive US to be earned in the presence of the feared CS.
Interestingly, Rauhut et al. (2001) showed that a Pavlovian conditioned inhibition (CI) procedure, a differential conditioning
(DC) procedure and an explicitly unpaired (EU) procedure prevented ABA fear renewal. In all of those procedures, the feared
CS came to signal a limited time period when it was safe to earn the appetitive US (i.e., when the shock would not occur).
As in Groups CC/I and CC/I/diff, this should have encouraged rats to respond during the CS and to be reinforced for doing
so. The difference between CI, DC and EU and countercondititioning is that in the former, the CS signaled that it was now
safe to earn the appetitive US (that was also available at other times) and in the latter the CS signaled that it was now
worth responding because the appetitive US was only available during that time. Collectively, these procedures imply that
transforming a feared CS into a positive discriminative stimulus for instrumental behavior may prevent fear renewal more
completely than conventional extinction where the CS might only signal the absence of an aversive US.
Future researchshouldinclude anABAgroupthat is only allowedtoearnsucrose during the CS anda CC/I groupreinforced
with sucrose rather than chocolate milk. These groups would allowassessment of the relative importance of the availability
and type of the appetitive US used. Additionally, fear relapse should be assessed using additional tests such as reinstatement
and retardation testing.
Acknowledgments
We thank Tina Stuart and Steven Mueller for their help running Experiment 3. We also thank Dr. John Ayres for his careful
reviewof a draft of the manuscript and Dave Revta for technical support throughout these studies.
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