Although the role of the amygdala in acquisition of conditioned fear is well established, there is debate concerning the intra-amygdala
not, suggesting that the BA is not normally involved in fear conditioning. If true, posttraining BA lesions should also have no effect.
Replicating previous studies, we found that rats given electrolytic BA lesions before training acquired conditioned fear normally. They
also showed normal long-term retention and extinction of conditioned fear. Unexpectedly, BA lesions made after training completely
It is well established that the amygdala is critical for the acquisi-
cuits involved in this process are unclear (Nader et al., 2001; Koo
et al., 2004). The lateral nucleus of the amygdala (LA) receives
information about conditioned and unconditioned stimuli (CSs
site of plasticity in fear conditioning (Ressler et al., 2002; Lam-
precht and LeDoux, 2004; Maren and Quirk, 2004). Potentiated
LA outputs are thought to drive neurons in the medial subdivi-
al., 1988; De Oca et al., 1998; Davis, 2000).
There has been debate, however, concerning the route by
whichtheLAinfluencestheCeM(Pare ´ etal.,2004).TheLAlacks
direct projections to the CeM but projects to the basal amygdala
[BA; defined as the basolateral (BL), basomedial (BM), and ac-
cessory basal (AB) nuclei], which in turn projects to the CeM
(Pitkanen et al., 1997; Pare ´ and Smith, 1998). This suggests that
the LA influences the CeM dysynaptically via the BA (LeDoux,
1995). However, pretraining BA lesions have little effect on fear
conditioning (Amorapanth et al., 2000; Goosens and Maren,
2001; Nader et al., 2001), suggesting that the LA can also influ-
ence the CeM through other routes (LeDoux, 2000). Based on
these pretraining lesion data, it was concluded that the BA is not
involved in simplefearconditioning
Amorapanth et al., 2000). Although one might expect posttrain-
always the case (Rosen et al., 1992; Campeau and Davis, 1995;
Corodimas and LeDoux, 1995; Rudy et al., 2004). To fully evalu-
of pretraining and posttraining lesions of BA.
acquisition of conditioned fear, it may be involved in extinction
of fear. Inhibition of NMDA receptors (Falls et al., 1992; Lee and
Kim, 1998), mitogen-activated protein kinase (Lu et al., 2001),
phosphatidylinositol 3? kinase (Lin et al., 2003), or protein syn-
thesis (Lin et al., 2003) in the BA and LA prevents extinction. In
infralimbicprefrontalcortex(IL)(McDonald,1991;Conde ´ etal.,
1995), a structure implicated in consolidation and storage of ex-
tinction memory (Morgan et al., 1993; Herry and Garcia, 2002;
Milad and Quirk, 2002; Hugues et al., 2004; Santini et al., 2004).
We therefore examined the effect of BA lesions on extinction of
conditioned fear with an experimental design used previously to
viously acquired fear memory.
All experimental protocols for this study were approved by the Institu-
9680 • TheJournalofNeuroscience,October19,2005 • 25(42):9680–9685
in compliance with the National Institutes of Health guidelines for the
care and use of laboratory animals.
ing ?300 g. They were housed individually in transparent polyethylene
cages in a negative-pressure Biobubble (Colorado Clean Room, Fort
water. Food was restricted to 18 g per day of rat chow until they reached
food on a variable interval schedule (VI-60). Bar pressing on a variable
reinforcement schedule maintains a constant behavioral background
against which freezing responses can be measured more reliably (Quirk
et al., 2000; Lebron et al., 2004).
training, were performed in the same chamber. The chamber was 25 ?
29 ? 28 cm, with aluminum and Plexiglas walls (Coulbourn Instru-
ments, Allentown, PA). The floor consisted of 0.5-cm-diameter stainless
steel bars spaced at 1.8 cm through which a mild footshock US was
delivered. A response lever was positioned 6.5 cm above the floor, and a
speaker was mounted on the outside wall opposite the lever for the de-
livery of tone CSs. The chamber was situated inside a sound-attenuating
box, which contained a ventilation fan, and was illuminated by a single
Surgery. Rats were anesthetized with ketamine (90 mg/kg, i.p.) and
xylazine (10 mg/kg, i.p.) and placed into a stereotaxic apparatus (David
Kopf Instruments, Tujunga, CA). Supplemental doses of ketamine were
given as needed to maintain a deep level of anesthesia, as indicated by a
slow respiratory rate and lack of response to tail pinch. Electrolytic le-
sions were made using an insulated wire electrode (0.25 mm diameter)
of the amygdala, modified from Amorapanth et al. (2000). The coordi-
nates for each lesion were as follows (in mm): anteroposterior: 2.1, 2.8,
3.3, 4.1; mediolateral: 4.9, 4.9, 5.3, 5.3; dorso-
ventral: 9.1, 9.3, 9.2, 9.3. A current intensity of
lesion. For sham-operated rats, the electrode
was lowered 3 mm ventral to bregma, and no
current was passed. To manage postoperative
pain, Buprenex (0.025 mg/kg) was injected
a loudness of 75 dB and a frequency of 4 or 1
kHz. During conditioning, each tone cotermi-
nated with a 0.5 mA, 0.5 s footshock US. In a
single day, rats received 5 habituation tones,
followed by 7 conditioning tones, followed by
20 extinction tones. Depending on the experi-
conditioning. The mean intertrial interval was
4–6 min throughout the experiment.
Histology. After each experiment, rats re-
ceived an overdose of sodium pentobarbital
(100 mg/kg) and were perfused intracardially
with 0.9% saline, followed by buffered forma-
lin. The brains were removed and stored for
sections (40 ?m thick) were cut with a mic-
rotome and stained with cresyl violet. Digitized
images of the tissue were acquired with an
lesion contours were traced onto drawings
from a stereotaxic atlas (Paxinos and Watson,
1998). The percentage of damage to the BA for
each rat was calculated with MetaMorph image
analysis software (Universal Imaging, Down-
on anatomical criteria were made blind with
respect to the experimental results.
Data analysis. Freezing to the CS was mea-
sured with a stopwatch from different video
The data were analyzed in blocks of two trials. Suppression of bar press-
ing was calculated as follows: suppression ratio ? (pretone rate ? tone
rate)/(pretone rate ? tone rate). A ratio of 0 indicates no suppression,
and 1 indicates maximal suppression. Freezing and suppression values
were compared with a Student’s t test.
The BA was defined to include the BL, BM, and AB nuclei (Paxi-
lesion group were (1) greater than ?40% destruction of the BA
of damage to the BA (bilaterally) in these 22 rats was 60.7% (36.3–
91.1%). In most cases, the BM and AB nuclei were completely de-
BA lesions made before training had no effect on acquisition of
conditioned fear. As shown in Figure 2A, sham-operated and
BA-lesioned rats exhibited similar levels of conditioned freezing
(58 and 59%) and suppression of bar pressing (0.69 and 0.68) at
the start of extinction, confirming previous reports that BA le-
and Maren, 2001; Nader et al., 2001). In addition, both groups
showed equivalent extinction, reaching negligible levels of freez-
ing and suppression in the final block of extinction (lesioned,
Paxinos and Watson (1998). B, Micrograph showing a representative BA lesion. C, Coronal sections through the rostrocaudal
with delay. The smallest lesion is represented by the dark shading, whereas the largest lesion is outlined but not shaded. CE,
Examples of electrolytic BA lesions. A, The BA was defined to include the BL, BM, and AB nuclei, modified from
Anglada-FigueroaandQuirk•BasalAmygdalaandExpressionofConditionedFear J.Neurosci.,October19,2005 • 25(42):9680–9685 • 9681
19% freezing; sham, 13% freezing; t(17)?
0.75; p ? 0.46). On day 2, spontaneous
recovery of freezing (measured as a per-
centage of maximal freezing acquired on
day 1) was similar in sham and lesioned
p ? 0.58). Thus, BA lesions did not pre-
vent acquisition or extinction of condi-
We next performed posttraining BA le-
sions, reasoning that previous condition-
ing might alter the function of BA with
respect to expression of conditioning or
extinction (Campeau and Davis, 1995).
Surgery was performed 2 d after condi-
before testing on day 10. Posttraining BA
lesions dramatically reduced the expres-
sion of conditioned fear to the tone (Fig.
2B). Lesioned rats dropped from 62%
ter surgery (t(8)? 6.45; p ? 0.001),
whereas sham-operated rats remained the
same (before surgery, 75%; after surgery,
76%). Similarly, bar-press suppression
was reduced in lesioned rats after surgery
(before surgery, 0.89; after surgery, 0.39;
t(8)? 3.66; p ? 0.006), whereas sham-
gery, 0.97; after surgery, 0.94). BA lesions
did not affect the rate of spontaneous bar
pressing (sham, 18 per minute; lesioned,
14 per minute; t(20)? 0.67; p ? 0.51), in-
dicating that reduced freezing was not at-
for food. Thus, posttraining lesions re-
vealed a role for the BA in the recall of
previously acquired fear associations.
Despite their inability to express previ-
ously learned fear, BA-lesioned rats were
able to recondition to a new CS (Fig. 3A).
Sham-operated and BA-lesioned animals
showed similar levels of acquired freezing
0.34) and suppression (0.57 and 0.62;
t(11)? 0.21; p ? 0.84) at the end of recon-
ditioning, which did not differ signifi-
lesioned and sham-operated rats showed
savings in the rate of reconditioning (Fig. 3B), suggesting gener-
alization between tones and some degree of preserved memory
for initial training in lesioned rats. There was a trend toward
suppression at the end of extinction differed significantly be-
tween groups (shams, 22%; lesions, 3%; t(11)? 1.67; p ? 0.12;
shams, 0.33; lesions, 0.12; t(11)? 1.25; p ? 0.24). The trend
toward faster re-extinction in lesioned rats is consistent with loss
of memory for the original conditioning.
not lowered into the amygdala in sham-operated rats (see Mate-
rials and Methods). To investigate this possibility, we prepared a
separate group of rats with posttraining sham operations, lower-
ing the electrode through the LA into the BA (n ? 5). Sham-
were not statistically different in any phase. B, Percentage of freezing to the tone (top) and suppression ratio (bottom) for
damage to the LA as the cause of blocked expression (blocks of two trials are plotted). B, Rates of conditioning (day 1) and
reconditioning (day 18) are compared for sham-operated (top) and BA-lesioned (bottom) rats. In both groups, savings was
observed in the rate of reconditioning, suggesting generalization between tones and some degree of preserved memory in
9682 • J.Neurosci.,October19,2005 • 25(42):9680–9685Anglada-FigueroaandQuirk•BasalAmygdalaandExpressionofConditionedFear
surgery, 76%; t(4)? 1.47; p ? 0.22), indicating that track-related
damage in the LA was not responsible for the reduced freezing
seen with posttraining BA lesions.
Another possible explanation for the BA lesion deficit con-
the first experiment but 8 d in the second experiment, because of
postsurgery recovery. It is possible, therefore, that rats with pre-
training BA lesions could acquire conditioned fear but could not
retain fear memory for 8 d. If so, this would suggest that post-
training lesions of the BA might have removed an essential long-
term storage site. Because previous studies of BA lesions mea-
sured retention at 24 h only (Amorapanth et al., 2000; Goosens
rats with BA lesions are capable of retaining fear memory over a
an 8 d delay between training and testing. BA lesions under these
10 (Fig. 4). Sham-operated (n ? 8) and lesioned (n ? 5) rats
89%, respectively; t(11)? 0.40; p ? 0.69). Eight days later, freez-
ing levels in both groups remained unchanged (sham, 84%; le-
sion, 85%; t(11)? 0.10; p ? 0.92), indicating that the passage of
fact that rats with pretraining BA lesions can form long-lasting
fear associations suggests that deficits caused by posttraining BA
retain fear memory over the recovery period.
We have revisited the issue of the intra-amygdala circuits in fear
conditioning, by comparing the effects of pretraining and post-
training lesions of the BA on the acquisition and expression of
conditioned fear. Replicating previous reports, we found that
pretraining BA lesions had no effect on acquisition of condi-
BA lesions can retain fear memory for at least 8 d. Unexpectedly,
posttraining BA lesions completely abolished conditioned fear,
suggesting that in the intact brain, the BA serves a critical role in
Pretraining lesions of the BA also had no effect on the extinc-
ilar results were reported recently by LeDoux and colleagues
(Sotres-Bayon et al., 2004). Thus, it appears that BA is not an
essential site of extinction-related plasticity because rats with
damage to the BA can still learn extinction. However, the role of
posttraining lesions of the BA blocked expression of conditioned
lesions on extinction must be viewed with caution.
Another possible site of extinction-related plasticity in the
amygdala is the LA (Sotres-Bayon et al., 2004). Pharmacological
manipulations of the BLA (BA plus LA) prevent extinction (Falls
et al., 1992; Lu et al., 2001; Lin et al., 2003), and the LA shows
extinction-induced upregulation of immediate-early genes
(Conde ´ etal.,1995;Vertes,2004),andrecentdatasuggestthatthe
IL is a site of consolidation of extinction memory (Milad and
Quirk, 2002; Hugues et al., 2004; Santini et al., 2004) (but see
Gewirtz et al., 1997). These two structures may work together to
acquire, store, and express extinction (Maren and Quirk, 2004).
Another possible source of extinction plasticity in the amygdala
are GABAergic intercalated (ITC) cells, which receive glutama-
tergic inputs from the LA and BA (Royer et al., 1999) and inhibit
CeMoutputneurons(Pare ´ etal.,2004).ITCcellsreceiveaprom-
inent projection from the IL (McDonald et al., 1996; Pinto and
tion (Royer and Pare ´, 2003), consistent with a role in extinction
expression and storage.
The most surprising finding from this study was that post-
training BA lesions completely blocked expression of condi-
tioned fear, whereas pretraining lesions had no effect. One pos-
sible explanation is that the BA is the preferred output pathway
ing lesions of the BA have no effect demonstrates that the LA can
conditioning-related plasticity and can access the CeM indepen-
dently of the BA, there should be no effect of pretraining or
posttraining BA lesions. It is also unlikely that our effects are
attributable to interruption of fibers of passage originating in
adjacent cortical areas such as the perirhinal cortex or auditory
cortex, because tracing studies show that these areas project ei-
ther exclusively to the LA (Romanski and LeDoux, 1993) or to
both the LA and BA (McDonald and Jackson, 1987; Shi and Cas-
Instead, our findings suggest that the LA–Ce system is not
sufficient to support fear conditioning in the intact brain, al-
though it is sufficient in the damaged brain. Under normal con-
CeM. In support of this, neurons in the BA show associative
plasticity during fear conditioning (Maren et al., 1991; Toyo-
mitsu et al., 2002). This suggests that infusions of the NMDA
receptor antagonist APV into the BLA, which prevents acquisi-
tion of fear conditioning (Miserendino et al., 1990; Fanselow et
to the CeM. The CeM receives projections from the BA, the me-
dial geniculate nucleus (MGm) of the thalamus (Pare ´ et al.,
2004),andtheLAviaITCcell-mediateddisinhibition(Pare ´ etal.,
2004). Recent studies suggest that the CeM is an essential site of
Maren,2003;Pare ´ etal.,2004).Long-termpotentiationhasbeen
observed in the projections from the BA to the CeM (Fu and
son and Pare ´, 2005). Thus, the CeM appears to be a site of con-
The pattern of lesion effects we observed (after training but
not before training) has been observed in other systems, such as
the perirhinal cortex in auditory fear conditioning (Rosen et al.,
Anglada-FigueroaandQuirk•BasalAmygdalaandExpressionofConditionedFearJ.Neurosci.,October19,2005 • 25(42):9680–9685 • 9683
the hippocampus in contextual fear conditioning (Maren et al.,
when present but dispensable if removed before learning? This
apparent paradox could be explained by competition between
parallel inputs, such that learning in one input inhibits learning
in other inputs to the same cell.
In support of this, recent physiological evidence suggests that
homeostatic control mechanisms dynamically adjust synaptic
strength to promote stability across multiple inputs (Buzsaki et
al., 2002; Royer and Pare ´, 2003; Turrigiano and Nelson, 2004).
For example, BA inputs to the CeM might gain a disproportion-
pared with other inputs (Fig. 5). Posttraining lesions of the BA
the conditioned response. In contrast, pretraining lesions would
be compensated for by increased plasticity among the remaining
inputs to the CeM, such as the MGm, which could then support
fear behavior. The LA also projects to the CeM but indirectly via
a chain of ITC cells thought to signal the CS by disinhibiting the
CeM(Pare ´ etal.,2004).Aninterestingpredictionofthismodelis
that posttraining lesions of the medial subdivision of the MG,
which normally have no effect (Campeau and Davis, 1995),
would block the expression of conditioned fear in rats that re-
ceived pretraining lesions of the BA.
Among the mechanisms that could account for this type of
heterosynaptic interaction is synaptic scaling in which decreases
number of AMPA and NMDA receptors at the remaining syn-
apses (Watt et al., 2000; Turrigiano and Nelson, 2004). This reg-
ulatory process is thought to occur over a time period of several
days, consistent with postlesion recovery time. If true for the
CeM, lesions of the BA would trigger a gradual increase in the
number of NMDA receptors at the remaining synapses onto
the CeM, making them more likely to exhibit plasticity during
mine whether CeM neurons show such heterosynaptic interac-
ral systems in which lesions cause deficits when performed after,
but not before, training.
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