Coming to terms with fear

Author(s): Joseph E. LeDoux

Source: Proceedings of the National Academy of Sciences of the United States of
America , February 25, 2014, Vol. 111, No. 8 (February 25, 2014), pp. 2871-2878
Published by: National Academy of Sciences

Stable URL: https://www.jstor.org/stable/23770849

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 Corningtototerms
Coming terms with
with fear
fear
Joseph
Joseph E.
E.LeDoux1
LeDoux1
Center for
Center forNeural
NeuralScience
Science and
and Department
Department of Psychology,
of Psychology, New New
YorkYork University,
University, New NY
New York, York, NY Department
10003; 10003; Department of Psychiatry
of Psychiatry and Department
and Department of Child and
of Child and
AdolescentPsychiatry,
Adolescent Psychiatry,NYUNYU Langone
Langone Medical
Medical Center,
Center, NewNew York,
York, NY 10016;
NY 10016; andNathan
and The The Nathan Kline Institute
Kline Institute for Psychiatric
for Psychiatric Research,Research, Orangeburg,
Orangeburg, NY 10962 NY 10962

This contributionisispart
This contribution partofof the
the special
special series
series of Inaugural
of Inaugural Articles
Articles by members
by members of theof the National
National Academy
Academy of Sciences
of Sciences elected inelected
2013. in 2013.

Contributed
Contributedby
byJoseph
JosephE. E.
LeDoux,
LeDoux,
January
January
9, 2014
9, 2014
(sent(sent
for review
for review
November
November
29, 2013)
29, 2013)

The brain mechanisms of fear have been studied extensively usingPavlovian Pavlovian Feat Conditioning:AATechnique
Fear Conditioning: Techniqueandand a Process
a Process
Pavlovian fear
Pavlovian fear conditioning,
conditioning,a aprocedure
procedurethat
that allows
allows exploration
exploration Fear is the
Fear most
is the extensively
most studied
extensively emotion,
studied and the
emotion, and way it hasit has
the way
of how
of how the
the brain
brain learns
learns about
about and
andlater
laterdetects
detectsand
andresponds
respondstotomost
most often
often
been
been
investigated
investigated
is through
is through
Pavlovian
Pavlovian
fear condi
fear condi
threats. However,
threats. However,mechanisms
mechanisms that
that detect
detect andand respond
respond to threats
to threats tioning.
tioning.
ThisThis
procedure
procedure
involves
involves
presenting
presenting
a biologically
a biologically
neutral neutral
are not
are not the
the same
same as
as those
thosethat
thatgive
giverise
risetotoconscious
consciousfear.
fear. This
This is is
anan conditioned
conditioned stimulus
stimulus(CS), often
(CS), a tone,
often withwith
a tone, a noxious or harmful
a noxious or harmful
important distinction
important distinction because
because symptoms
symptomsbased basedononconscious
consciousand andunconditioned
unconditioned stimulus
stimulus (US), typically
(US), a mild
typically electric
a mild shock.
electric As As
shock.
nonconsciousprocesses
nonconscious processesmaymay bebe vulnerable
vulnerable to different
to different predispos
predispos- a result, the the
a result, CS comes to elicit
CS comes species-typical
to elicit (presumably
species-typical innate)innate)
(presumably
ing
ing factors
factors and
and may
may also
also be
be treatable
treatable with
with different
different approaches
approaches in inbehavioral
behavioral responses (e.g.,freezing
responses (e.g., freezingbehavior)
behavior)andand supporting
supporting
people who
people who suffer
suffer from
from uncontrolled
uncontrolledfearfearor oranxiety.
anxiety.AAconception
conceptionphysiological
physiological adjustments
adjustments controlled
controlled byautonomic
by the the autonomic
nervous nervous
of so-called
of so-called fear
fear conditioning
conditioning in in terms
termsof ofcircuits
circuitsthat
thatoperate
operatesystemsystem (e.g., changes
(e.g., changesin heart
in heart rate,rate,
blood pressure,
blood respiration)
pressure, respiration)
nonconsciously, but
nonconsciously, but that
that indirectly
indirectly contribute
contributeto toconscious
consciousfear,
fear,isisQr orby
byendocrine
endocrine systems
systems (e.g.,
(e.g.,
adrenocorticotropic
adrenocorticotropichormone,
hormone,
cor Cor
proposed
proposed as way forward.
as way forward. tisol, epinephrine) (7-12). Through (7-12).
tisol, epinephrine) fear Through
conditioning, researchers
fear conditioning, researchers
thus
thus have
have control
controlof
ofthe
theantecedent
antecedent
conditions
conditions
(the(the
independent
independent
Pavlovian
Pavlovian conditioning
conditioning | emotion | |survival
emotion | survival
circuits | circuits | variables,
variables, namely
namely the the CS US)
CS and andand
US)
canand can measure
measure the outcomes
the outcomes
global
global organismic
organismic states
states | consciousness | consciousness (dependent variables,
(dependent suchasas
variables, such freezing
freezing behavior
behavior or autonomic
or autonomic
nervous
nervous system
systemresponses).
responses).
Hunger,like,
Hunger, like, anger,
anger, fear,fear, and
and so so forth,
forth, is a phenomenon
is a phenomenon that can bethat Thecanfear-conditioning procedure procedure
be The fear-conditioning works because
works it because
taps intoit taps into
known
knownonly
onlybybyintrospection. When
introspection. applied
When to another..
applied it isa process
.species, .species,
to another.. it is acalled associative
process learning that
called associative is a feature
learning that is of circuits of
a feature in circuits in
merely
merelya aguess about
guess the possible
about nature nature
the possible of the animal's
of the subjective
animal's state. the nervous
subjective systems
state. the of systems
nervous many ifofnot all animals
many (4,animals
if not all 13-16) (4,
and13-16) and
may
may also
also exist
existin
insingle-cell
single-cellorganisms
organisms
(17,18).
(17,18).
When
When
associative
associative
NicoTinbergen
Nico Tinbergen(1) (1)learning
learning occurs
occurs in in
thethe circuit
circuit engaged
engaged by fear
by the the fear conditioning
conditioning
procedure,
procedure, the
thelearning
learningprocess
processitself
itself
is also
is also
called
called
fear
fear
condi
condi
Neuroscientists
Neuroscientists useuse "fear"
"fear" to explain
to explain the empirical
the empirical betweentioning.
relationrelation betweenThe fear-conditioning
tioning. process allows
The fear-conditioning the US
process to alter
allows thetheUS to alter the
two events:
two events;for
for example,
example, ratsrats
freezefreeze
whenwhen they
they see see apreviously
a light effectiveness
light previously of the CS of
effectiveness in activating circuits that
the CS in activating control
circuits defense
that control defense
associatedwith
associated with electric
electric shock.
shock. Psychiatrists,
Psychiatrists, psychologists,
psychologists, responses
and
and most in anticipation
most responses of harm.of harm.
in anticipation
experi Fear conditioning has many attractive
has many features as afeatures
laboratory I/) w
citizens,ononthe
citizens, the other
other hand,
hand, use.. use.. ."fear"
."fear" to nameto aname a conscious
conscious experi- Fear conditioning attractive as a£ laboratory
u
enceof
ence ofthose
those
whowho dislike
dislike driving
driving overbridges
over high high bridges tool. It is rapidly
or encountering
or encountering acquiredacquired
F is rapidly (19), and (19),
is long-lasting, often persisting
and is long-lasting, often persisting
largespiders.
large spiders. These
These two two uses suggest..
uses suggest.. .several .several fear
fear states, states,
each throughout
each
with its life (20). Also,
with its throughout life it canAlso,
(20). be used across
it can a wide
be used range
across of range of
a wide
owngenetics,
own genetics, incentives,
incentives, physiological
physiological patterns,
patterns, profiles. animals,
and behavioral
and behavioral including
profiles. animals,vertebrates and invertebrates
including vertebrates (4, 13, 14, 16),
and invertebrates (4, 13, 14, 16),
allowing
allowing explorations
explorationsofofthe
theextent
extentto to
which
which
similar
similar
mechanisms
mechanisms
JeromeKagan
Jerome underlie the conditioning process in diverse organisms (21).
Kagan(2)(2) underlie the conditioning process in diverse organisms (21).

Fear Conditioning During the Age of Behaviorism

My research
My research
to threats,focuses
focuses
to threats, andI Ion
and on
how
have
have how
the
long the
argued
long brain
brainthat
argued detects
detects and
these
that and responds
responds
mechanisms
these mechanisms FearFear Conditioning
conditioning
Fear conditioning is oftenissaid During
often
to the
said to
endow Age
endow
the CS ofthe
the
with Behaviorism
CSability
with the ability
are distinct
are distinctfrom
from those
those that
that make
make possible
possible the conscious
the conscious to elicittofear.
feeling
feeling It fear.
elicit is, after all,after
It is, calledall,
fear conditioning.
called However, However,
fear conditioning.
of fear
fear that
thatcan
canoccur
occurwhen
whenone
oneis is
in in
danger
danger(3-6).
(3-6).
However,
However,
I, I,
and
and others,
others, have
havecalled
calledthe
thebrain
brainsystem
system
that
that
detects
detects Significance
Significance
andand
responds
responds to
tothreats
threatsthe
thefear
fear
system.
system.This
Thiswaswas
a mistake
a mistakethatthat
has has
led
led to
to much
muchconfusion.
confusion.MostMostpeople
people
whowhoareare
notnot
in the
in the
field Research on Pavlovian fear conditioning has been very suc
field
naturally
naturally assume
assumethat
thatthe
thejob
job
ofof
a fear
a fearsystem
system is to
is make
to make cessful in revealing what has come to be called the brain's fear
con con
scious
scious feelings
feelingsof offear,
fear,because
because thethecommon
common meaning
meaning of fear is system.
of fear is The field has now matured to the point where a sharper
conceptualization of what is being studied could be very useful
the
the feeling
feeling of ofbeing
beingafraid.
afraid.Although
Although research
research on on
thethe
brainbrain
as we go forward. Terms like "fear conditioning" and "fear
mechanisms
mechanismsthat thatdetect
detectandandrespond
respond to to
threats
threats in animals
in animalshas has
system" blur the distinction between processes that give rise to
important
important implications
implicationsfor forunderstanding
understanding howhowthethehuman
humanbrain
brain
conscious feelings of fear and nonconscious processes that
feels
feels fear,
fear, ititisisnot
notbecause
becausethethethreat
threat detection
detection andand
defense
defensecontrol defense responses elicited by threats. These processes
responses
responses mechanisms
mechanismsare arefear
fearmechanisms.
mechanisms. It is
It instead
is instead
because
because
interact but are not the same. Using terms that respect the dis
these
these nonconscious
nonconsciousmechanisms
mechanisms initiate
initiateresponses
responses in the
in the
brain
brain
tinction will help focus future animal research on brain circuits
and
and body
body that
thatindirectly
indirectlycontribute
contribute to to
conscious
consciousfear.fear. that detect and respond to threats, and should also help clarify
In this
this article,
article,I Ifocus
focuson onPavlovian
Pavlovian fear
fearconditioning,
conditioning, a pro
a pro
the implications of this work for understanding how normal and
cedure
cedure that
thathas hasbeen
beenused
usedextensively
extensively to to
study
studythetheso-called
so-called
fearfear
pathological feelings of fear come about in the human brain.
system.
system. II will
willpropose
proposeandanddefend
defenda different
a differentwayway
of talking
of talking aboutabout
research, one
this research, one that
thatfocuses
focusesononthe
theactual
actualsubject
subjectmatter
matter andandAuthor contributions:
Author J.E.L. wrote
contributions: j.e.l.the paper. the paper,
wrote
The author declares no conflict of interest.
(threat detection
data (threat detection and
and defense
defenseresponses)
responses)and
andthat
thatisisless
lesslikely
likelyThe author declares no conflict of interest,
compel the
to compel the interpretation
interpretationthat
thatconscious
conscious states
states Ofof fear
fear underlie
underlie Freely available
Freely available online through
online throughthe PNAS open access
the PNAS openoption.
access option,
defense
defense responses
responses elicited
elicitedby
byconditioned
conditionedthreats.
threats.ItItwill
willnot
notbebeQnAs
See seeonQnAs on page 2860.
page 2860.

easy to give up
up the
the term
term fear
fear conditioning,
conditioning, but
but I Ithink
thinkwe
weshould.
should. 'e -mail:
1 E-mail: ledoux@cns.nyu.edu.
ledoux@cns.nyu.edu.

www.pnas.org/cgi/doi/10.1073/pnas.1400335111
www.pnas.org/cgi/doi/10.1073/pnas.1400335111 PNAS
PNAS || February
February 25, 2014 || vol.111
25,2014 vol.111 || no. 8 | 2871-2878

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what different researchers have meant by fear has been a moving psychological or physiological entities (states or processes) that
target since the procedure was first used. intervene between stimuli and responses (58). However, drive
The story begins with John Watson, the father of behaviorism and fear theories led to much discussion about the relative merits
(22). As is well known, the behaviorists banished consciousness of pure intervening variables vs. intervening variables that implied
from psychology, focusing instead on observable events. How hypothetical entities to explain behavior (58-60). Tolman later ac
ever, they did not eliminate mental state terms—fear was still knowledged that at times he was actually referring to hypothetical
studied but was viewed as something other than a feeling. constructs (59). Although hypothetical constructs are generally
Watson, following Ivan Pavlov (23), viewed fear as a condi viewed as acceptable when empirically grounded in observable
tionable reflex (22) and used Pavlov's defensive conditioning events, they cause problems when reified and given a status that is
procedure to condition the fear reflex in a young boy (24). B. F. not empirically verifiable (e.g., when the construct is named with
Skinner, another behaviorist, adopted a different approach, in a common language term that implies a psychological state, and the
strumental (operant) conditioning, in which behavior is learned construct then takes on assumed attributes of the state in theory and
by its consequences (25). Fear became a behavioral disposition data explanation) (58-60). Fear as a nonsubjective physiological
determined by a history of aversive reinforcement. state that intervenes between stimuli and responses is a potentially
Watson and Skinner were opposed to assumptions about un verifiable construct (35). However, when fear takes on its received
observable events inside the head. However, Edward Tolman meaning as a conscious feeling, and researchers start looking for
found a way to call upon inner factors and still be a behaviorist properties associated with human fearful feelings in animals, the
(26). The inner factors were psychological but not conscious; more problematic kind of hypothetical construct exists.
they were "intervening variables" defined by the empirical re The expression "state of fear," practically begs the reader to
lation between observable independent and dependent variables. think of rats feeling afraid of the CS and to think that this feeling
Fear, for example, was an intervening variable that accounted for is the cause of defensive behavior. However, because the research
the expression of defensive behaviors in the presence of a threat. discussed above was done by researchers who were working in the
Importantly, intervening variables were not entities (states or behaviorist tradition, it seems likely that they were thinking along
processes) but instead descriptions of the relation between observ the lines of empirically verifiable constructs and not in terms of
able factors. Tolman emphasized that this approach could be used unverifiable feelings in their animal subjects. In fact, a variety of
to study introspecting and nonintrospecting organisms alike (27).
empirically based interpretations of fear were proposed (9, 35
While behaviorism was flourishing, so was Sigmund Freud's 44). On the other hand, Mowrer, a leading figure in this field,
psychoanalytic theory, which emphasized drives as inner forces
explicitly endowed the central state of fear with subjective prop
of motivation (28). Clark Hull (29) integrated Freud's drive erties that were said to cause behavior. For example, Mowrer wrote
theory with Tolman's intervening-variable approach, arguing that
that "consciously experienced fear.. .must invariably be present, in
reinforcement of behavior during learning results from reduction
some degree, as the cause of the observed behavior" (30), and "we
in a physiological drive state. For example, food deprivation
do not have to say that the rat runs 'in order to' avoid the shock; we
increases drive, and behaviors that lead to food are reinforced by
can say instead that the rat runs because (or by-cause) of fear" (31 ).
the reduction in drive that follows eating of the food. Intervening
However, even authors who seemingly adhered to empirically
variables were, for the most part, abstract psychological con
based approaches wrote about fear in a way that could easily be
structs for Tolman but were physiological states for Hull.
interpreted to mean a subjective feeling. For example, Bolles men
Two of Hull's protégés, O. Hobart Mowrer and Neal Miller, de
tions the "frightened rat" (39), McAllister and McAllister say the
veloped the view that fear is a learned drive state that comes to be
CS is "an elicitor of fear" (38), and Kamin and colleagues describe
elicited by the CS after Pavlovian conditioning with a shock US (30
rats as being "very fearful of the CS." Adding to the ambiguity is the
33). They used an instrumental task called avoidance conditioning in
fact that in a given paper the word fear would sometimes be in
which rats learn to perform responses that reduce shock exposure.
Skinner said that avoidance conditioning was reinforced by escape quotes and sometimes not, implying that two kinds of fear were
from the shock, but Mowrer and Miller proposed that avoidance is being discussed, but without explaining the different uses (37).
reinforced by reduction in a CS-elicited fear drive. Early in training,
To try to gain some clarity on the nature of what fear really
stimuli in the chamber become CSs that are associated with the US. meant in this literature, I contacted several of the behavioral
Exposure to the CSs then elicits a fear state that motivates per researchers who played an active role in this work and asked
formance of behaviors that eliminates CS exposure, thus reducing whether they were thinking of fear as a conscious feeling, along
the state. (A related two-process theory was proposed by Konorski the lines of Mowrer, or as an intervening variable that did not
and Miller; see ref. 34.) imply subjective states. Robert Rescorla, Bruce Overmier, Donald
Over the subsequent decades, much research was done to Levis, and Michael Fanselow responded, each noting that they did
evaluate the role of fear in avoidance (35-44). Drives came to be not view fear as conscious feeling but instead as an empirically
called central (i.e., brain) motive states (34, 45, 46). Because so defined term based on observable events. (These comments were
little was known about the brain, Donald Hebb referred to obtained through e-mail correspondence. Respondents agreed to
central states as existing in a conceptual nervous system ratherbe quoted.) For example, Rescorla noted: "I do not think that
than the central nervous system (47). However, drive proved reference to subjective experiences (by which I mean private
problematic as an all-purpose explanation of motivation becauseexperiences not subject to independent inter-observer verification)
organisms are also impelled to act by external incentives (46, 48, is especially useful." Fanselow said: "I feel that part of our job is to
49, 50). Still, central states survived because incentives were also redefine the concept of motivation in a scientific manner and that
said to activate motivational states that control behavior. Robert those new definitions should replace the layman's informal view. I
Bolles, for example, argued that avoidance does not reflect don't
re see how subjective experience helps us do that."
duction in fear drive, but instead results, because the CS actiWith the constraints of behaviorism loosened, animal con
vates a fear system that generates a fear state, and this limits sciousness is no longer a taboo topic (61-66). Lacking the con
behavioral options to species-specific defense responses (9, ceptual 39). and historical foundations needed to navigate the
The defense response selection rules turn out to be more com ambiguous use of fear and the subtle issues that were being
plex than this (51, 52) but are still said to involve activation grappled
of with by those who treated fear as a nonsubjective in
a fear system by stimuli that predict harm (19, 53) and also,tervening for variable, readers today (including scientists, journalists,
some, a central state of fear that causes defense responses and (38, lay people) are easily drawn toward the conventional
41, 54-57). meaning of fear as a conscious feeling and to the everyday
Originally, intervening variables were conceived of as abstract belief that fearful feelings cause us to respond in a certain way
constructs (a means of connecting observable independent and to threats. Let us look at contemporary brain research to see
dependent variables), with no "surplus meaning" that implied why this view is neither necessary nor desirable.

2872 I www.pnas.org/cgi/doi/10.1073/pnas.1400335111 LeDoux

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Conditioned
Conditioned FearFear as a Circuit
as a Circuit FunctionFunction 99) and without 99) and reporting
withoutany particular
reporting any feeling,
particulareven feeling,when even when
In the
the 1950s,
1950s,avoidance
avoidance conditioning
conditioning became
became the the main task task
main usedinstructed
instructedto
used totrytry to to introspect
introspect about about feelings
feelings (98). (98).
TheThe condi condi
to
to explore
explorebrain brainmechanisms
mechanisms of of fearfear and and aversive aversivelearning learning tioning
tioning process
process cancan alsoalso be carried
be carried out nonconsciously
out nonconsciously (99-101) (99-101)
(67-72). However,
However, this this work
work led led to to inconclusive
inconclusiveresults results(4, (4,68, and
68, 69,69, without
and without awareness
awareness of of the theCS-US
CS-UScontingency
contingency (102). (102).Ac Ac
73).
73). By
By the
the 1980s,
1980s,researchers
researchers interested
interested in in learning
learning in mammals
in mammals quisition
quisition effects
effectsare are sometimes
sometimes weaker weaker(101), (101), but but thisthis is likely
is likely
and
and other
other vertebrates
vertebratesturned turned toto Pavlovian
Pavlovian conditioning
conditioning 75),attributable
(74, (74, attributable to
75), to the
the degraded
degraded input inputrequired
required toto prevent
prevent awareness
awareness
inspired
inspired in inpart
partby bythe the successful
successful useuse of of simple simple conditioning
conditioning than
than to to the limitsof
the limits ofnonconscious
nonconscious processing
processing per per se because
se because
approaches
approachesininstudies studies of ofinvertebrates
invertebrates (14, (14,16, 76, 16,77).76,This complex
77). complex
This cognitive
cognitive andand social
social processes
processes that thatcontrol controlhuman human
be be
strategyworked
strategy workedremarkably
remarkably well, well,
and and Pavlovian
Pavlovian fear condition
fear condition- havior
havior areareoften carried
often out without
carried out without conscious awareness
conscious of their of their
awareness
ing
ing became
became the the"go-to"
"go-to"method method inin mammals
mammals forfor studying
studying occurrence
aver- aver occurrence in daily life life
in daily (103-105).
(103-105). Also,Also, functional
functional imaging imaging
sive
sive learning
learning(4, (4,54,54,78),
78), asas well
well as asforfor studies
studies of theof the relation studies
relation studieshave have shown
shown thatthat thethe amygdala
amygdala is activated
is activated when when condi condi
betweenemotion
between emotion and and memory
memory (4, 79).(4, 79). tioned or unconditioned tioned or unconditioned threatsthreats are presented
are presented with with ororwithout
without
The
The neural
neuralcircuits
circuits andand cellular,
cellular, synaptic,
synaptic, and molecular
and molecular CSCSawareness
awareness(97, (97,98,98,101,
101, 106-112).
106-112). [Under [Under certain certain conditions
conditions
mechanisms
mechanismsunderlying underlying thethe acquisition
acquisition and and expression
expression of con- ofof of attentional
con attentionalload, load,subliminal
subliminal activation
activation of ofthethe amygdala
amygdala is reis re
ditioned
ditioned fear fearresponses
responses havehave been been characterized
characterized in detail
in detail (4, 5,duced
(4, 5,butbut
duced notnot eliminated
eliminated (e.g., ref.ref.
(e.g., 113).]113).]Amygdala,
Amygdala, butbut notnot
53, 80-82).
80-82). (For
(For aadifferent
differentperspective
perspective onon the the circuitry,
circuitry, seesee hippocampal,
refs.refs.hippocampal, activation
activation also also
occursoccurs when when subjects
subjectsare unaware
are unaware
49
49 and
and 83.)
83.)The Thelateral
lateral nucleus
nucleus of the
of the amygdala
amygdala (LA) receives
(LA) receives of
of thethe CS-US
CS-UScontingency
contingency(114). (114).Finally,
Finally, inin people
people withwith blind
blind
sensory
sensory inputs
inputsabout aboutthe the CSCS andand US.US. Before
Before training,
training, the theCS onlyCSness attributable
ness
only attributable to damage
to damage to visual cortex,
to visual visualvisual
cortex, threats elicit elicit
threats
weakly
weakly activates
activatesLA LAneurons.
neurons.After Afterthe the CSCS is ispaired
paired withwith thethebody
US,US, responses
body responses and amygdala
and amygdala activation
activation without awareness
without awareness of of
the
the ability
abilityof ofthetheCSCStoto activate
activate thethe LA LA increases.
increases. When Whenthe CS the
the thestimulus
CS stimulus andand without
without any any obviousobviousfeeling of fear
feeling of (115-118).
fear (115-118).
later
later occurs
occursalone,alone,CSCSactivation
activation of ofthethe LA LA leads to neural
leads to neural ac- If acconditioned
If conditioned fear fear responses
responsesdo donot notrequire
requireconsciousness
consciousness in in
tivity
tivity that
that propagates
propagatesthrough throughamygdala amygdala circuits
circuits to tothethe centralhumans,
central humans, we should
we should not callnot uponcall uponconsciousconscious mental mentalstatesstatesto to
nucleus
nucleus(CeA).(CeA).OutputOutput connections
connections of CeA of CeA thenthen result result
in thein explain
the how
explain how aa CS CS elicits
elicitsfreezing
freezingand andautonomic
autonomicconditionedconditioned
expression
expression of of defensive
defensivebehavior behaviorand and physiological
physiological responses,
responses, responses
as responses
as in animals.
in animals. Behavioral
Behavioral and physiological
and physiological responses responses
well
well changes
changesbrain brainarousal.
arousal.Plasticity
Plasticity also alsooccursoccurs in the
in the central elicited
central elicited by by a CSa tell us about
CS tell us about processes
processes that that detect the CS
detect theand CS and y
nucleus
nucleus of ofthe theamygdala
amygdala (84-86)
(84-86) and and in inCS CS sensorysensory processing
processingcontrol
control thethe responses.
responses. Fear (in (in
Fear the the sense senseof aof conscious
a conscious feeling) feeling) g
areas
areas (87).
(87). At
At thethecellular
cellularand andmolecular
molecular levels,
levels, fear
fear conditioning
conditioning is not in that
is not causalcausal
in that sequence. Conscious
sequence. fear can
Conscious fearoccur
canwhen occurthe when the !«
occurs
occurs whenwhenLA LAneurons
neurons that that process
process the the CS are CS weakly
are weakly acti-conditions
conditions
acti areare favorable,
favorable, butbut such suchconscious
conscious states comecome
states aboutabout g
vated
vated at atthethesamesame time
time that that thethe US US strongly
strongly depolarizes
depolarizes the throughthe different
through different processes
processes that thatinvolve
involve different
different circuits. The The £
circuits.
neurons
neurons(5, (5,53,53,80, 80,81,81,88,88,89).89).This Thisresults
results in aninincrease
an increase in thefunction the ofof
infunction the neural
the neural circuit
circuit that underlies
that underlies fearfear
conditioning
conditioning is is
strength
strength of of the
thesynapses
synapsesthat that process
process the theCS,CS, allowing
allowing it to toto
it more coordinate
more to coordinate brain and body
brain and body resourcesresourcesto increase the chance
to increase of
the chance of
effectively
effectivelyactivateactivateamygdala
amygdala circuits.
circuits. Molecular
Molecular mechanisms
mechanisms surviving
surviving the the encounter
encounter predictedpredicted
by the by CS withthe CS with adverse
minimal minimal OZadverset/i
UJ
0 ^
engaged
engaged resultresult in in gene
gene expression
expressionand andprotein
proteinsynthesis,synthesis,stabi- stabi consequences
consequences (3, 9, 42,(3, 51,9,119),
42, not 51, to 119),
make not to make
conscious conscious
fear. < yfear. < B
lizing
lizing temporary
temporarychanges changesininsynaptic synaptic strength
strength andand creating
creating long- AA
long striking
striking example
example of the
of the problems
problems caused by the
caused by ambiguous
the ambiguous < —
— 1/1

term
term memories.
memories.Many Many ofof the the molecular
molecular findings
findings werewere pursued use
pursued useofof thethe termterm fear
fear comes
comes from from a recent
a recent study
study showing
showing thatthat
2
2 >>
following leads
following leadsfrom frominvertebrate
invertebratework work (14, (14,77,77, 90).90). a woman a woman withwith bilateral
bilateral amygdala
amygdala damage damagecould could still
still experience
experience o E
O t
Fear
Fear conditioning
conditioning thus
thusbecame
became a process
a process thatthat is carried
is carried
out by out"feelings
"feelings
by of fear" (120). This was surprising to the authors and to 5g
of fear" (120). This was surprising to the authors and to
5 p.
cells,
cells, synapses,
synapses,and andmolecules
molecules inin specific
specific circuits
circuits of ofthethe nervous journalists.
journalists.
nervous Science,
Science, Nature,
Nature, and andother other
esteemed esteemed publications
publications pub pub
system.
system. As Assuch,
such,fear fearconditioning
conditioning is isexplainable
explainable solely in terms
solely lished
in terms lished stories
storieswith dramatic
with dramatic headlines
headlines about the study.
about the study. Flowever,However,
of associations
of associations created
created andand stored stored via cellular,
via cellular, synaptic, synaptic,
and the theand
only
onlyreason
reason this would be
this would besurprising
surprising is isif ifoneone believed
believed thatthatthe the
molecular
molecular plasticity
plasticitymechanisms
mechanisms in inamygdala
amygdala circuits.
circuits. When When the amygdala
amygdala
the is the
is the wellspring
wellspring of fearful
of fearful feelingsfeelings
and thatand amygdala
that amygdala
CS later
CS lateroccurs,
occurs,itit activates
activates thethe association
association and leadsand leadsto thetoex- the ex
controlled
controlled responses
responses are are reliable
reliable markersmarkers of theseof these
feelings feelings
(121). (121).
pressionofofspecies-typical
pression species-typical defensive
defensive responsesresponses that prepare
that prepare the ThatThat the the amygdala
the amygdala is is responsible
responsible for forfearfearis, is,ininfact,
fact,a awidely
widely held
held
organism
organism to to cope
cope withwith thethedanger
dangersignaledsignaledby bythe theCS. CS. There
There isbelief
nono
is (120).(120).
belief However,However, as weashave we have seen,seen, neither amygdala
neither amygdala ac ac
need for
need forconscious
conscious feelings
feelings of offear fear to intervene.
to intervene. The circuit
The circuit tivitynor
tivity noramygdala-controlled
amygdala-controlled responses
responses are are telltale
telltale signatures
signatures
functionisisthe
function the intervening
intervening variable.
variable. Yet, IYet, and Iothers and others
muddied muddied
ofof fearful
fearful feelings.
feelings. As As long
longasaswe weuse usethe the termterm fearfear
to toreferreferto theto the
the waters
waters by by continuing
continuingtotocall callthe the circuits
circuits involved
involved in in detecting neural
detecting mechanisms
neural mechanisms underlying
underlying bothboth consciousconsciousfeelings and non
feelings and non
responding to
and responding to threats
threatsthe thefear fearsystemsystem(4, (4,19,19,54).
54). consciousconscious threat
threatprocessing,
processing, confusionconfusion will will occur.
occur. Conscious
Conscious fear fear
can cause us to to act
act inin certain
certain ways,ways, but but it it isis not
not the
the cause
causeof ofthethe
Nonconscious
Nonconscious Conditioned
Conditioned Fear in Fear Humans in Humans expression of defensive
expression of defensive behaviors
behaviorsand and physiological
physiological responses responses
Embedded
Embeddedininthe the intervening
intervening variable
variable approach approach was the was as-the elicited
as by
elicited by conditioned
conditionedororunconditioned
unconditioned threats.
threats. We should
We should not not
sumption
sumption that thatthe therelevant
relevantfactors factors (the(the observable
observable facts)
facts)in the
inhave have
the called it a it
called fear system.
a fear system,
brain
brain could
couldininprinciple
principle be beaccounted
accounted for in for introspecting
in introspecting and and
nonintrospecting
nonintrospectingorganisms. organisms. And And thethe neuroscience
neuroscience perspective Going
perspective Going Forward
Forward
described
describedabove aboveprovided
provided a biological
a biological account
account thatthat mademade it un- Research
itResearch
un underunder thethe banner
banner of of fear fearconditioning
conditioning hashas been beenex ex
necessarytotocall
necessary calluponupon conscious
conscious fearfear to account
to account for the for thetremely
data. data. productive.
tremely productive.We We areare at at
thethe crossroads
crossroads between
between a fledgling
a fledgling
However,
However, findings
findingsfrom from studies
studies of offear fear conditioning
conditioning in humans andand
in humans maturemature field.field. I propose
I propose that thatthis this transition
transition could could
be greatlybe greatly
made ititunnecessary
made unnecessary to to further
further tiptoe tiptoearound around consciousness,
consciousness, be- be byby
facilitated
facilitated adopting
adopting termsterms thatthat distinguish
distinguish processes
processes that give
that give
cause
cause the
the relation
relationbetweenbetweenconsciousconscious and and nonconscious
nonconscious processing rise rise
processing to conscious
to conscious feelings
feelingsof fear of fearfromfrom processesprocesses
that that operate operate
can be
can be directly
directlyevaluatedevaluated in in ourour species. nonconsciously
species. in detecting
nonconsciously and responding
in detecting and responding to threats.
to threats.
Research on
Research onpatients
patientswith with brain
brain damage
damage revealed
revealed thatthat fearThe fear
Thestorystory ofof fearfear research
research shows shows how how hard hardit is to it keep
is to con keep con
conditioning
conditioningcreates createsimplicit
implicit (nonconscious)
(nonconscious) memories
memories thatthat are
scious scious
are fear fear
out of out theofcausal
the causal
sequence sequence
of behavior. of behavior.
In research, In research,
distinct
distinct fromfrom explicit/declarative
explicit/declarative(conscious) (conscious)memory memory(4, (4,5,
scientists
5,91, 91, scientists
measure measure
responses responses
to threats. to threats.
However,However, some then some then
92).
92). Thus,
Thus,damagedamagetotothe the hippocampus
hippocampus in humans
in humans disrupts
disrupts ex- conclude
conclude ex that conscious
that conscious fear underlies
fear underlies the responses the responses
and thusand thus
plicit conscious
plicit consciousmemory memoryofofhaving having beenbeen conditioned
conditioned butbut has
hasthatno thatno responses
the the responses can signal can signal
the presencethe presence of consciousof conscious
fear in fear in
effect on on fear
fear conditioning
conditioning itself, itself,whereas
whereasdamage damageto tothe theamyg-
people
amyg people and animals.
and animals.
dala disrupts
dala disrupts fear fearconditioning
conditioningbut butnot notthe the conscious
conscious memory
memory of of
We We
havehave conscious
conscious feelings feelings
of fearofwhen fearwe when we actand
act afraid, afraid,
it is and it is
havingbeen
having beenconditioned
conditioned (93,(93, 94). 94). Furthermore,
Furthermore, behavioral behavioral
naturaltotoassume
natural assume thatthat thesethese feelings
feelings are causal
are causal in our inbehavior
our behavior
studies in
studies in healthy
healthyhumans humanshave havefound found that that conditioned
conditioned orand or
un-un inandthein the behavior
behavior of others of (122),
othersincluding
(122), including
animals (61-66).animals (61-66).
conditioned
conditionedthreats threatspresented
presented subliminally
subliminally elicitelicit
physiological
physiological However,
However, much much
researchresearch in psychology
in psychology and neuroscience
and neuroscience shows shows
responseswithout
responses withoutthe the person
person beingbeing aware aware of the of stimulus
the stimulus (95-
thatthat(95
peoplepeople exercise
exercise less conscious
less conscious controlcontrolof their ofbehavior
their behaviorthan than

LeDoux PNAS | February 25, 2014 | vol.

PNAS I111 | 25,
February no.2014 | 8
vol. |1112873
| no. 8 | 2873

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they believe (103-105, 123-125). Careful analyses show that im
plicit processes often underlie (126), and in some cases account for
(127), presumed mental states in animals. Conscious mental states
should not, in the absence of direct evidence, be the first choice
explanation of behavior, even in humans. Also, when the processes
in question are represented similarly in the brains of humans and
animals, and do not require consciousness in humans, we should be
especially cautious in giving conscious states a causal role in these
processes and the responses they control in animals.
The story of fear research also illustrates the perils of using an
everyday term about human subjective experience, like fear, as
a nonsubjective scientific term. When those not "in the know"
about the nonsubjective meaning of fear (whether they are other
scientists, lay people, or journalists) encounter the term "fear,"
they naturally conclude that the research is about fear as a feel
ing. Loose talk by those who believe otherwise promotes mis
understanding. Researchers today can commonly be heard to
say: "we used freezing as a measure of fear" (I have done this
myself.) The burden is on scientists who think of fear in non
subjective terms to be clear about what they mean because the
default, everyday meaning of fear needs no such help. It is not
sufficient to simply say, "science is complicated, so those outside
the field cannot be expected to know what is really going on."
We depend on public funding for science, and the public has
a right to expect that we try to explain what we are doing as
clearly as possible. This is especially important for topics that
have clinical relevance, as is the case for fear conditioning.
It is routine for novelists and poets to assume that their
readers will turn to shared assumptions captured by everyday
language to understand ambiguous statements. Ambiguity is not
only tolerated but can be a virtue in literature and poetry but
should be avoided in science (128). Francis Bacon cautioned
centuries ago against the conceptual dangers of imprecise sci
entific terminology and the potential for reification (128). We
should heed his warning. Otherwise, those not in the loop will
fail to understand that fear does not always mean conscious fear.
I am not suggesting that we banish the "F" word from our scien
tific vocabulary and research. On the contrary, I think that we need
to come to terms with fear because the conscious feeling of fear is
a key part of human experience and an important factor in psycho
pathology. Neither am I suggesting that animal research is irrelevant
to understanding human conscious feelings of fear. Animal research
is essential. However, we need a conception that allows us to un
derstand how nonconscious processes in other species contribute to
conscious fear in humans. (This includes animals that are relatively
close relatives of humans, like mammals, as well as species far from
our evolutionary roots, such as worms, slugs, and flies.)
The required conception is unlikely to be achieved by looking
for human mental states in animals. Why should we expect that
our introspections will lead to an accurate portrayal of the or
ganization and operation of ancient processes in our own brains
or in the brains of other organisms (129). Experiences we label
and talk about as fear are not directly tied to the circuits that
detect and respond to threats (see Nonconscious Conditioned
Fear in Humans), and are not reliably correlated with body
responses elicited by threats (130). Claims by some that animals
must have conscious feelings because of the continuity of be
havior across species (61-66) assume that behavior and con
scious feelings are coupled in the brain. However, if this not the
case, and it does not appear to be, we cannot use information
about defense responses to tell us whether animals are experi
encing fear. Lloyd Morgan long ago warned against "humanizing
the brute," arguing that just because scientists necessarily start
their exploration of animal behavior from their own subjective
experiences does not justify the attribution of similar experiences
to other animals (131). This kind of attribution is desirable, he
says, when we interact socially with other humans but question
able when trying to understand animal behavior. Assumptions
about unobservable subjective states are more complex than the
assumptions about unobservable entities of physics or astronomy
(128, 132).
2874 I www.pnas.org/cgi/doi/10.1073/pnas. 1400335111 LeDoux
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I am not proposing that animals lack conscious feelings. I just do
not think that this is an issue that can be resolved scientifically, as
Tinbergen also implied in the opening quote. We are on safe
ground when we compare observable variables across species
(defense responses elicited by threats). We can also be confident
when we assume unobservable variables (feelings of fear) in other
people, because all people have brains with the same functions and
because we can compare notes with each other verbally. However,
whether other animals feel fear when threatened is another matter.
Different species have different brains, and even when the same
brain areas and circuits are present, these do not necessarily per
form the same exact functions. Also, as we have seen, responses
elicited by threats are not telltale signs of fear, even in humans.
Nevertheless, as I discuss below, we can learn quite a bit that is
relevant to human feelings from studies of animals without
making any assumptions about consciousness. Some will surely
counter that this is too limiting. However, if we do not limit the
discussion, confusion inevitably results. Those who observe our
field lose track of what we are studying and what it means and
are left to draw their own conclusions, which are understandably
based on their everyday understanding of fear. Going forward,
we need clear terms and concepts to advance the field.
Coming to Terms with Fear
There is a really simple solution to these problems. We should
reserve the term fear for its everyday or default meaning (the
meaning that the term fear compels in all of us—the feeling of
being afraid), and we should rename the procedure and brain
process we now call fear conditioning.
So what should fear conditioning be called? There are two
viable options. Pavlov's original term, "defense conditioning," is
one. This expression reflected Pavlov's focus on stimulus sub
stitution—transfer of control of the defensive reflex from the US
to the CS. Whereas the CS does come to control defensive
freezing, this is not the same response elicited by the US—the U
elicits jumping, flight, and other responses (9, 51, 57). Pavlovian
aversive conditioning instead is more appropriately conceived of
as involving a process in which the meaning of the CS has bee
changed (133). For this reason, I prefer the second option, "threa
conditioning." This phase implies that a stimulus that was no
threatening becomes so. One could argue that threat is in the ey
of the beholder and thus defense conditioning is more neutra
However, a threat can be defined objectively as a stimulus tha
elicits defense responses. Thus, although either is better than fear,
threat has advantages over defense as a description of the proces
We can thus say that the association of the CS with the US
changes the meaning of the CS, making it a threat and giving i
the ability to flow although amygdala circuits and elicit defens
responses. The particular response that occurs depends on fa
tors such as perceived proximity to the threat in space and tim
(51, 52). Autonomic and endocrine responses that also occur ar
part of the physiological preparation for responding to the threa
and are part of the "defense response complex."
Much has been written about the language of psychology
where the use of everyday terms based on human introspection
invites each reader to interpret the words in their own way (59
128, 134, 135). Some argue for a new scientific language to r
place everyday folk concepts (128, 135). I have not proposed
anything so radical. I have stuck with everyday terms (threa
defense) that describe observable events (stimuli and responses).
I also keep the everyday term fear because it reflects states tha
we know are part of conscious experience, at least in humans.
The problem is not the terms but the way we use them. Sp
cifically, problems arise when we conflate terms that refer t
conscious experiences with those that refer to the processing o
stimuli and control of responses and assume that the brain
mechanisms that underlie the two kinds of processes are the
same. By making mild changes that capture these distinctions, w
have an easy fix that has the potential for eliminating much of
the terminological confusion in the field. We may someday fin
an abstract
an abstractscientific
scientific language
language for for describing
describing all In
all this. this.
the In the mean-most
mean most central fearstate
central fear state hypotheses
hypotheses (9, 41,
(9, 38, 38,54-57),
41, 54-57),
without without
time,we
time, weshould
shoulduseuse
thethe language
language we more
we have have carefully.
more carefully. pulling the reader
pulling or listener's
the reader mind toward
or listener's the conclusion
mind toward that
the conclusion that
One
One could
couldargue
arguethat
thatweweshould
shouldnotnot
go go
downdownthisthis
roadroad
unless
unless thethe state in question
state involves
in question a subjective
involves feeling
a subjective of fear,
feeling of fear.
we are
we are willing
willingtotododoit it
forfor other
other psychological
psychological processes
processes labeled The The
labeled termterm
"defensive motivational
"defensive circuits"
motivational might might
circuits" be useful
be as
useful as
with mental
with mentalstate
state terms.
terms. I would
I would argue
argue that that
this isthis is indeed
indeed correct.correct. aa description
descriptioncircuits
circuitsthat, in the
that, presence
in the of threat
presence predicting
of threat predicting
There
There arearepractical
practicalimplications
implications of of
getting
getting the the
terminology
terminology cues, cues, control
control defensive
defensive instrumental
instrumental behaviors (goal-directed
behaviors (goal-directed
correct.Pavlovian
correct. Pavlovian conditioning
conditioning research
research is usedis used to understand, actions
to understand, actionssuch such as as
avoidance
avoidance andand other coping
other responses).
coping The deThe de
responses).
and,
and, in
in some
somecases,
cases,guide
guide treatment
treatment of, of,
psychiatric
psychiatric disorders
disorders(130, (130, fensivefensive reaction
reaction and and
action circuits
action likely likely
circuits interact (5, 49, 73).
interact (5, And
49, 73). And
136-140).
136-140). Understanding
Understandinghow how conditioning
conditioning in animals
in animals relates to to both
relates both contribute
contribute to defensive
to defensive organismicorganismic states,states.
conscioussymptoms,
conscious symptoms, as as opposed
opposed to underlying
to underlying processes
processes that in that in- A defensive
A defensive organismic
organismicstate state
is triggered
is triggeredby activity in survival
by activity in survival
directlycontribute
directly contribute to to conscious
conscious symptoms,
symptoms, is important,
is important, because because circuits circuits that thatdetects
detects threats
threats andand generates
generates automaticautomaticdefense defense
explicit and
explicit andimplicit
implicitsymptoms
symptoms may may be susceptible
be susceptible to different reactions
to different reactions (3).(3).
TheThe detection
detection circuits are either
circuits prewired
are either to re
prewired to re
treatments.
treatments.Approaches
Approaches that thatalter the the
alter potencypotencyof threats by maby ma- spond
of threats spondtotospecies-typical
species-typical threats
threatsor are orwired
are wired
via experience
via experience(as (as
nipulation of
nipulation ofthethestorage
storageororretrievalretrieval of ofimplicit
implicit memories
memories are are sociative
sociative learning)
learning) to detect novel novel
to detect stimuli that predict
stimuli sources sources
that predict of of
offering
offeringvariations
variationsof, of,and and alternatives
alternatives to, to,
exposure
exposure therapytherapy(138, (138, harm harm (3,19,146).
(3,19,146). When Whenactivated
activatedby a by threat, a variety
a threat, of responses
a variety of responses
140-144).
140-144). Whereas
Whereasthese theseoperate
operateononnonconscious
nonconscious systems
systems byby results: species-typical
results: species-typical behaviors (e.g. freezing)
behaviors (7-10, 19),
(e.g. freezing) periph
(7-10, 19), periph
directly
directlychanging
changing howhow these
these detect
detectand and
respondrespondto threats, ther ther- eral
to threats, eralphysiological
physiological responses
responses of the of autonomic
the autonomic nervous and endo
nervous and endo
apies
apies based
basedon oninsight
insightoror cognitive-change
cognitive-change work, work,in part, through
in part, through crine crine systems
systems (10-12, 75, 78)
(10-12, 75,that
78) produce
that produce signals signals
that feedback to
that feedback to
systems
systemsthat thatgivegiverise
riseto toconscious
conscious awareness
awareness and thatand that
thathave that have the the brain
brain (32,(32,37, 37,
159),159),
and changes
and changes in brain in activity,
brain activity,including including
limited
limited access
access to toprocesses
processesunderlying
underlyingimplicit implicit memory.
memory. Both Both synaptic synaptictransmission
transmission within and between
within and between circuits, and increases
circuits, in
and increases in
approacheshave
approaches have a place.
a place. Recognizing
Recognizing whatwhat eachin
each does does
the inbrain the brain generalgeneralarousal arousal duedue to widespread
to widespread releaserelease
of aminergicof aminergic
neuro neuro
may
may better
betterfocus
focusefforts
efforts to totreat
treatspecific
specificneeds of the
needs of individual,
the individual, modulators modulators (78,(78,
160).160).
Collectively,
Collectively,these responses
these responses constitute constitute
the the
and
and recognizing
recognizingwhich whichaspectsaspects ofof human
human brainbrainfunction
function animal animal defensivedefensive organismic
organismic state.state.
Such Suchstatesstates
are multidimensional,
are multidimensional, not not
research
researchisismostmostrelevant
relevant to to
givesgivesa more
a more realistic viewview
realistic of what of whatto to unitary
unitary (3, (3,
9, 41, 119);119);
9, 41, different
different componentscomponents may bemay activated to
be activated to
expect
expect from
fromthis thiswork.
work. This
This viewviewis consistent
is consistent withwiththe newthe newfocusfocus different different degrees
degrees under different
under different conditions,
conditions.
awayfrom
away fromdiagnostic
diagnostic categories
categories of psychiatric
of psychiatric disorders disorders
and to and to- The Theglobal
global defensive
defensive organismic
organismic statestate can be canthought
be thought of as of as
wardbasic
ward basicbrain
brain mechanisms
mechanisms that that
may be may be altered
altered (145). (145). a "metaconditioned a "metaconditioned response"response"
that depends thaton the more
depends on specific
the more specific
In sum,
sum, itit seems
seemsobvious
obviousthat that scientists
scientists should
should be asbe precise
as precise as as constituent
constituent conditioned
conditionedresponses. In this view,
responses. In this theview,
globalthe state is
global state is
possible
possible totoshort-circuit
short-circuit thethe opportunity
opportunity for formisunderstanding.
misunderstanding. If If not nota cause
a cause of the
of the specific
specific
conditioned
conditioned responses, responses,
as is sometimes
as is sometimes
we can
we canavoid
avoidconfusion
confusion by simply
by simply changing
changing the terms,the terms,
why would why wouldassumed assumed (9, 38,54-57),
(9, 38, 54-57), butbut rather
rather a consequence.
a consequence. This needsThis needs
we
we not not
do it? do it? some clarification because some "state"
clarification is often
because "state" used is ambiguously.
often used ambiguously.
There
There is, is,of course,
of course, some neural some stateneural
that occurs statelocally thatinoccurs the local
Survival
Survival CircuitsCircuitsand Global and Organismic
Global States
Organismic States
survival circuit survival
when it is activatedcircuit by when
a threat and it thatis activated
accounts < " by
Having
Having argued
argued for a for different a different
way of talking way about of Pavlovian
talking for theabout Pavlovian
initial defense response. for the
Also, initial
during defensethe
conditioning, — 1/1
uresponse.
< —
^

aversive
aversive conditioning,
conditioning, I will putI the will ideas put the ideas
described above CS and US both
described
into elicit neural
above into states CS and that US interact
both as part
elicit of neural
as sta
2
2 >>
practice
practice using using
two conceptstwo concepts that I recently that I recently
introduced: survivalsociative
introduced: learning.survivalSome, if not most, who
sociative have used the
learning. Some, nonO t if not
o £

circuits and
circuits and global
globalorganismic
organismicstates states (3).(3). subjective central state of
subjective fear state
central construct
of fearlikely construct havelikely had havethis had localthis local S§
5g
A neural
neural circuit
circuit that that underlies
underlies the theexpression
expressiondefense defenseresponses
responsesstate notion
state notion in inmind.
mind. Models
Modelsthat thatargue argue thatthat a US-induced
US-inducedaf ££8S
af
elicited
elicited by byconditioned
conditioned and and unconditioned
unconditioned (presumably
(presumably innate) fective
fective state
innate) associated with
state is associated withthe theCS CSduring
duringlearninglearning maymay alsoalso
threats
threats can canbe becalled
calleda a"defensive
"defensive survival
survival circuit"
circuit" (3), (3),whichwhichishave
have
is a alocal
local neural
neural state
state in mind mind (34, (34, 48,48,49, 49,161).
161).Calling
Callingthese these
similar to what what has has been
been calledcalled aa defense
defense system system(19, (19,34,119,130).
34,119, 130).local responses
local responses central
centralstatesstatesof offearfearconfuses
confuses them with with the the
There areare aa number
number of of defensive
defensivecircuits circuitsininthe thebrain
brain(146). (146).Theseglobal
These globalstatesstates being
being discussed
discussedhere herethat thataffect
affect widespread
widespread brain brain
together
together constitute
constituteone oneofofseveralseveral classes
classes ofof survival
survival circuits,
circuits,in- areas,
areas,
in as as wells
wells asasthethebody,
body,and andare arenecessarily
necessarily slower slower to to unfold.
unfold,
eluding
cluding circuits
circuitsfor foracquiring
acquiringnutrients nutrients and and energy
energy sources,
sources,bal-Although
Althoughthe
bal thedefensive
defensiveorganismic
organismicstate, state, as as II view
view it, it, does
does not ac
ancing
ancing fluids,
fluids,thermoregulation,
thermoregulation, andand reproduction
reproduction (3,19, 119, 147,count
(3,19,119,147, countfor forrapidly
rapidlytriggered
triggered default defensive responses,
default defensive responses,like likefreez
freez
148, 149).
148, 149).Survival
Survivalcircuits
circuits areare conserved
conserved within within mammalian
mammalian spe- ing, spe ititmay
ing, maycontribute
contributeto toother
otherspecies-typical
species-typicaldefensive defensivethat thatemerge
emerge
cies and,
cies and, to tosome
someextent,
extent,between between vertebrates.
vertebrates. Invertebrates
Invertebrates havehaveas the
as the threatening
threatening situation situation evolves
evolvesover overtime time(9, (9,19,19, 51,51,52).
52).
different
differentcircuitcircuit schemes
schemes thanthan vertebrates
vertebrates but nevertheless
but nevertheless have have However,
However, an an unresolved
unresolved issue
issue is isthetheextent
extenttotowhich whichglobal global
that perform
circuits that perform similar similar survival
survival functions
functionsand andthat thatappear
appear organismic
toto organismic states, as opposed
states, as opposed theirtheircomponent
component processes,processes, have have
be precursors
precursors of of survival
survivalfunctions functionsininvertebrates vertebrates(15, (15,21,21,150-a causal
150 a causal role role ininbehavior.
behavior.Is, Is,in inother
other words,
words, the global state
the global state
152).
152). Related
Related survival
survivalfunctions
functionsalso alsoexistexist inin single
single cellcellorganisms,
organisms, greater
greaterthan than the the sum
sum of its its component
componentparts? parts?Such Such states
states are,are,
in in
and
and thus
thus predate
predateneuronsneurons and and circuits
circuits (3) (3)
andand likelylikely depend dependon principle,
on measurable
measurable and and are are thus
thusnot notsimply
simplyreified reifiedconstructs,
constructs.
mechanisms that that are
are primitive
primitive precursors
precursors of of neuronal
neuronal elements elements However,
in
inHowever, whether
whether thethe state
state itself
itselfhas hasa acausal
causal rolerole beyond
beyond the the
animals
animals (153). neural activity occurring in the
(153). neural specific
activity occurring circuits in the that specific process
circuits that threats,process threats,
A
A notable
notable consequence
consequence of activating
of activating a survival a survival
circuit is that circuita
retrieve ismemories,
that a retrieve generate arousal,memories, generateand
select responses, arousal,
motivateselect resp
global(body-wide)
global (body-wide) state stateemerges emerges
in the organism, in the organism, componentsand components
of reinforce behavior of and reinforce
is unclear. Because behavior is unclear.I Because o
of this uncertainty,
whichmaximize
which maximize well-beingwell-being in situations in situations
where challenges whereorprefer challenges
op the expression
or op- prefer defensive the organismic
expression state defensive
over relatedorganism
portunities
portunities exist
exist
(3, 148).(3, 148)."Global "Global
organismic organismic
states" in mammals states" in mammals
expressions expressions
[i.e., central motive state [i.e., central
(45, 46), central motive state(9,(45, 46), c
fear state
and
andother
other vertebrates,
vertebrates, like thelike survival
the circuits
survival thatcircuits
initiate them,that initiate
38, 54-57), them, 38,
or defensive 54-57), or
motivational defensive
state (34, 41,130)] motivational
that imply state (3
areelaborations
are elaborations of similar
of similar states in states in invertebrates
invertebrates (151, 154, 155). (151,
that the 154,state155).itself that
organizes theand state itself
controls organizes and controls beh
behavior.
Thestate
The state thatthatresults results
when anwhen organism an isorganism
in danger, as is we
inhavedanger,
Regardless, as we have to
however, Regardless,
the extent that however,
defensive toorganismic
the extent that d
seen,has
seen, hasbeen been
called called
a central a central
state of fear. stateThis of construct
fear. This states,
played construct or their played
components, states, contribute
or theirresponse components, selection,contribute
mo r
an
an important
important rolerole in advancing
in advancing research on both Pavlovian
research on bothtivation, and
Pavlovian and tivation,
reinforcement, or other reinforcement,
processes, it is not orbecause
otherthey processes, i
aversive
aversive instrumental
instrumental conditioning.
conditioning. Now that Now neuroscience has
that neuroscience
constitute a statehasofconstitute
consciously experienceda state offear. consciously
The latter is experienced
an
made
madeprogress
progress in replacing
in replacing Hebb's Hebb's conceptual conceptual
nervous system nervous system almost
almost unavoidable, yet mostly unavoidable,
unintended, yet mostly
implication of unintended,
much i
(47)
(47)with
with circuits
circuits and mechanisms
and mechanisms that underlie thatPavlovian
underlie aversive
Pavlovian
of the central aversive fear stateof the central
literature. fear state
A conscious stateliterature.
of fear mayA conscio
conditioning,
conditioning, and and is beginning
is beginning to do theto samedo for theinstrumental
same for occur, but that is not
instrumental the factor
occur, but that thatselects,
is notmotivatesthe factor and/or that select
aversive
aversive tasks
tasks (49, (49,
156-158), 156-158), we can we ask can moreask more specifically
specifically about
reinforces behavior. about reinforces
A similar argument behavior. has beenA similarmade for argument
ap ha
what
whatsuch such a state
a state does.does. I think renaming
I think the state the
renaming would help
statepetitivewould help petitive
instrumental behaviors instrumental
(eating, drinking, behaviors
and sexual(eating,be drin
facilitate
facilitate thisthis
research
research and its and interpretation.
its interpretation. The expression Thehavior,expression
and behaviors havior,relatedand to use behaviors
of addictive related to use of addict
drugs)—circuits
"defensive
"defensive organismic
organismic state" captures
state" captures the spirit and theemphasis spirit and andcellular
of emphasis of and cellular
and molecular mechanisms and molecular
involved mechanisms inv
in reinforcing

LeDoux PNAS | February 25, 2014 | vol.111 | no. 8 | 2875

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and motivating these are not the same mechanisms that give rise materials that nonemotional experiences lack. What distinguishes
to conscious states of pleasure (83, 162, 163). the various kinds of fears (fear of a snake, of social situations, of
I thus assume, until proven otherwise, that a defensive or being late for an appointment, of having a panic attack, of an ex
ganismic state and its constituent components are implicit (non amination, of falling in love, of failure on a task, of not leading
conscious). If so, to be felt as fear, the state or its components have a meaningful life, of the eventuality of death) is also the combi
to become a presence in conscious awareness (3-6). This can only nation of raw materials involved (4, 5, 170, 172, 176). Some fears
happen in organisms that have the capacity to be aware of brain depend on survival circuits but others do not. The "survival-circuit
representations of internal and external events, and may also re dependent" kind of fear is the romanticized version but is not the
quire the ability to know in a personal, autobiographical sense that only kind of fear we have. Fear is what happens when the sentient
the event is happening to them (164). In short, someone has to be brain is aware that its personal well-being (physical, mental, social,
home in the brain to feel fear. Infants can react in "emotionally" cultural, existential) is challenged or may be at some point. What
long before they can feel emotion (165). Similarly, it is possible, in ties together all instance of fear is an awareness, based on the raw
fact likely, that animals can react "emotionally" without feeling materials available, that danger is near or possible. A theory of fear
emotional (even if they in some situations do feel emotional). In has to account for fears that do and do not involve survival
the end, as I have noted, the question of whether animals react but circuit activity.
do not feel, or whether they both react and feel, is, in my opinion, Fear can be thought of as emerging in consciousness, much the
not something we can determine scientifically. way the character of a soup emerges from its raw materials, its
By using different terms for conscious feelings and the non ingredients. Start with salt, pepper, garlic, onions, carrots, and
conscious events that can, in some organisms, contribute to chicken. Add roux and chicken soup becomes gumbo, or add
feelings in the presence of threats, much of the ambiguity and curry paste, and it shifts it in a different direction. None of these
confusion about the neural mechanisms that detect and control are soup ingredients. They are just things that exist in nature and
responses to threats, and neural states that may result, is that avoi can be combined to make soup or many other things. Sim
ded. Furthermore, research on these mechanisms can be con ilarly, emotions emerge from nonemotional ingredients, events
ducted without having to struggle with questions about whetherthat exist in the brain and body as part of being a living organism
the animal does or does not experience fear. These mechanismsof a particular type (e.g., survival circuit activity, brain arousal,
can be studied the same in humans and other animals, including body responses and feedback, memories, thoughts, predictions).
invertebrates. Fear itself, although, is best studied in humans. No one ingredient is essential to fear. Variation in the kind and
amount of ingredients determine whether you feel fear, as op
Fear Itself
posed to some other emotion, and also determine the variant of
Restricting the term fear to the conscious experience that occursfear you feel. Barrett has expressed a related view (134).
when an organism is threatened eliminates the awkward dis We do not know whether other organisms have feelings of fear
tinction that is required when theorists assume that some emoor other states of consciousness. However, even if they experi
tional feelings are innately wired in brain circuits and others areence conscious states of awareness, these states are likely to be
psychologically or socially determined (61, 159, 166, 167). I dovery different from ours (177). Our experiences depend, in part,
not think of emotions in this dualistic way, where fear is a bot on our capacity for natural language, as well as other cognitive
tom-up state that is unleashed in a prepackaged pure form ofcapacities (134). The idea that language and culture shape expe
experience stored in a hardwired subcortical circuit, and otherrience (178), including emotional experience, is currently thriving
feelings are cognitively constructed. in psychology (176, 179-183). We have English words to distin
My conception is more aligned with theories that propose thatguish more than three dozen variants of fear-related experiences
feelings result from the cognitive processing of situations in which(184). Animals, lacking our language and culture, cannot experi
we find ourselves (168-175). In my view, the feeling of fear occursence the world the way we do. Their feelings, if they have them,
in the same way as the feeling of compassion or pride—through cannot be like those made possible by our brain's capacities to
cognitive processing of neural raw materials. Some feelings involve conceptualize, categorize, label, and interpret, and to introspect
raw materials provided by activation of survival circuits and theirabout and consciously experience, our outer and inner worlds.
consequences, but others do not. Fear often does, but pride or As Kagan says in the opening quote, the mechanisms that
compassion typically does not. What distinguishes kinds of emoallow organisms to respond to threats are different from the
tional experiences is the combination of raw materials that are inmechanisms that give rise to conscious fear. Using terms that
play. What distinguishes emotional experiences from nonemotionalacknowledge this difference will help avoid confusion about what
experiences is the fact that emotional experiences have raw we study and what it means as our field moves forward.

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