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The Contribution of the Amygdala to Aversive and Appetitive Pavlovian Processes

Justin M. Moscarello and Joseph E. LeDoux
Emotion Review 2013 5: 248
DOI: 10.1177/1754073913477508
The online version of this article can be found at:
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477508
2013

EMR5310.1177/1754073913477508Emotion ReviewMoscarello and LeDoux Pavlovian Processes and the Amygdala

The Contribution of the Amygdala to Aversive

and Appetitive Pavlovian Processes

Emotion Review
Vol. 5, No. 3 (July 2013) 248253
The Author(s) 2013
ISSN 1754-0739
DOI: 10.1177/1754073913477508
er.sagepub.com

Justin M. Moscarello
Joseph E. LeDoux

Center for Neural Science, New York University, USA

Abstract
Pavlovian cues predict the occurrence of motivationally salient outcomes, thus serving as an important trigger of approach and
avoidance behavior. The amygdala is a key substrate of Pavlovian conditioning, and the nature of its contribution varies by the
motivational valence of unconditioned stimuli. The literature on aversive Pavlovian learning supports a serial-processing model
of amygdalar function, while appetitive studies suggest that Pavlovian associations are processed through parallel circuits in the
amygdala. It is proposed that serial and parallel forms of information processing can be attributed to differential recruitment of
amygdalar nuclei, with emphasis placed on the lateral amygdala.

Keywords
amygdala, appetitive, aversive, motivation, Pavlovian conditioning

Motivational states direct and energize animal behavior (Bindra,

1969; Hull, 1943), and are generally considered along a bivalent
continuum, spanning from appetitive to aversive (Bindra, 1969).
Approach and avoidance behaviors, designed to attain appetitive goal states or minimize aversive outcomes, are often guided
by environmental cues (Berridge, 1999; Bindra, 1969), which
can acquire their motivational valence through a process of
Pavlovian conditioning. This form of learning occurs when a
previously neutral conditioned stimulus (CS), such as a light or
a tone, comes to predict an unconditioned stimulus (US) with an
inherent motivational value, such as a food morsel or a foot
shock. While Pavlov (1927) argued that conditioning results
from a temporal coincidence between CS and US, subsequent
scholarship indicates that the CS must carry information (i.e.,
reduce uncertainty) about the timing and likelihood of US
delivery (Gallistel, 2003; Rescorla, 1988).
Thus, Pavlovian learning allows animals to develop expectancies about motivationally relevant outcomes, and then to
determine the appropriate preparatory response. This review
focuses on the acquisition of Pavlovian associations and the
amygdala circuitry that underpins conditioning. Interestingly,
the neural substrates of Pavlovian learning vary by the motivational valence of the US (appetitive or aversive). The acquisition of aversive associations relies on the serial progression
of information through the amygdala, while evidence from

appetitive studies seems to support a parallel-processing model.

The following sections characterize the behavioral function of
freezing, a common readout of aversive Pavlovian learning, and
then contrast the neural circuitry of aversive and appetitive conditioning.

Pavlovian Processes and Innate Defensive

Behavior
The LeDoux lab has long studied a model of auditory Pavlovian
threat conditioning (for review, see Johansen, Cain, Ostroff, &
LeDoux, 2011), in which a tone CS predicts a foot shock US
and thus elicits robust freezing (immobility and the adoption of
a hunched posture). It is important to note that freezing is an
innate behavior (Blanchard & Blanchard, 1969; Blanchard,
Blanchard, & Griebel, 2005); Pavlovian processes teach the animal when to deploy this response, but not its value as a defensive measure. Freezing is thought to be a component of the
rodents unlearned repertoire of defenses against predation.
Contact with a predator will elicit strong freezing from rats
(Blanchard, Blanchard, Rodgers, & Weiss, 1990), as will the
mere presentation of a novel predator odor (Endres & Fendt,
2009; Wallace & Rosen, 2000). In a natural setting, freezing
occurs in the interval prior to a predatory attack, when the prey
animal has noticed a predator, but has gone unnoticed by its

Corresponding author: Justin M. Moscarello, Center for Neural Science, New York University, 4 Washington Place, Room 809, New York, NY 10003, USA.
Email: jmoscarello@gmail.com

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Moscarello & LeDoux Pavlovian Processes and the Amygdala 249

potential attacker (Elliam, 2005; Fanselow & Lester, 1988).

Freezing makes the animal less conspicuous and more likely
to avoid detection, and is replaced by fleeing if and when the
predator strikes (Elliam, 2005).
Freezing and other species-typical defensive reactions are
considered a default response to a wide array of aversive stimulation (Bolles, 1970; Fanselow & Lester, 1988), which is why
they can be elicited by artificial stimuli in a laboratory setting.
Indeed, it seems that presentation of an aversive CS activates
the behavior that occurs prior to an imminent predatory strike:
immobility or freezing. The increase in muscle tension also prepares the rat to flee when the predicted US is presented, much as
animals flee when predatory attack actually occurs. It has been
proposed that Pavlovian learning allows rodents to instate oncoming threats in a predatory imminence continuum (Fanselow &
Lester, 1988). Thus, rapidly acquired associations provide information about the proximity of an aversive event or outcome,
allowing the animal to deploy the appropriate innate defensive
strategy, such as CS-evoked freezing in the interval prior to US
delivery (Bolles, 1970; Fanselow & Lester, 1988).
This complex and vital form of processing is underpinned by
an elaborate neural architecture in the amygdala. The next section describes how a constellation of amygdalar nuclei acquire
aversive Pavlovian information, and how these associations
are used to coordinate important defensive reactions, such as
conditioned freezing.

Aversive Conditioning and the Amygdala

The lateral and central nuclei of the amygdala (Figure 1) play a
crucial role in the acquisition phase of Pavlovian threat conditioning. The lateral nucleus (LA) contains multimodal neurons that
respond to auditory and somatosensory stimulation (Romanski,
Clugnet, Bordi, & LeDoux, 1993), and are thus well situated to
acquire an association between an auditory CS and a foot shock
US. Aversive Pavlovian learning has strong correlates in LA
activity, and conditioned freezing to an auditory CS develops in
parallel with conditioned increases in LA cell firing (Repa etal.,
2001). Threat conditioning also causes spiking in LA neurons to

Figure 1. Anatomy of the amygdala; arrows represent connections

between and within amygdalar nuclei. BA, basal nucleus; CeA, central
nucleus, with lateral (L) and medial (M) subnuclei; ICM, intercalated cell
masses; LA lateral nucleus.

synchronize within a specific frequency range (Pare & Collins,

2000; Quirk, Repa, & LeDoux, 1995), suggesting that the predictive valence of the CS is encoded by both the rate and rhythm
of action potentials in LA (Maren & Quirk, 2004). Extinction
training attenuates CS-evoked behavior and returns LA activity
to baseline levels, with the exception of a subpopulation in ventral LA that continues to show conditioned responses to the CS
(Repa etal., 2001). These cells are thought to carry an indelible
element of the memory trace that allows for the rapid return of
conditioned reactions after extinction.
LA projects to a variety of amygdalar nuclei, and the central
nucleus (CeA) receives a good deal of nonreciprocal, convergent
input from within the amygdala (Pitkanen, 2000), suggesting that
conditioned information originates in LA and flows forward to
CeA. In support of this model, pharmacological inactivation of
CeA does not prevent LA neurons from developing conditioned
responses, indicating that LA does not require CeA to form aversive CSUS associations (Goosens, Hobin, & Maren, 2003).
Complementary studies demonstrate that inactivation of LA
(Wilensky, Schafe, Kristense, & LeDoux, 2006), selective lesions
of LA (Goosens & Maren, 2001; Nader, Majidishad, Amorapanth,
& LeDoux, 2001), or lesions of the entire basolateral complex
(BLA; Maren, 1999) block the normal formation of an aversive
association with a CS. It is important to note that pretraining lesions
of the basal nucleus do not impact the initial acquisition of aversive
Pavlovian associations (Anglada-Figueroa & Quirk, 2005; Nader
etal., 2001), even though posttraining lesions and inactivations of
the basal nucleus do have a selective effect on the expression of
previously acquired associations (Amano, Duvarci, Popa, & Pare,
2011; Anglada-Figueroa & Quirk, 2005). As such, it seems acquisition deficits caused by BLA lesions depend critically on damage to
LA. In a direct test of the functional anatomy, asymmetric lesion
experiments demonstrate that threat conditioning does not proceed
if the connection between BLA and CeA is severed (Jimenez &
Maren, 2009). Thus, aversive Pavlovian learning relies on a serial
form of information processing in the amygdala, with LA playing a
key role in the acquisition of CSUS associations.
In spite of this serial-processing perspective, it is important
to emphasize that CeA also participates in the acquisition phase
of aversive Pavlovian learning (Wilensky etal., 2006), though
LA and CeA make dissociable contributions to this process.
Like LA, CeA neurons develop conditioned responses over the
course of Pavlovian threat conditioning, displaying a varied
profile of unit activity (Duvarci, Popa, & Pare, 2011). The lateral subnucleus of CeA contains distinct populations described
as CS-on and CS-off cells (Ciocchi etal., 2010). Excitations
among CS-on cells are thought to inhibit the CS-off population,
which causes the disinhibition of the brainstem-projecting neurons in medial CeA that are critical for CS-evoked freezing
(Ciocchi etal., 2010; Duvarci etal., 2011). Thus, freezing to the
CS is driven by a complex disinhibitory process in CeA.
In contrast, CeA also mediates CS-evoked exploration and
risk assessment, which occur at an earlier phase of the predatory
imminence continuum, when a predicted threat is quite distal
(Fanselow & Lester, 1988). Projection cells in lateral CeA mediate this behavior by disinhibiting basal forebrain cholinergic

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250 Emotion Review Vol. 5 No. 3

neurons (Gozzi etal., 2010). This lateral CeA population also

inhibits medial CeA (Gozzi etal., 2010), and may conform to
the CS-off cells that are inactivated under conditions that promote freezing. Exploration and immobility, then, may be driven
by opposite patterns of CeA activity, suggesting that the exact
nature of the reaction to the CS is determined by the function of
CeA microcircuits.
Together, these data suggest that LA represents the relationship between a CS and an aversive US, while CeA evaluates
conditioned information and determines the appropriate behavioral response to imminent danger. A reasonable proposal, then,
is that LA acquires and stores memory for the predictive valence
of the CS, while CeA acquires and stores memory linking a CS
to its appropriate profile of defensive reactions. This putative
arrangement preserves the elements of the serial-processing
model, insofar as it requires the flow of information from LA,
while ascribing both LA and CeA with active roles in the
process of aversive Pavlovian learning.
Killcross, Robbins, and Everitt (1997) provide a compelling
counterpoint to this serial-processing perspective. Using a complex instrumental procedure, they demonstrate a double dissociation between BLA lesions, which prevent animals from avoiding
a lever punished intermittently with aversive CSUS pairings,
and CeA lesions, which prevent the conditioned suppression of
lever-press during the presentation of an aversive CS. From this
the authors conclude that BLA and CeA function independently,
thus de-emphasizing the serial flow of information through the
amygdala. This divergent result may stem from the training protocol employed, which involved an average of 120 CSUS pairingsfar more trials than any other aforementioned report.
Studies of overtraining in rats with BLA lesions have yielded
mixed results. One report demonstrates that animals with BLA
lesions can acquire an aversive association with a context, but
not an auditory CS, after 75 CSUS pairings (Maren, 1999).
However, a study using a comparable training protocol demonstrates that animals with BLA lesions can acquire an association
with both a CS and a context, but only after more pairings than
intact animals require (Zimmerman, Rabinak, McLachlan, &
Maren, 2007). Intriguingly, animals with BLA lesions not only
acquired contextual associations more slowly, but also forgot
them more quickly (Poulos etal., 2009).
It is possible that multiple systems can encode aversive
Pavlovian information, and that the circuitry of serial processing simply happens to be the most efficient at producing a durable memory (Fanselow, 2010). This is a key point, because the
expectancies developed by these systems are designed to counter mortal threat in the wild, and slow, incremental learning and
short-lived memory fail to provide the same adaptive advantage. As such, the literature on overtraining highlights how the
expedient acquisition of lasting aversive associations requires
the serial flow of information from LA.

Appetitive Conditioning and the Amygdala

While the data support a serial-progression model in the case
of aversion, appetitive Pavlovian processes seem to rely on a

qualitatively different form of information processing in the

amygdala (Figure 2). The literature on appetitive conditioning suggests that BLA and CeA function in parallel, independently encoding their own distinct representations of a given
CSUS association (Balleine & Killcross, 2006; Everitt,
Cardinal, Parkinson, & Robbins, 2003). BLA is thought to
process associations between a CS and the specific elements
of an appetitive US, as evidenced by BLA manipulations that
block US devaluation (Hatfield, Han, Conley, Gallagher,
& Holland, 1996), or hinder US-specific Pavlovian-toinstrumental transfer (Blundell, Hall, & Killcross, 2001;
Corbit & Balleine, 2005). In contrast, CeA is thought to process associations between a CS and generalized behavioral
reactions that occur regardless of the specific US, as evidenced by CeA manipulations that attenuate the conditioned
orienting response (Gallagher, Graham, & Holland, 1990), or
block general forms of Pavlovian-to-instrumental transfer
(Corbit & Balleine, 2005).
The appetitive conditioning phenomena that support a
parallel-processing model are generally measured at an expression time point, after the association has already been learned.
Interestingly, the amygdala plays an unknown role in the initial
acquisition of appetitive Pavlovian associations. One study
found that CeA lesions attenuate the acquisition of conditioned
approach (Parkinson, Robbins, & Everitt, 2000), though several
others demonstrate that comparable lesions have no effect on
approach learning (Corbit & Balleine, 2005; Gallagher etal.,
1990; Han, McMahan, Holland, & Gallagher, 1997). However,
CeA lesions do block the development of a conditioned orienting response, while sparing approach (El-Amamy & Holland,
2007; Gallagher etal., 1990; Han etal., 1997). Conditioned orienting is thought to reflect event processing (Holland &

Figure 2. Serial versus parallel-processing models of amygdala function.

Left: Serial model, in which CSUS associations are acquired and stored in
LA, and then processed through CeA to produce defensive reactions. Right:
Parallel model, in which BLA stores the association between the CS and
the specific properties of the US, and the CeA encodes the relationship
between the CS and general conditioned reactions, such as orienting.

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Moscarello & LeDoux Pavlovian Processes and the Amygdala 251

Gallagher, 1999) or attention paid to the CS when an error in US

prediction occurs in a previous trial (Pearce & Hall, 1980).
Commensurate with this, CeA neurons show firing increases
when a US is smaller than anticipated, and this activity precedes
a potentiated orienting response to subsequent CS presentations
(Calu, Roesch, Haney, Holland, & Schoenbaum, 2010). Thus,
CeA contributes to CS associability with a mechanism described
in learning theory, potentially allowing new information to
update previously acquired appetitive associations. However,
Pearce-Hall requires a past trial in order for learning to occur
(Pearce & Hall, 1980), making it unlikely that this mechanism
drives the initial process of acquisition.
Like CeA, lesions of BLA have no effect on the acquisition
of conditioned approach behavior (Corbit & Balleine, 2005;
Hatfield etal., 1996; Parkinson etal., 2000). In contrast, BLA
lesions do prevent appetitive second-order conditioning, in
which a previously acquired CS is used to reinforce a novel CS
(Hatfield etal., 1996; Setlow, Gallagher, & Holland, 2002).
While these lesion data suggest that BLA is selectively involved
in higher order appetitive learning processes, a divergent result
comes from a recent optogenetic study. Using a light-activated
ion channel to rapidly inhibit neuronal activity, Stuber etal.
(2011) showed that the BLA projection to the nucleus accumbens is required during CS presentation in order for subjects to
acquire a conditioned licking behavior. These disparate results
may be attributable to functional accommodation that occurs
after tissue damage, but not fast-acting optical stimulation, suggesting that other structures can take over for BLA in the case of
lesion. Together, the data suggest that BLA might participate
in first-order appetitive Pavlovian learning, but can also be
accommodated for if destroyed.
At first glance, these data seem to align with the literature on
aversive Pavlovian learning, in which BLA is required for firstand second-order conditioning (Maren, 1999; Parkes & Westbrook,
2010). However, excitotoxic BLA lesions strongly hamper the animals ability to acquire an aversive association with a CS, while
first-order appetitive associations proceed unimpeded by permanent damage to that structure. Key encoding differences
must exist if the brain can easily accommodate the destruction
of BLA in one circumstance and not the other.
One possibility is that the two forms of Pavlovian learning
recruit a different pattern of nuclei within BLA. Threat conditioning depends on LA, and in particular on its dorsal subregion,
which contains cells that acquire fast conditioned responses to an
aversive CS (Repa etal., 2001). LA-dependent, aversive Pavlovian
conditioning occurs quickly, usually in 15 CSUS pairing
(Johansen etal., 2011), and is strongly attenuated with damage to
the LA or BLA. Conversely, the appetitive Pavlovian processes
described in the articles cited here occur more slowly, and proceed
unimpeded by permanent BLA damage. Thus, it seems that appetitive Pavlovian learning lacks key features of dorsal LA-dependent
conditioning, suggesting that the differential recruitment of this
region may explain the information-processing differences
observed between appetitive and aversive domains.
This begs the question of why dorsal LA is selectively
recruited in the aversive circumstance. It is possible that the

difference is due to a motivational asymmetry between the

aversive and appetitive stimuli employed in laboratory studies
of animal behavior. Food and sucrose solutions used to reinforce appetitive CSs have considerable motivational pull, and
gain further value when animals are food restricted to the moderate degree permitted in the lab. However, aversive Pavlovian
learning taps into a system designed to counter the existential
threat associated with predation (Bolles, 1970; Fanselow &
Lester, 1988), and thus engages a profile of behaviors that
function to prevent potentially lethal outcomes in the wild.
While truly life-threatening forms of hunger and thirst may
take motivational priority over cues that signal an imminent
threat, it has long been established that aversive CSs can powerfully suppress appetitive behavior, even when animals have
been food restricted (Estes & Skinner, 1941). This suggests that
common aversive stimuli have a motivational edge over the
appetitive stimuli used in neuroscientific experiments of
behavioral learning.
Thus, dorsal LA circuitry may function as a rapid acquisition
system, which is recruited in circumstances of heightened motivational salience that demand a fast behavioral response. The
trade-off for quick learning and durable memory seems to be
dependence on LA and an inability to accommodate its loss.
Conversely, Pavlovian learning that does not recruit dorsal LA
seems to trigger multiple amygdalar representations of the CS
US relationship, distributed across CeA and more ventral regions
of BLA. Dorsal LA-independent learning seems more amenable
to accommodation after permanent damage to a given structure,
as the loss of one circuit can be accounted for by another that
functions in parallel. This kind of learning seems to occur more
slowly, but is also relatively resilient to amygdala damage.

Conclusions
Pavlovian learning allows organisms to determine the predictive
relationship between environmental stimuli and motivationally
relevant outcomes. The contribution of amygdalar circuits to this
process may be determined by the motivational salience of the
stimuli being conditioned. In particular, Pavlovian learning that
occurs in highly motivating scenarios may recruit dorsal LA,
which rapidly encodes the CSUS relationship and coordinates
with CeA to guide conditioned reactions. In this circumstance,
fast behavioral learning relies on the serial progression of conditioned information through the amygdala. In contrast, learning
that does not recruit dorsal LA may yield multiple representations of CSUS associations that are distributed across parallel
amygdalar circuits. While dorsal LA-independent conditioning
generally occurs more slowly, a more diffuse representation of
Pavlovian information allows for a more ready accommodation
of function after damage to the amygdala.

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