Emotion, Motivation, and Anxiety: Brain Mechanisms
and Psychophysiology
Peter J. Lang, Margaret M. Bradley, and Bruce N. Cuthbert
The organization of response systems in emotion isfounded on two basic motive systems, appetitive anddefensive. The subcortical and deep cortical structuresthat determine primary motivated behavior are similar
across mammalian species. Animal research has illuminated these neural systems and defined their reflex outputs. Although motivated behavior is more complex andvaried in humans, the simpler underlying response patterns persist in affective expression. These basic phenomena are elucidated here in the context of affective perception. Thus, the research examines human beings watchinguniquely human stimuli—primarily picture media (butalso words and sounds) that prompt emotional arousal—
showing how the underlying motivational structure isapparent in the organization of visceral and behavioral
responses, in the priming of simple reflexes, and in thereentrant processing of these symbolic representations inthe sensory cortex. Implications of the work for understanding pathological emotional states are discussed,
emphasizing research on psychopathy and the anxiety
disorders. Biol Psychiatry 1998;44:1248 –1263 © 1998
Society of Biological Psychiatry
Key Words: Emotion, anxiety, brain mechanisms, motivation, fear

IntroductionT

he aims of this paper are twofold. First, a theoreticalmodel of emotion is presented that is founded on basic
experiments from both the animal and human researchlaboratories. In this view, emotions are held to be productsof Darwinian evolution. Expressed emotions developed
from primitive actions that facilitated the survival of
species and individuals. In man, the evolved affects are
best characterized as motivationally tuned states of readiness. The second aim of this paper is to show how thisapproach generates a useful technology, facilitating particularly the study of human anxiety disorders. Applica-

From the NIMH Center for the Study of Emotion and Attention, University of
Florida, Gainesville, Florida.
Address reprint requests to Peter J. Lang, PhD, Box 100165 HSC, University of
Florida, Gainesville, FL, 32610.
Received April 16, 1998; revised August 10, 1998; accepted August 21, 1998.

© 1998 Society of Biological Psychiatrytions are described that can aid in the differential diagnosisof anxiety. Research is presented, showing that psychophysiological analyses conducted during initial patient
evaluation can help predict success in therapy.

The Motivational Organization of Emotion
Patterns of emotional expression are highly varied. Theorists have compiled categorical lists that include as many
as eight (Plutchik 1962) or 10 (Izard 1977) so-called
primary affective states, augmented by various blends.
Verbal reports of affects can have a great richness andsubtlety of discrimination, with hundreds of emotionallydescriptive words available in natural language lexicons. It
is proposed here, however, that the evolutionary foundation of emotion has a simpler, two-factor motivationalorganization. That is, affects are organized by brain
systems that adaptively respond to two basic types ofstimulation, appetitive or aversive. This biphasic organization of emotion has been proposed by many theorists.
Konorski (1967), for example, developed a model basedon a typology of unconditioned reflexes and their biological, motivational roles. Exteroceptive reflexes were either
preservative (e.g., ingestion, copulation, nurture of progeny) or protective (e.g., withdrawal from or rejection of
noxious agents). Preservative emotions include such affects as sexual passion, joy, and nurturance; fear and anger
are representative of protective affects. Dickinson and
Dearing (1979) further developed Konorski’s dichotomy
into two opponent motivational systems, aversive andattractive, each activated by a different, but equally wide
range of unconditioned stimuli, determining perceptual–
motor patterns and the course of learning.
The view that affects might be organized by overarching motivational factors has also been suggested byresearchers studying subjective reports of emotion, beginning with Wundt’s (Wundt 1896) “mental chemistry.”
Contemporary studies of natural language categories(Shaver et al, 1987; Ortony et al 1988) suggest thatemotional knowledge is hierarchically organized, and thatthe superordinate division is between positivity (pleasantstates: love, joy) and negativity (unpleasant states: anger,sadness, fear). Osgood and his associates (e.g., Osgood et0006-3223/98/$19.00
PII S0006-3223(98)00275-3

Emotion and Anxiety

al 1957), using the semantic differential, earlier showedthat emotional descriptors were primarily distributed along
a bipolar dimension of affective valence—ranging fromattraction and pleasure to aversion and displeasure. A
dimension of activation—from calm to aroused—also
accounted for substantial variance. Similar conclusions
have been drawn by other investigators based on verbal
reports (e.g., Mehrabian and Russell 1974; Russell 1980;
Tellegen 1985), as well as facial expressions (Schlosberg
1952).
The view taken here merges these lines of theoreticaldevelopment. It is postulated that two motivational systems exist in the brain, appetitive and defensive, and thateach can vary in terms of activation or arousal. That is,arousal is not viewed here as having a separate substrate,
but rather as representing intensity of activation (metabolic and neural) of either the appetitive or aversive system,or the coactivation of both systems (see also Cacioppo andBernston 1994). The varying emotional states, observed
and reported, reflect these basic motive systems. That is,
the motive system determines the general behavioral
strategy, defense or appetitive acquisition. The specificsomatic and autonomic patterns of affective responding
are tactical, in that they are formed by the behavioral
context. To give an example from the observation ofanimals, if a caged rat is subjected to electric shock on thefoot pads, the defense system is engaged. It is then likely
to 1) flee if an exit is available (“fear”), or 2) attack acagemate if one is present (“anger”). If shocks are repeatedrandomly and uncontrollably it will 3) first cower helplessly and then become dull and unresponsive (“depression”). Although emotions may come in many forms,
shaped by genetics and learning to fit the demands of local
context, their fundamental organization is motivational.
Thus, their primary description is in terms of affective
valence (i.e., appetitive or aversive) and arousal (intensityof activation).

Patterns of Human Emotion
The behavior of very primitive organisms can be wholly
characterized by two responses: direct approach to appetitive stimuli and withdrawal from aversive stimuli (seeSchneirla 1959). This modest behavioral repertoire cannot,
however, implement the many subgoals of human beings
nor effectively deal with the perceptually rich, complex
environment in which we live. Elaborate instrumental acts,
behavioral delay, and response inhibition have evolved,
complicating the path of simple bidirectional goal-related
behavior. Thus, emotional behaviors in humans are more
adaptive and creative, and less predictable than those ofless evolved species.
In human beings, the presumed indices of emotional

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expression include responses in three reactive systems(Lang 1978): 1) expressive and evaluative language; 2)physiological changes mediated by the somatic and autonomic systems; and 3) behavioral sequelae, such as
patterns of avoidance or performance deficits. This is the
database of emotion, and a theory of emotion has to copewith its breadth and diversity. The task is not simple.
Correlations among emotion indices, within and between
systems, are generally quite modest (e.g., Lang 1968;
Mandler et al 1961), and the patterns of response can varyconsiderably within subjects and across different contexts
of stimulation (Lacey 1958; Lacey and Lacey 1970).
Analysis is further complicated by the fact that, whereas
human emotions appear to have derived from primitive
actions, the defining response may never actually occur;
the boss’s insult may incite hostility, but the angry blow is
withheld. In this sense, emotions are often dispositions toaction, with an accompanying physiology of preparationthat is not discharged.
As noted previously, affective expression is in great parta tactical response to contextual demands. Thus, response
patterns in emotion have often proven unreliable, reflecting variability in stimuli and methods across experiments.
If procedures are held constant, however, and standard
emotional stimuli are used, tactical features can be specified and emotion’s underlying strategic framework ofappetite and defense should be highlighted. We haveextensively tested this hypothesis in such a standard
context—viewing emotional pictures—as a method forinvestigating emotion in the laboratory.

Emotion and Perception
Over the past 10 years, we have developed a set ofcalibrated picture stimuli to use in the scientific study ofemotion. There are currently over 600 pictures in theInternational Affective Picture System (IAPS; Lang, Bradley, & Cuthbert, 1997), which includes normative ratingsof the pleasure and arousal associated with each picture,obtained from groups of naive subjects. A representative
sample of IAPS pictures, distributed in the two-dimensional affective space formed by covarying pleasure andarousal ratings, is presented in Figure 1. The overallboomerang-shaped distribution of these picture stimuli
indicates two arms that extend from a common calm,
nonaffective base toward either the high-arousal pleasantor the high-arousal unpleasant quadrant. This organizationis consistent with an underlying bimotivational structure:
two systems of appetitive and aversive motivation thateach vary along a dimension of arousal. Despite considerable effort to fill gaps in this affective space (e.g., in theunpleasant–low arousal quadrant) and force a circumplex
model, this pattern has remained relatively stable, and is

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P.J. Lang et al

Figure 1. Distribution of pictures from the IAPS standardization sample of men and women, plotted in a two-dimensional affective
space, defined by the mean ratings of pleasure (y-axis) and arousal (x-axis) for each stimulus. The separate limbs of the overallboomerang-shaped distributions are consistent with the hypothesis that emotional reactivity is organized by two underlying neuralsystems—appetitive and defensive—that each vary in arousal.

very similar for collections of acoustic stimuli [International Affective Digitized Sounds (IADS); Bradley etal 1998] as well as verbal materials [Affective Norms
for English Words (ANEW); Bradley et al 1998] (seeFigure 1).

The Psychophysiology of Picture Processing
Research has demonstrated that these photographic images
evoke a broad range of emotional reactions, varying in
intensity, and involving both pleasant and unpleasantaffect (e.g., Greenwald et al 1989; Lang et al 1993). As
Figure 2 illustrates, a number of physiological systems
covary significantly with pleasure or arousal, as defined byevaluative judgments. When valence ratings are ranked
from the most to the least unpleasant for each subject,facial muscle activity during picture viewing is strongly
related to differences in affective valence; corrugator(“frown”) electromyographic (EMG) activity increases
linearly as pictures are rated as more unpleasant; conversely, zygomatic (“smile”) EMG activity increases withjudged pleasantness. Heart rate is also responsive todifferences in affective valence; unpleasant pictures generally prompt marked deceleration during viewing,whereas greater acceleration is obtained when viewing
pleasant pictures.
Other evoked responses vary with changes in rated
arousal, rather than affective valence. Skin conductanceactivity covaries positively with judged arousal, increasing
monotonically with increases in rated arousal, regardlessof picture valence. The slow cortical response evokeddirectly by the picture stimuli is also directly correlatedwith stimulus arousal; both pleasant and unpleasant arousing pictures prompt a marked positive-going slow wave
(Cuthbert et al in submission). This positive slow wave issustained for nearly the entire viewing period, whereas theslow-wave response to neutral pictures is distinctly morenegative. These measures, then, index the intensity or
activation level of the current motivational state, rather
than its direction (i.e., appetitive or defensive).
Behaviors elicited in the context of emotional picture
perception also covary with motivational parameters.
When first exposed to a new picture, reaction time
responses to probes are significantly slower for emotionally arousing, compared to calm, pictures (Bradley et al1992). These data suggest that new activating images may
require more attentional resources at encoding. Choiceviewing behavior also covaries with arousal. When normal

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Figure 2. Covariation of affective judgments of pleasure (top row) or arousal (bottom row) with physiological and behavioral responses
to picture stimuli. Corrugator EMG (top left), zygomatic EMG (top middle), and heart rate (HR) (top right) each vary consistently withdifferences in rated pleasure. On the other hand, skin conductance (bottom left), cortical event-related potentials (ERPs) (bottom
middle), and viewing time (bottom right) vary consistently with differences in arousal ratings. In each plot, affective judgments are rankordered for each subject; the graphs depict the mean responses at each rank across subjects.

subjects are placed in a free-viewing context, unpleasantpictures are viewed as long as pleasant pictures, and bothare viewed for a longer duration than unarousing, neutral
pictures. As might be inferred from the popularity of“slasher” movies, or the habitual slowing of traffic at aroadside accident, normal subjects allocate more processing time to arousing, intense images, regardless of valence.
This relationship does not occur if pictures evoke very
high levels of distress; when phobics view pictures specific to their fear, a palpable reduction in viewing time isfound, consistent with their general avoidant behavior
pattern (see Hamm et al 1997).
As the phobia data imply, relationships between specificmeasures can vary widely for individuals, and to someextent between particular groups. Gender effects are clear.
For example, pleasantness ratings covary more closelywith facial muscle activity in female than male subjects;
on the other hand, skin conductance changes are moreclosely correlated with arousal ratings in male than infemale subjects (Lang et al 1993). Overall, however,motivational variables of affective valence and arousal
predominate in organizing the picture perception data. A
factor analysis (see Tables 1 and 2) of various affectself-report, physiological, and behavioral measures resulted in a strong two-factor solution, with pleasantness
ratings, heart rate, and facial muscles loading on a first,
valence factor and arousal and interest ratings, viewing
time, skin conductance, and cortical slow-wave electroen-

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Table 1. Factor Analyses of Measures of Emotional Picture
Processing
MeasureValence ratings
Corrugator musclea
Heart rate
Zygomatic musclea
Arousal ratings
Interest ratings
Viewing time
Skin conductance

Factor 1 (valence)

Factor 2 (arousal)

.86
2.85
.79
.58
.15
.45
2.27
2.37

2.00
.19
2.14
.29
.83
.77
.76
.74

Lang et al 1993. aBioelectric potentials from muscles that mediate facial
expression.

cephalographic (EEG) activity loading highly on a second,arousal factor. The cross-loadings for all measures arevery low. Thus, affects are built around motivational
determinants. The motivational states elicited by these
affective cues (and the somatic, cortical, and autonomic
substrates of their perception) are assumed to be fundamentally similar to those occurring when organisms stop,
look, and listen, sifting through the environmental buzz forcues of danger, social meaning, and incentives to appetite.

Neural Imaging: Motivation in the Visual Cortex
Using positron emission tomography (PET), Lane et al(1997) examined regions of brain activity in a group of
female subjects, viewing pleasant, neutral, and unpleasantpictures from the IAPS set. The largest blood oxygenationlevel dependent (BOLD) effects were found for unpleasantpictures—in the thalamus and in Brodmann’s visual areas
18 and 19 of the occipital cortex (when activity occasioned
by neutral pictures was subtracted out). Unexpectedly, theactivity prompted by pleasant pictures was not muchdifferent from that for neutral stimuli. This finding wasconsistent, however, with skin conductance recordings
taken coincident with the PET measurement. That is, forthis sample of 10 female subjects, pleasant pictures led tosignificantly less electrodermal activity than unpleasantmaterials.
Table 2. Sorted Loadings of Dependent Measures on Principal
Components
MeasureValence ratings
Corrugator musclea
Heart rate
Arousal ratings
Cortical slow wave
Skin conductance

Factor 1(valence)

Factor 2(arousal)

.89
2.83
.73
2.11
2.06
.19

.07
2.10
2.02
.89
2.79
.77

Cuthbert et al in submission.
aBioelectric potentials from muscles that mediate facial expression.

We recently extended our exploration of brain activity
during emotional picture processing, utilizing functional
magnetic resonance imaging (fMRI; Lang et al 1998). In
this experiment, functional brain activity was monitored inboth female (n 5 8) and male (n 5 12) subjects. Data
were collected while subjects processed pleasant, neutral,and unpleasant pictures. Results again indicated more
extensive activity in occipital cortex when viewing bothpleasant and unpleasant picture viewing, relative to viewing neutral pictures (Figure 3, upper panel). In general, alarger area of activation was found in the right than in theleft visual cortex. Although all stimulus contents activatedarea 17 in the calcarine fissure, areas specific to emotional
stimuli were apparent in Brodmann’s areas 18 and 19, inthe fusiform gyrus, and at parietal sites. Echoing the PET
data, significantly more right hemisphere activation was
found in female than male subjects, specifically for unpleasant stimuli (see Figure 3, lower panel). Male subjects,
on the other hand, tended to have a larger area ofactivation for pleasant pictures.
The fMRI data suggest that emotional inputs undergo
more processing than nonaffective stimuli at a very earlystage in cortical afferent analysis. One explanation isbased on research findings with animal subjects by Amaral
et al (1992). These investigators suggest that reentrant
projections from the amygdala feed back to primary visualcortex. The PET experiment results (Lane et al 1997) are
not inconsistent with this view, in that activity temporally
coincident with occipital activation was apparent in theleft ventral temporal stream, including the region of theamygdala. An alternative view has been offered by Posner(1996). He proposed that projections from cingulate cortex
determine attentional priming of the visual area. These
different anatomical hypotheses are testable using functional images of the whole brain during picture processing.
That is, presumed connections between neural structures
can be assessed by covariance methods that assess interacting regions of BOLD activity (e.g., Horwitz 1994).

Motivational Circuits in the Brain
The psychophysiological reactions, patterns of regional
blood flow in occipital cortex, and behavioral responses
that are all evoked by picture viewing reflect (in theirorganization) the engagement of neural structures in appetitive or defensive motivation systems. What we know
about the brain’s motivational systems comes primarily
from animal research, particularly behavioral neurophysiology studies of rodents. An outline of the rat’s defense
motivation system, with its efferent output paths, is illustrated in Figure 4.
Input normally passes from the sense organs to thesensory cortex and then from sensory-specific nuclei of

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Figure 3. Top: Sites of functional activity during processing ofpleasant (left column), neutral (center column), and unpleasant(right column) pictures, compared to no picture processing, as
determined from averaging functional maps across subjects.
Pixel clusters meeting criteria are depicted in outlined white,
located on two successive coronal slices 5 mm thick, with themost anterior slice approximately 10 mm from the occipital pole.
Top row: In this most anterior slice, all stimulus picture contents
show activity centered on the calcarine fissure; only emotional
pictures are beginning to show activity in the right occipitalgyrus (MRI view, i.e., from an anterior perspective). Second
row: All picture contents continue to show activity centered on
the calcarine fissure, as well as in a portion of Area 18 directly
above the calcarine fissure. Only emotional pictures show
bilateral activity in the occipital gyrus (Lang et al, 1998).
Bottom: Functional activity in the right posterior occipital cortex
during processing of emotional and neutral pictures for men andwomen. Women show significantly more activation for unpleasant than pleasant pictures; men tend to show an opposite effect,
greater activation for pleasant than unpleasant stimuli.

the thalamus to the amygdala. Efferent to the amygdala,
the aversion circuit branches, with each path apparently
governing separate response outputs. Direct projections to
the nucleus reticularus pontis caudalis modulate the startle

response, potentiating the reflex in the context of nociceptive and fear-conditioned stimuli (e.g., Davis 1989, 1997;
Davis et al 1987; Fendt et al 1994). Autonomic response(e.g., blood pressure change) is dependent on an intact

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reduced in the context of signals that specifically indicate
the animal is safe from painful shock (Falls and Davis
1995). Other work shows that startle is reduced in thepresence of a stimulus that has previously been paired witha primary reward (Schmid 1995). Neither startle reduction
in “safe” environments nor the inhibition found in thecontext of reward require amygdala activation. “Pleasureattenuated startle” does depend, however, on an intact
nucleus accumbens (Koch et al 1996). “The finding thatthe mesolimbic dopamine system is involved in thisphenomenon suggests that other parts of the complex
limbic–striatal–pallidal circuitry that governs reward-related behavior . . . might also be relevant for the reductionof the ASR (acoustic startle response) in the presence of astimulus that predicts reward” (Koch and Schnitzler 1997,
p 45; see also Robbins and Everitt 1996).

The Emotional Priming Model

Figure 4. Defense motivation system. Unconditioned and conditioned aversive stimuli proceed from sense receptors to sensory
cortex and/or sensory thalamus (see Le Doux 1990). The lateral
nucleus of the amygdala receives input signals from the thalamus, transmitting them to the amygdala’s central nucleus. There
are three important connections efferent to the amygdala: a) a
projection from the central amygdala to the lateral hypothalamicarea that mediates the autonomic emotional response; b) projections to the midbrain central gray region, which mediates coping
behaviors (see Fanselow et al 1995); and c) a direct projection to
the nucleus reticularis pontis caudalis, which modulates thestartle circuit (see Davis 1989, 1997 for details).

pathway through the hypothalamus (LeDoux 1990),
whereas somatic components require an intact midbrain(i.e., periaqueductal central gray). Furthermore, the ventral
central gray is the fear “freezing” path, whereas the dorsal
gray is a critical part of the fight/flight action circuit (seethe data and discussion of Fanselow et al 1995, and thepapers edited by Depaulis and Bandler 1991). Taken
together, the neurophysiological findings suggest that theamygdala is a key site in the defensive motivational
system; structures “downstream” from the amygdala are
implicated in the different types of defense behaviors.
Some of these same neural structures are active inappetitive motivation; other nuclei are specific to theappetitive system, mediating different outputs or inhibiting
defense responses. The startle reflex, for example, isexaggerated in defensively motivated rats. It is, however,In addition to organizing responding to specific affecteliciting input, the active motivational system exerts a
modulatory effect on other processing operations in thebrain. This means that memory associations, action programs, and other representations that are linked to theengaged motivational system are specially “primed.” Thatis, they are preset for activation; they have a higher
probability of being accessed than other information in thebrain (and have a greater potential output strength).
Reciprocally, memories and action programs linked to thenonengaged system have a reduced probability andstrength of activation. To provide a cognitive example: if
we give a subject the category prime “baked goods,” hisfirst association to the word “roll” might well be “bread.”
Conversely, the associations “wagon” or “skates” would
be much less likely, and perhaps even actively inhibited. A
quite different result would be expected, of course, if thecategory prime was “toys” or “playthings.” Priming is an
automatic process (McKoon and Ratcliff 1980). It can takeplace outside awareness, e.g., when priming stimuli arepresented rapidly, below recognition threshold. Thismechanism may explain why negative, unpleasant associations are more probable in depressed individuals, or why
anxious patients respond more rapidly to “threat” cues.
The most primitive and fundamental motivational priming is at the level of unconditioned exteroceptive reflexes.
It will be recalled that reflexes can be sorted (Konorski1967) according to the primary reinforcement propertiesof their unconditioned stimuli, either appetitive or aversive, and the consummatory or defensive function of thereflex itself. In the priming view, responses to unconditioned stimuli are modulated depending upon the relationship between: 1) the motivational, biological role of thereflex—appetitive as in salivation or defensive as in pain

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withdrawal; and 2) the currently active motivational state,appetitive or defensive, in the neural circuits of thesubcortex. An independently evoked defensive reflex
should be augmented when the organism is already reacting to an aversive foreground stimulus (i.e., is in a
defensive state); this same reflex will be reduced inamplitude when the organism is processing an appetitive
foreground. Finally, both these priming effects—potentiation and diminution of responding—are expected to beenhanced according to the level of affective drive or
activation.

Startle Modulation
The startle response has proven to be a convenientdefensive reflex for testing the above hypotheses. In most
mammals, an abrupt sensory event will prompt a chainedseries of rapid flexor movements that cascade throughout
the body (Landis and Hunt 1939). This startle reaction
appears to be a primitive defensive reflex that serves a
protective function, avoiding organ injury (as in theeyeblink), and acting as a behavioral interrupt (Graham
1979), clearing processors to deal with possible threat.
Abruptness is the key to startle elicitation; the risetime ofthe eliciting stimulus should be instantaneous. In humansubjects, sudden closure of the eyelids is one of the first,
fastest (occurring within 25– 40 msec after startle stimulus
onset), and most stable elements in the reflex sequence,and this blink component is measured in the studies
reported here. Electromyograph electrodes placed justbeneath the eye (see Anthony 1985; Lang et al 1990) sense
the bioelectric potentials produced by orbicularis oculi
contraction, allowing one to measure the onset latency andmagnitude of this muscle activity. Although strong stimuli
generate larger and more reliable reflexes, high stimulus
intensity is not necessary to evoke a reaction.
According to the motivational priming hypothesis, thedefensive startle reflex should be of significantly greater
amplitude (and faster) when the aversive motivational
system is active, e.g., as in a fear state. Alternatively, if
appetitive system activation predominates, as in states ofpleasure, the startle reflex should be attenuated (see Figure5). Evidence for defense system priming of the startle
reflex has been found in both animal and human studies offear conditioning. This was first examined systematicallyby Brown et al (1951), who compared reflex responses tostartle probes (shots from a toy pistol) presented to malerats during neutral or shock-conditioned stimuli at extinction. Results conformed to expectation; animals did indeed
react more forcefully when the startle stimuli were presented during fear-conditioned signals (see also Ross 1961;
Spence and Runquist 1958). As already noted, appetitive
priming of the startle reflex in animals has also been

Figure 5. Startle reflex priming. Probe stimuli (acoustic, auditory, or tactile) activate the pontine startle circuit, resulting instartle reflex output. When previous aversive unconditioned orsymbolic stimuli activate the defense motive system, its direct
projections to the startle circuit potentiate (augment) this reflex
response. Alternatively, when the appetitive motive system is
active, its projections to the startle circuit result in reflex
inhibition.

demonstrated, i.e., probe reflex responses are attenuated bothduring “safety” signals and in the presence of stimuli associated with reward (e.g., Koch and Schnitzler 1997).
Several studies have confirmed reliable potentiation of
the blink response in humans following simple shock
exposure or as a function of learned associations thatparallel the modulatory patterns previously obtained withrats (Greenwald et al in submission; Hamm et al 1993;
Grillon and Davis 1995). In brief, the blink response to astartle probe is generally larger after subjects experienceelectric shock, and selectively larger to startle probes
presented during exposure to a shock-conditioned stimulus
than to probes presented during exposure to an unshocked
control stimulus. Wide use has been made of startle probes
in the assessment of human attention.

Probing Emotional Perception
As mentioned earlier, picture viewing is an observational,
intake task in which—like a “freezing” rat or an attentive
predator—subjects are generally immobile, with sensory
processors engaged. When startle probes are administered

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tation of the same picture stimuli. That is, although there
is an overall diminution of the startle reflex over blocks oftrials with the same pictures, affective potentiation andinhibition remain to the last trial block (Bradley et al1993). Similarly, affective modulation persists when thesame set of pictures is viewed in separate experimental
sessions (Bradley et al 1995).

Figure 6. The startle reflex is clearly modulated by affective
valence, with blinks elicited when viewing unpleasant picturespotentiated, and blinks evoked when viewing pleasant pictures
inhibited, compared to neutral stimuli. Although the overallmagnitude of the blink reflex decreases (i.e., habituates) withrepeated presentation, affective modulation of the startle reflex
continues to occur both when pictures are repeated within asession (top panel, Bradley et al, 1993) and between sessions(bottom panel, Cuthbert et al, 1996).

in this context, results have consistently conformed to themotivational priming hypothesis as Figure 6 illustrates,
there is a startle inhibition during pleasant stimuli andstrong potentiation when pictures were judged to be
unpleasant; the largest startle blink responses occurred
during unpleasant content and the smallest during pleasantpictures (e.g., Lang et al 1990; Vrana et al 1988; see
Bradley et al in press for a recent review).
These emotional–perceptual effects seem ubiquitous.
Balaban (1995) found affective picture modulation ofstartle probe responses in 5-month-old infants. Jansen andFrijda (1994), using evocative video film clips, and Hamm
et al (1990), using IAPS pictures, having obtained theaffect–startle effect in European subjects. Interestingly,
emotional modulation of the reflex does not seem todepend on novelty. It persists even with repeated presen-

INTENSITY AND MODALITY. Probe studies of picture
perception have generally employed binaural startle stimuli in the range of 90 –100 dB; however, lower intensities(sufficient to reliably evoke startle) also produce affective
startle modulation (Cuthbert et al 1996). Furthermore,significant affective modulation has been shown withmonaural acoustic probes. In the monaural case, emotional
pictures appear to be differentiated most reliably by probes
presented to the left (presumably conferring an advantage
in right brain processing) compared to the right ear(Bradley et al 1991, 1996).
Affective modulation of startle is observed for picture
stimuli regardless of whether the startle probe is visual,
acoustic, or tactile (e.g., Bradley et al 1990; Hawk and
Cook 1997), suggesting that modality-specific processes
are not primary in these modulatory effects. Furthermore,
affective modulation is not confined to visual percepts;
when the foreground stimuli consist of short, 6-sec soundclips of various affective events (e.g., sounds of lovemaking; babies crying; bombs bursting), and the startle probe
is a visual light flash, the same affect–reflex effect isobtained (Bradley et al 1994). Other researchers havefound startle potentiation in subjects smelling unpleasantodors (Miltner et al 1994; Ehrlichman et al 1995), supporting the view that affective reflex modulation isbroadly motivational and thus consistent across affective
foregrounds of differing stimulus modality.

Psychophysiology and Psychopathology
Consistent with the motivational priming hypothesis, modulatory effects on the startle reflex appear to increase withgreater activation in each motive system. Probe startle
potentiation is largest for unpleasant pictures that are rated
most arousing, whereas conversely, the most arousing
pleasant pictures prompt the greatest probe startle inhibition (Cuthbert et al 1996). Thus, individuals with specificphobia, looking at pictures of the phobic object (e.g.,snakes or spiders) show startle potentiation well beyond
that routinely seen in normal subjects (Hamm et al 1997).
The potentiation is, however, clearly selective; that is,these same phobics show the normal reflex inhibition tostartle probes when looking at arousing pleasant stimuli(See Figure 7, Sabatinelli et al 1996).
Probe reflex inhibition reflects attentional engagement

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1257(Graham 1992), as well as an appetitive motive state.
Consistent with this view, probes presented during lessarousing, unpleasant stimuli—pictures of sad events, pollution, ill people—tend to prompt some reflex inhibition.
Strong potentiation is found mainly during viewing ofhighly arousing stimuli (Cuthbert et al 1996). Interestingly, incarcerated psychopaths show reflex inhibition(relative to neutral pictures) to both arousing pleasant andarousing unpleasant picture stimuli (see Figure 8, Patrick
et al 1993). This probe effect is not reflected in thesubjective reports of psychopaths; they rate the unpleasantpictures negatively, in the same way as normal subjects.
Furthermore, when a subsample of the psychopath groupis selected, based on Hare’s checklist (Hare 1991), who
are high on measures of emotional detachment (e.g.,
showing blunted affect and no remorse for criminal acts),
this reflex inhibition to unpleasant stimuli is further
accentuated. These findings are dramatically different
from what is seen in the normal population, and the exact
opposite of those found in phobic patients. They support
the view that psychopaths may have a deficit in theaversive motivational system (see Lykken 1957).

Anxiety Disorders
The model of emotion outlined here has also guided
research on the anxiety disorders. Two current lines ofresearch are of particular clinical relevance. The first
approach may help to sharpen differential diagnosis, with
implications for the development of more effective treatment plans; the second line of inquiry may prove useful inimproving prognosis.
FEAR AND ANXIETY. Cook et al (1988) studied thepsychophysiological responses of three groups of anxiety
patients—simple phobia, social phobia, and panic disorderwith agoraphobia—all of whom participated in an assessment of their emotional imagery prior to treatment.
In the imagery procedure, texts were presented (overearphones) that describe neutral or fearful situations,which patients were instructed to use as prompts to an
imagined, personal experience of events. Some of the fear
scripts described dangerous encounters that are generally
fear evoking (e.g., an auto accident, an intruder in thehouse); other scripts were developed after interview andwere specific to individual patients. These latter texts
focus on individual clinical problems in an effort toactivate patients’ specific pathological fear. The scripts ofpanic patients, for example, would emphasize themes ofpanic, physiological distress, entrapment, or loss of control, taking place in the supermarket, workplace, or on the
highway. During this imagery, heart rate and skin conductance were recorded. Afterwards patients rate their expe-

Figure 7. Startle reflex blinks evoked by probes presented duringviewing of pleasant erotic pictures, emotionally neutral pictures,and pictures of snakes. Individuals high and low in snake phobia
are compared. For snake phobics, startle potentiation duringsnake pictures clearly exceeds both that found for neutral
pictures and for probe stimuli presented during the nonpicture,intertrial intervals (Sabatinelli et al 1996). Startle is in analogue
to digital units. Startle magnitude during intertrial interval (ITI)
represented by dotted line.

rience of each image for affective valence, feelings ofdominance/control, and intensity of arousal.
In the overall results of an initial study (n 5 133),
patients generally showed strong activation of autonomic responses during fear imagery, relative to neutral
imagery, and reacted with particular intensity to thephobia-related content. Furthermore, no difference be-1258

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Figure 8. Mean blink response magnitudes for startles presented
during viewing of pleasant, neutral, and unpleasant slides, bydiagnostic group: top panel 5 nonpsychopaths; middle panel 5
mixed group (an intermediate group with some psychopathic
features); bottom panel 5 psychopaths; n 5 18 per group.
Group assignment was determined by Hare’s Revised Psychopathy Checklist (Hare 1991). Startle magnitude is expressed instandard score units (mean 5 17; SD 5 10) obtained bynormalizing raw blink magnitude scores within subjects; onset
latency is expressed in raw units (msec) (Patrick et al, 1993).

tween groups was found in their reported fear experience; regardless of diagnosis, patients all rated theirpersonal fear images as very arousing and highly
unpleasant.

P.J. Lang et al

When autonomic responses were examined, however, asignificant group difference emerged in both heart rate andskin conductance reactivity; simple phobics showed thelargest overall reactivity to their clinical fear content, andpanic patients, the smallest. That is, despite verbal reportsof fear that were equal in intensity across groups, the panic
patients were minimally responsive physiologically, relative to the robust reactions of simple phobics. At the time,the data were difficult to interpret. In many ways, thepatients with panic and agoraphobia could be seen as
having a more severe, more generalized disorder. The
findings suggested, however, that the distress of panic
patients might be less focused, less well organized around
specific cues, than is the case with simple phobics.
Recent research with animals provides an interesting
perspective on the above clinical experiment. Phillips andLeDoux (1992) and Kim and Fanselow (1992) havereported a significant neurophysiological difference between cue-explicit fear (fear behavior in the presence of anauditory stimulus that has been reliably followed byelectric shock) and a more generalized fear of the context
in which shock occurs (e.g., the experimental chamber).
Both cue and context prompt fearful freezing in the rat;
however, whereas hippocampal lesions significantly reduced context freezing, they do not affect the incidence of
freezing to an explicit shock cue. A further distinction
between cue-explicit and more generalized fear has been
made by Michael Davis and colleagues. As already noted(see Figure 4), potentiated startle that normally occurs in
the presence of fear cues is eliminated by lesions of thecentral nucleus of the amygdala. Potentiated startle is also
observed after corticotropin-releasing hormone (CRH) is
injected into the cerebral ventricles of the rat, inducing ageneralized state of arousal, resembling anxiety. Unlike
cue-conditioned fear, however, CRH potentiated startle is
not eliminated by lesions of the amygdala’s central nucleus. Instead, this anxietylike, CRH-driven potentiatedstartle appears to depend on a different structure, the bed
nucleus of the stria terminalis (Lee and Davis 1997). Thissame bed nucleus (and not the amygdala’s central nucleus)
is also critical to potentiated startle occurring when rats
(naturally light-avoidant animals) are exposed to a brightly
lit experimental chamber (Walker and Davis 1997). In
brief, the defense system neurophysiological circuit forunconditioned anxietylike reactions appears to involve a
different pathway from that engaged by explicit, conditioned fear cues. The failure of human panic patients toshow clear cue-specific autonomic nervous system reactivity (e.g., to text-prompted memory imagery), despite
clear evidence of high anxiety, may similarly indicate thata different circuit is active in these patients than the one
mediating defense reactions to explicit phobic stimuli.
In a new study of 116 patients and control subjects, theEmotion and Anxiety

Figure 9. Anxiety group differences in blink reflex magnitude tostartle probes administered during three sequential blocks of four
rest trials (i.e., during intertrial intervals between imagery cues).
Ag, agoraphobia.

startle probe reflex was added to the physiological measures being recorded. As previously observed, heart rateincrease during personal fear imagery was again smaller
for panic patients, relative to other diagnoses. Furthermore, panic patients also showed the least reflex potentiation to startle probes presented during these images(relative to their neutral scene response). On the other
hand, the absolute magnitude of startle reflexes was
actually largest for panic disorder. As can be seen in
Figure 9, the panic group (along with a newly added
posttraumatic stress disorder (PTSD) group) showed significantly larger base startle reactions over trials than otherphobic patients. Thus, although panic patients were relatively less reactive than other diagnoses to the specificdistress cues specified at interview, the startle findings
suggest that—like the light-avoidant rat—they were significantly more activated by the general context (i.e., thenovel, perhaps threatening context of psychological test
and evaluation).
Startle sensitivity may characterize patients high innegative affect, a temperamental disposition defined by
Watson et al (1988). In addition to larger reflexes, thepanic patients (along with the PTSD group) had higherscores than simple and social phobics on questionnairemeasures of generalized anxiety and depression (all pvalues ,.01). In a further exploration of these phenomena,
we studied the effects of comorbid mood disorder (DSMIV diagnosis) on startle magnitude. As can be seen in

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1259

Figure 10. Differences in blink reflex magnitude (during rest
trials) between anxiety research subjects with no current comorbid mood disorder and subjects satisfying DSM-IV criteria for acurrent mood disorder.

Figure 10, those in the sample who were also depressed
showed significantly larger base startle reflexes than those
without this comorbidity. Although these are general
phenomena, across diagnoses, it is worth noting that theincidence of mood disorder and the base startle potentiation effect were greatest in the panic disorder group.
IMAGERY AND PROGNOSIS. In an early study ofdesensitization, Lang et al (1970) recorded heart rateduring treatment of snake-phobic subjects. Fear images
reported to be maximally frightening—images so distressing that the subject was temporarily unable to proceed—
were compared across subjects. The degree of heart rate
acceleration evoked by these images was found to besignificantly related to measures of therapeutic outcome(averaged behavior test, observer reports, and self-ratings:
r 5 .75, p , .05). A parallel covariation was foundbetween improvement on these measures of treatment
outcome and the degree of heart rate reduction found withrepeated fear image exposure (r 5 .91, p , .05).
Some years later (Lang 1985), we analyzed data fromanxiety-disordered patients who had been seen in thePsychology Department Clinic at the University of Wisconsin. They had all been administered an emotional
imagery battery prior to treatment, during which heart rate
was recorded, and were subsequently treated with somevariant of cognitive or behavior therapy. Therapists’ re-1260

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ports and case notes were used to distinguish patients who
had been successfully treated from those terminating
treatment prior to the resolution of their distress. Whenthese two groups were compared, successful patients again
showed faster heart rates during personal fear imagery
than were found for unsuccessful cases (Levin et al 1982).
At the University of Florida Fear and Anxiety Disorders
Research Clinic, we continue to assess the imagery responses of anxiety-disordered patients prior to treatment.
Recently, we analyzed the data from 87 patients whose
treatment had been terminated—patients variously diagnosed as simple phobia, social phobia, or panic disorder
who either completed or failed to successfully complete
cognitive– behavioral therapy. In a discriminant function
analysis of the cardiac data, successful patients again
showed significantly higher heart rates in anticipation of,and during fear imagery, than did the noncompleters [R 2
5 .19, F(2,37) 5 4.36, p , .05]. Furthermore, in alarger analysis (including demographic variables, distancefrom the clinic, diagnosis, questionnaire responses, andphysiological reactivity), the heart rate response in imagery was the second best predictor of successful treatment,
second only to pay structure (income and insurance), andahead of the third best predictor, education.

Summary and Conclusions
In the view presented here, emotions are considered to beaction dispositions. It is held that affects evolved fromreflexive, overt reactions to appetitive or aversive stimulation that served immediate survival functions (e.g.,
nurturance, sexual approach, fight, flight). The neuralmechanisms for these functions are preserved in thehuman brain in subcortical and deep cortical structures,
and are the foundation of human emotion. Anxiety andfear are states in which the defensive components of the
motivation circuit are active, and related primitive autonomic and somatic reflexes are engaged. Thus, humanemotional arousal can be measured bioelectrically as
activity (often subovert) in muscles and glands.
We have tried to show experimentally that these physiological data can importantly elucidate the valence andarousal characteristics of emotion, and can be of significant value to the diagnostician and the therapist. Psychopaths show a clear deficit in defense responding, reactingwith probe startle inhibition during stimulation that normal
subjects find fearful and excitatory. Anxiety diagnoses
differ importantly in patterns of emotional processing,perhaps reflecting neurophysiological circuit variants currently being elucidated in animal research. Thus, simple
phobia is a cue-specific disorder, with defense responses
readily activated by explicit phobic imagery; panic disorder appears to be less tied to explicit cues, characterized bya more general hyperreactivity that suggests a temperamental sensitivity of the defense system. Finally, it is
proposed that the degree to which defense responding is
activated by memory imagery may predict subsequent
therapeutic success. Patients showing strong heart rate
acceleration to phobic cues are more likely than low
responders to have completed treatment with a successful
outcome.
Overall, the approach described here underlines theimportance of animal research in providing a neurophysiological foundation for study of human emotion andanxiety. Psychophysiological measurement (including
neural imaging) is clearly the fundamental bridging tool,connecting these advances in basic science to research inpsychopathology. The work implies that clinical analysis
will need to go beyond traditional interview and testing,integrating behavioral and physiological data into a newconception of emotional disorder, with the goal of explicating pathological affects and devising more effective
treatments for anxiety.

This work was supported in part by National Institute of Mental Healthgrants MH37757 and MH43975 and P50-MH52384, an NIMH Behavioral Science grant to the Center for the Study of Emotion and Attention(CSEA), University of Florida, Gainesville, Florida.
Thanks to the many students, postdoctoral associates, and collaborators whose contributions to the research described in this article are
greatly appreciated.
This work was presented at the Research Symposium on “Brain
Neurocircuitry of Anxiety and Fear: Implications for Clinical Researchand Practice” in Boston, Massachusetts, on March 26, 1998. The
symposium was jointly sponsored by the Anxiety Disorders Associationof America and the National Institute of Mental Health through anunrestricted educational grant provided by Wyeth-Ayerst Laboratories.

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