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Psychological Review1990, VoT97, No. 3, 377-395 Copyright 1990 by the American PsychologicalAssociation, Inc.0033-295X/90/S00.75

Emotion, Attention, and the Startle ReflexPeter J. Lang, Margaret M. Bradley, and Bruce N . CuthbertDepartment ofClinical and Health Psychologyand the Center for Research in PsychophysiologyUniversity of Florida

This theoretical model of emotion is based on research using the startle-probe methodology. It ex-plains inconsistencies in probe studies of attention and fear conditioning and provides a new ap-proach to emotional perception, imagery, and memory. Emotions are organized biphasically, asappetitive or aversive (defensive). Reflexes with the same valence as an ongoing emotional state areaugmented; mismatched reflexes are inhibited. Thus, the startle response (an aversive reflex) is en-hanced during a fear state and is diminished in a pleasant emotional context. This affect-startleeffect is not determined by general arousal, simple attention, or probe modality.The effect is foundwhen affects are prompted bypictures ormemory images, changes appropriately with aversive condi-tioning,and may be dependent onright-hemisphere processing. Implications for clinical, neurophys-iological, and basic research in emotion are outlined.

Recent evidence suggests that the vigor of the startle reflexvaries systematically with an organism's emotional state. Athe-ory is presented to elucidate this relationship, suggestinghowthe amplitudeof the eyeblink response to an abrupt, task-irrele-vant probe may be modulated by the affective content of ongo-ing perception and thought.

The present approach defines emotions as action disposi-tions, founded on brain states that organize behavior along abasic appetitive-aversive dimension. It is postulated that allaffects are primitively associated with either a behavioral setfavoring approach, attachment, and consummatory behavioror a set disposing the organism to avoidance, escape, and de-fense. The efferent system as a whole (including exteroceptivereflexes) is presumably tuned according to the current statusof this central affect-motivational organization. Thus, reflexesassociated with an appetitive set (e.g., the salivary response to asucrose probe) would be enhanced if activated when a subjectwas already engaged in a positive emotional response; con-versely, the startle reflex to a sudden loud noise is viewed asan aversive or defensive response and would be augmented if itoccurred in the context of an ongoing aversive emotion. Inshort, reflexes that match a concurrent, tonic affective processwill be amplified. A reciprocal rule is also postulated: A mis-matched reflex (e.g., a defensive reflex initiated during a pleas-ant state ofaffairs) will show relative inhibition or attenuation.

The following discourse explores these general propositions,focusing on the hypothesized modulation of an aversive reflexwhen evoked in the context of various affective states.Analysesare based on a specific data set comprising the results of re-

This research was supported by National Institute of Mental HealthGrants MH37757, MH41950, andMH43975.

Margaret M. Bradley is now in the Department of Psychology, Uni-versity of Florida.

Correspondence concerning this article should be addressed to PeterJ. Lang, Department of Clinical and Health Psychology, University ofFlorida, Box J-165 JHMHC, Gainesville, Florida 32610.

search in which startle stimuli were used to probe cognitive(perceptual and learning) tasks. Webeginwith a description ofthe eyeblink reflex, because this is the component of the startleresponse that has been measured in most probe experimentswith human subjects. Previous research is then reviewed thatsuggests that blink amplitude varies both with attention alloca-tion to foreground tasks and with fear conditioning. Problemsin the theoretical interpretation of these data are elucidated,and the view that the startle-probe response is modulated byemotional valenceisoffered as an integrative solution. The rela-tionship between reflex excitation and the dimensional organi-zation of emotion is elaborated later in this article. An explicittheory isdescribed: Five hypotheses aregenerated (two primaryand three ancillary), each ofwhich istested byexperiment. Theresults consistently support the view that the startle reflex ismodulated by the valence of ongoingaffective responses, inde-pendent of probe modality and regardless of whether the affec-tive foreground content is perceptual or imaginal. These dataprompt a reevaluation of attention- and arousal-theory expla-nations of probe findings. This new affect-startle effect is thencritically examined. Issues addressed include the relationshipof the blink reflex to concurrent facial and visceral responsepatterns, possible neurophysiological limitations, the signifi-cance of emotional intensity for startle modulation, and theeffects of conditioned changes in emotional responding. Thefinal section is a deliberation on the role ofaffect ininformationprocessing and proposes new directions for the study of emo-tion.

The Startle Reflex and the EyeblinkEarly interest in the human startle response wasstimulatedby the work of Landis and Hunt (1939). Apistol shot activated

the startle reflex in their experiments, and subsequent move-ment was recorded with high-speed motion pictures. Drawingsof the rapidly unfolding, whole-body startle were frequently re-produced in textbooks (e.g., Woodworth & Schlosberg, 1956).

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Figure 1. Left panel: Illustration of the orbicularis oculi and corrugator muscles on the left side of the faceand the placement of the eyeblink recording electrodes when positioned beneath the right eye. Toprightpanel: A muscle action potential from orbicularis, recorded during a blink reflex. Bottom right panel: Anintegration of this same signal, which is the response waveform scored for peak amplitude and latencyin most human subject studies of the probe reflex. (EMG = electromyogram; A-D = analog-to-digitalconversion.)

Its gross features include a forward thrusting of the head and adescending flexor wave reaction, extending through the trunkto the knees. The first, fastest, and most stable element in thesequence is the sudden closure of the eyelids. The primacy ofthe eyeblinkhas been confirmedbysubsequent research, whichfurther showed that lid flexion alone may occur to stimuli notsufficiently strong to engage the whole reflex. Because of theseresponse properties, the eyeblinkhas become an important toolin experiments probing such diverse phenomena as classicalconditioning and cognitive resource allocation in attention. Al-though studies vary widelyin subject populationand theoreticalorientation, they consistently show that variations in the inten-sity of the blink indexes the brain's receptivity to informationinput.Eyeblink isoccasioned byrapid contraction of the orbicularisoculi muscle (see Figure 1). It occurs reflexively 30-50 ms afterthe onset of an abrupt acoustic stimulus. The primary charac-teristic of the eliciting stimulus is its rapid rise time (ideally,instantaneous), with intensity secondary. The blink reflexshows a regular course of habituation with repeated presenta-tion at short interstimulus intervals. However, it dishabituatesquickly and thus can be evoked repeatedly within a relativelybrief period (as many as 40-50 probe trials are practical in ahalf-hour experimental session). The response is variously re-cordedby photography; by using a potentiometer attached

with a thread to the eyelid; by the electro-oculogram, whereabrupt pen movements indicate the lid passing rapidly over thecorneal surface; or indeed, inadvertently by electroencephalo-gram, in whichthe recording of the reflex mayappear as a trou-bling artifact. The electromyographic measurement of orbicu-laris muscle during eyeblink is shown in Figure 1. This methodcaptures events most proximal to the neural path of innervationand is thus preferred by most investigators.

Context and Reflex EvocationThe reliability of the knee jerk as a neurological sign depends

on the bedside manner (as well as the motor skill) of the diag-nostician who delivers a percussive tap to the patellar tendon.This fact, that reflexes vary with the psychological context inwhich they are evoked, has long been practical knowledgeforhealth-careworkers and was a focus ofstudy for scientists beforethe turn of the century (Bowditch & Warren, 1890; Ison &Hoffman, 1983; Sechenov, 1863/1965). More recent researchon the startle reflex has contributed importantly to two majortopics in psychologythe study of attention and the study ofconditioned fear.Attention

Frances Graham and her associates have reported a series ofexperiments based on an innovative startle-probe methodology

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EMOTION, ATTENTION, AND STARTLE 379(e.g., Anthony&Graham, 1985; Graham, 1975, 1979). In thisresearch, various stimuli, tasks, and instructional manipula-tions are used to guide the subject's attentional focus. Whilethe subject is thus engaged,brief nonsignal startling stimuli arepresented, with the expectation that the eyeblink reflex will beenhanced or attenuated according to the amount of attentionalresources allocated to the primary task.

Several important phenomena have been shownin this work.For example, instructions to attend to the probe stimulus itselfprompt an augmentation of the reflex (e.g., Bohlin & Graham,1977; Hackley & Graham, 1984). Conversely, reflex attenua-tion results if unsignaled probes are presented in the foreperiodof a reaction time task. In this latter case, attention is not di-rected to the startle stimulusbut is presumably focused on theanticipated go signal. This probe reflex reduction is greatest,furthermore, when the go signal is imminent (and attention toit most needed), as corroborated by greater late-foreperiodheart rate decelerationa common measure of stimulus "ori-enting" (Graham & Clifton, 1966). These studies and relatedwork, aswell as an attentional theory of the startle probe, havebeen admirably reviewed by Anthony (1985).Of particular interest for this presentation are a group ofcross-modality experiments. In this procedure, the subject's at-tention is directed to either a visual or auditory foreground taskwhile startle probes are administered in either the same or thealternate sensory channel. The hypothesis examined is that at-tentional resources are limited and are allocated a priori ac-cording to modality. Thus, when subjects engagein a visual task(e.g., viewing pictures), resources available to the auditory sys-tem are reduced, and the reflex response to an acoustic startleprobe is expected to be attenuated. Results from Anthony andGraham's (1985) test of this view are presented in Figure 2.Both infants and adults show blink reflexes that are smaller andslower when the modality of the probe does not match the mo-dality offoreground stimulation.

A further aspect of this research concerns the interest valueof the foreground stimulus. Anthonyand Graham (1985)pro-posed that more interesting stimuli (e.g., slides of human faces,or music)engage attention to agreater extent than do less inter-esting stimuli (e.g., blank slides or single pure tones), and thuscross-modality probe response attenuation should be greaterwith interesting than with dull foregrounds. Again, both infantsand adults show this effect. Recently, Simonsand Zelson (1985)undertook a test ofthe hypothesis, using stimuli that were moreevocative of emotion. Subjects viewed two content classes ofphotographic slides as a foreground task: interesting content, avarying series ofattractive nudemen and women, and dull con-tent, a picture of a small wicker basket, repeatedly presented.Unpredictable auditory startle probes were presented duringboth slide presentations. As expected, the blink reflex wassig-nificantly smaller for interesting than for dull slide content.Fear Conditioning

Brown, Kalish, and Farber (1951) undertook a probe studyof classical fear conditioning, based on a very different theoryof startle modulation. The investigators noted that anxietypa-tients often show exaggerated startle responses. Presuming thiswasa function of a high drive state (Hull, 1943), they reasoned

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