3. E. F. Evans, in Neuronal Mechanisms ofHear-ing, J. Syka and L. Aitkin, Eds. (Plenum, NewYork, 1981), p. 69; M. B. Sachs and E. D.Young, J. Acoust. Soc. Am. 66, 470 (1979).

4. J. E. Rose, J. E. Hind, D. J. Anderson, J. F.Brugge, J. Neurophysiol. 34, 685 (1974); D. H.Johnson, thesis, Massachusetts Institute ofTechnology (1974); M. B. Sachs and E. D.Young, J. Acoust. Soc. Am. 68, 858 (1980).

5. E. Javel, J. Acoust. Soc. Am. 69, 1735 (1981).6. N. F. Viemeister, ibid. 56, 1594 (1974); B. C. J.

Moore and D. H. Raab, ibid. 57, 400 (1975).7. D. H. Johnson, Biophys. J. 22, 413 (1978).8. The final threshold for each subject was based

on the average of at least five separate thresholdestimates. The standard deviation of these esti-mates was typically less than 2 dB and rangedfrom 0.7 to 3.8 dB.

9. The cutoff frequencies were chosen such that atthe highest level of the band-reject masker, thebandpass noise was approximately 10 dB aboveits masked threshold for all subjects. The noiseswere produced by multiplying a lowpass and abandpass noise by a 10-kHz sinusoid and addinga 20-kHz highpass noise.

10. Audio Technica ATH-7 Electret headphoneswere used. Since no high-frequency calibrationstandard exists for these or any headphones, thespectrum levels reported are the 1-kHz equiva-lents measured with a flat plate coupler. Theoverall level is approximately 43 dB greater thanthe reported spectrum level; the highest levelsused in this experiment were in excess of 100-dBSPL overall.

11. M. H. Lurie, J. Acoust. Soc. Am. 11, 420 (1940);Y. Katsuki, N. Suga, Y. Kanno, ibid. 34, 1396(1962); N. Y.-S. Kiang, Ann. Otol. Rhinol. Lar-yngol. 77, 656 (1968).

12. M. C. Liberman, J. Acoust. Soc. Am. 63, 442(1978); Science 216, 1239 (1982).

13. A. R. Palmer and E. F. Evans, Exp. Brain Res.Suppl. II (1979), p. 19; Hear. Res. 7, 305 (1982).

14. This is the number of independent, optimally

combined Poisson channels that would yield athreshold equal to that observed in the band-reject condition. For a single channel the per-formance measure, di', is approximatelyAIdBr (I)[T/r(I)]'n, where T is the interval overwhich events (spikes) are counted, r(I) is themean firing rate at intensity I, r'(I) is the slope ofthe rate-intensity function at I, and AIdB is thedecibel difference between the two stimuli. Forn independent, optimally combined channelswith equal d',, the resulting overall performanceis d' = n"'2d',. Thus, n = [d'IAldFr'()12r(I)IT.[See J. P. Egan, Signal Detection Theory andROC Analysis (Academic Press, New York,1975), pp. 162-217, for an excellent treatment ofPoisson observers.] At No = 50 dB in the band-reject condition, AIdB = 4.8 for d' = 0.77. As-suming a fixed counting interval of 100 msec anda mean firing rate of 100 spikes per second atNo = 50 dB, then for slopes of five or two spikesper second per decibel, n is 1.03 or 6.4 fibers,respectively. These slopes are reasonable forrate-intensity functions obtained with broad-band noise at lower spectrum levels [T. B.Schalk and M. B. Sachs, J. Acoust. Soc. Am.67, 903 (1980)]. The assumption of optimumcombination requires, in effect, that saturatedchannels, those with d! = 0, be ignored. Wheth-er the auditory system actually achieves orapproximates optimum combination is not di-rectly relevant to the question of whether, at thelevel of primary fibers, a rate code is evenpossible.

15. I thank D. A. Burkhardt, W. D. Ward, M.Ruggero, and G. Wakefield for their commentson the manuscript. I also thank H. S. Colburnand W. M. Rabinowitz for stimulating discus-sions on this topic. This work was supported bygrant NS12125 from the National Institute ofNeurological and Communicative Disorders andStroke.

8 February 1983; revised 24 May 1983

Autonomic Nervous System ActivityDistinguishes Among Emotions

Abstract. Emotion-specific activity in the autonomic nervous system was generat-ed by constructing facial prototypes of emotion muscle by muscle and by relivingpast emotional experiences. The autonomic activity produced distinguished not onlybetween positive and negative emotions, but also among negative emotions. Thisfinding challenges emotion theories that have proposed autonomic activity to beundifferentiated or that have failed todifferentiation in emotion.

For almost a century scientists haveargued about whether or not activity inthe autonomic nervous system (ANS) isemotion-specific. Some of the most in-fluential cognitive theories of emotion (1,

address the implications of autonomic

2) presume undifferentiated autonomicarousal despite a number of reports ofemotion-specific autonomic activity (3-5). We now report evidence of suchspecificity in an experiment designed to

remedy methodological problems thathave lessened the impact of previousstudies: (i) A broad sample of six emo-tions was studied, rather than the two orthree that are typical. (ii) Verificationprocedures were instituted to maximizethe likelihood that each sample con-tained only the single target emotion andno other. (iii) A sufficiently broad sampleof autonomic measures was obtained toenable differentiation of multiple emo-tions, with appropriate statistical protec-tion against spurious findings due to mul-tiple dependent measures. (iv) Autonom-ic measures were taken from the onset ofemotion production continuously until itwas terminated. More typical measurestaken before and after production of anemotion may completely miss short-lived target emotions. (v) Multiple elicit-ing tasks were used with the same sub-jects. (vi) Professional actors (N = 12)and scientists who study the face(N = 4) served as subjects to minimizecontamination of emotion samples byextraneous affect associated with frus-tration or embarrassment.We studied six target emotions (sur-

prise, disgust, sadness, anger, fear, andhappiness) elicited by two tasks (direct-ed facial action and relived emotion),with emotion ordering counterbalancedwithin tasks. During both tasks, facialbehavior was recorded on videotape,and second-by-second averages were ob-tained for five physiological measures:(i) heart rate-measured with bipolarchest leads with Redux paste; (ii) left-and (iii) right-hand temperatures-mea-sured with thermistors taped to the pal-mar surface of the first phalanges of themiddle finger of each hand; (iv) skinresistance-measured with Ag-AgClelectrodes with Beckman paste attachedto the palmar surface of the middle pha-langes of the first and third fingers of thenondominant hand; and (v) forearm flex-or muscle tension-measured with Ag-

Fig. 1. Frames from the videotape of one of the actor's performance of the fear prototype instructions: (A) "raise your brows and pull themtogether," (B) "now raise your upper eyelids," (C) "now also stretch your lips horizontally, back toward your ears."

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AgCl electrodes with Redux paste andelectronic integration of the electromyo-gram.The directed facial action task com-

prised six trials; in each a nonemotionalexpression was performed and followedby an emotion-prototypic expression,that is, an expression that theory andevidence indicate universally signals oneof the target emotions (6). Subjects werenot asked to produce an emotionalexpression but instead were told precise-ly which muscles to contract (Fig. 1).Their attempts to follow these instruc-tions were aided by a mirror and coach-ing (by P.E.). The nonemotional expres-sion comprised two actions not includedin any of the emotional expressions tocontrol for ANS changes associated withmaking any facial movement. Expres-sions were held for 10 seconds. This taskresembles a traditional emotion posingtask (in which, for example, subjects areasked to look fearful), but improves on itby precisely specifying for the subject,and for the experimenter's subsequentverification, the exact set of musclemovements that is required. Video rec-ords offacial expressions were measured(7) to ensure that autonomic data wouldbe included in the analyses only if theinstructed set of actions had been made;86.5 percent of the data were used.

In the relived emotion task, subjectswere asked to experience each of the sixemotions (in counterbalanced orders) byreliving a past emotional experience for30 seconds. This task resembles tradi-tional imagery tasks, but more specifical-ly focuses on reliving a past emotionalexperience. After each trial, subjects rat-ed the intensity of any felt emotion on ascale from 0 to 8. Autonomic data wereused only when the relived emotion wasfelt at the midpoint of the scale or greaterand when no other emotion was reportedat a similar strength; 55.8 percent of thedata were used.Change scores were computed for

each emotion on each task (directed fa-cial action: averaged data during emo-tional face minus that during nonemo-tional face; relived emotion: averageddata during relived emotion minus thatduring the preceding 10-second rest peri-od). The experiment was analyzed in a 2by 2 by 6 (actors versus scientists by taskby emotion) multivariate analysis of vari-ance. Our hypothesis that there are auto-nomic differences among the six emo-tions was supported [emotion main ef-fect, F(25, 317) = 2.51, P < 0.001].There were differences in emotion-spe-cific autonomic patterns between thetwo eliciting tasks [task by emotion in-teraction, F(25, 62) = 2.0, P = 0.014].16 SEPTEMBER 1983

Skin High:High - temperature Anger

/ Low:Heart Fearrate Sad

Low:HappyDisgustSurprise

Fig. 2. Decision tree for discriminating emo-tions in direction facial action task.

The nature of the emotion-specificANS activity was explored with t-testswithin significant univariate effects. Twofindings were consistent across tasks: (i)Heart rate increased more in anger(mean calculated across tasks + stan-dard error, +8.0 ± 1.8 beats per minute)and fear (+8.0 ± 1.6 beats per minute)than in happiness (+2.6 ± 1.0 beats perminute). (ii) Left and right fingertemperatures increased more in anger(left, +0.100C ± 0.0090; right, +0.080C ±0.008°) than in happiness (left, -0.07°C +0.0020; right, -0.03°C ± 0.002°).

In addition to these differences be-tween the negative emotions of angerand fear and the positive emotion ofhappiness, there were important differ-ences among negative emotions. In the

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directed facial action task we were ableto distinguish three subgroups of emo-tions (Fig. 2) on the basis of heart rateand finger temperature differences (Fig.3). Additional differentiation in the re-lived emotions task enabled distinctionbetween sadness and other negativeemotions on the basis of significantlylarger decreases in skin resistance insadness [-12.6 ± 164.6 kilohm (8)] thanin the others (fear, -0.37 ± 1.0 kilohm;anger, -2.1 ± 3.7 kilohm; and disgust,+4.4 ± 6.6 kilohm).There were also three negative find-

ings of note. No significant differenceswere found between emotions on theforearm flexor measure, thus indicatingthat heart rate effects were not artifactsof fist clenching or other related muscleactivity. No statistically significant dif-ferences were found between actors andscientists studying facial expression, in-dicating that the findings generalized toboth of these populations. Finally, whenthe major analyses were rerun includingall ANS data without regard to whetherverification criteria were met, only thenegative versus positive emotional dis-tinctions remained; all distinctionsamong negative emotions were lost. Weinterpret this finding as supporting theimportance of verification of emotional

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Fig. 3. Changes in (A) heart rate and (B) right finger temperature during the directed facialaction task. Values are means + standard errors. For heart rate, the changes associated withanger, fear, and sadness were all significantly greater (P < 0.05) than those for happiness,surprise, and disgust. For finger temperature, the change associated with anger was significant-ly different (P < 0.05) from that for all other emotions.

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state and as indicating one reason previ-ous studies that failed to include verifica-tion procedures have been unable todistinguish so many negative emotions.Combining the results from the two

tasks, this experiment provides the firstevidence (to our knowledge) of autonom-ic differences among four negative emo-tions (disgust and anger distinguishedfrom each other and from fear or sadnessin the directed facial action task; sadnessdistinguished from disgust, anger, or fearin the relived emotion task) as well asshowing general distinctions betweenpositive and negative emotions in bothtasks. In addition to this new evidence,we replicated with the directed facialaction task the single most reliable find-ing from past studies: anger and fearshow similar heart rate increases butdiffer in peripheral vascular function (in-dicated by our finding of colder fingers infear than in anger). The magnitude ofthese heart rate increases, both mean(Fig. 3) and maximum (fear, +21.7; an-ger, +25.3 beats per minute) are compa-rable to other such findings (9).

Further research is needed to choosebetween two alternative explanations ofthe differences in the results we obtainedwith the two eliciting tasks: (i) the tasksinvolve different neural substrates,which generate different patterns ofemo-tion-specific autonomic activity; or (ii)the tasks differ in the extent of emotionblending they produce. Further work isalso needed to demonstrate that emo-tion-specific autonomic activity is notunique to actors and scientists, althoughthe possibility that training in either pro-fession would have such a profound ef-fect on autonomic patterning in emotionseems unlikely.Our finding of emotion-differentiated

autonomic activity, albeit important in

its own right, begets the question of howthat activity was generated. Particularlyintriguing is our discovery that produc-ing the emotion-prototypic patterns offacial muscle action resulted in autonom-ic changes of large magnitude that weremore clear-cut than those produced byreliving emotions (a more naturalisticprocess). With this experiment we can-not rule out the possibility that knowl-edge of the emotion labels derived fromthe facial movement instructions or see-ing one's own or the coach's face wasdirectly or indirectly responsible for theeffect. We find this unlikely since itwould indicate either (i) that just viewingan emotional face directly producedautonomic patterning or (ii) that subjectsinferred the "correct" set of autonomicchanges from the label and then some-how produced these complex patterns.The biofeedback literature (10) suggeststhat people cannot voluntarily producesuch complex patterns of autonomic ac-tivity.We propose instead that it was con-

tracting the facial muscles into the uni-versal emotion signals which broughtforth the emotion-specific autonomic ac-tivity. This might occur either throughperipheral feedback from making the fa-cial movements, or by a direct connec-tion between the motor cortex and hypo-thalamus that translates between emo-tion-prototypic expression in the faceand emotion-specific patterning in theANS. Although further studies are need-ed to verify this hypothesis and to deter-mine the pathways involved, the factthat emotion-specific autonomic activityoccurred is of fundamental theoreticalimportance, no matter what the underly-ing mechanisms may turn out to be. Itraises the question of how such complexpatterns of autonomic activity relate to

changes in the central nervous system,cognitive processes, motor behaviors,and the subjective experience of emo-tion; it also underscores the centrality ofthe face in emotion as Darwin (11) andTomkins (12) suggested.

PAUL EKMANROBERT W. LEVENSON*WALLACE V. FRIESEN

Department of Psychiatry,University of California School ofMedicine, San Francisco 94143

References and Notes

1. S. Schachter and J. E. Singer, Psychol. Rev. 69,379 (1962).

2. G. Mandler, Mind and Emotion (Wiley, NewYork, 1975).

3. A. F. Ax, Psychosom. Med. 15, 433 (1953).4. D. H. Funkenstein, S. H. King, M. Drolette.

ibid. 16, 404 (1954); R. A. Sternbach, J. Psycho-som. Res. 6, 87 (1962).

5. R. J. Roberts and T. C. Weerts, Psychol. Rep.50, 219 (1982).

6. P. Ekman and H. Oster, Annu. Rev. Psychol.30, 527 (1979).

7. P. Ekman and W. V. Friesen, The Facial ActionCoding System (Consulting Psychologists Press,Palo Alto, Calif., 1978). To avoid directly sug-gesting emotion labels, we did not obtain emo-tion ratings, relying instead on facial measure-ment for verification in this task.

8. This large value reflects the influence of oneoutlying subject.

9. Distinctions between fear and anger were basedon changes in heart rate and diastolic bloodpressure and on the magnitude of heart ratechange (3, 5). Increases were also comparable toheart rate change in Schachter and Singer's (1)anger-epinephrine condition.

10. G. E. Schwartz [Science 175, 90 (1972)] reportedone of the few instances in which biofeedbackproduced complex patterns of two ANS func-tions-heart rate and blood pressure. There area few reports of different patterns of one auto-nomic and one somatic function (for example,heart rate and respiration rate) [D. Newlin andR. Levenson, Biol. Psychol. 7, 277 (1978)].

11. C. Darwin, The Expression of the Emotions inMan and Animals (Univ. of Chicago Press,Chicago, 1965).

12. S. S. Tomkins, Affect, Imagery, and Conscious-ness (Springer, New York, 1962).

13. We thank E. Callaway, R. Lazarus, P. Tannen-baum, and S. Tomkins for their comments onthis report; the John D. and Catherine T. Mac-Arthur Foundation for research funding; and L.Temoshok, J. Kamiya, and L. Zegans for theuse of equipment.

* Present address: Department of Psychology,Indiana University, Bloomington 47405.

3 May 1983

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Autonomic nervous system activity distinguishes among emotionsP Ekman, RW Levenson and WV Friesen

DOI: 10.1126/science.6612338 (4616), 1208-1210.221Science 

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