Rdwenes ad Nos

1. V. V. Zhelkznyakov, Sov. Astron. AJ 6, 3(1962); T. Kakinuma and G. Swarup, Astrophys.J. 136, 975 (1962); M. R. Kundu, Solar RadioAstronomy (Interscience, New York, 1965); P.Lantos, Ann. Astrophys. 31, 101 (1968); E. Ya.Zlotnik, Sov. Astron. AJ 12, 245 (1968); ibid., p.464; V. V. Zheleznyakov, Radio Emissionfromthe Sun and Planets (Pergamon, New York,1970); A. Kruger, Introduction to Solar RadioAstronomy and Radio Physics (Reidel, Boston,1979).

2. 1. A. Ratcliffe, The Magneto-Ionic Theory(Cambridge Univ. Press, Cambridge, 1962); K.R. Lang, Astrophysical Formulae (Springer,New York, 1974, 1980).

3. M. R. Kundu and C. E. Alissandrakis, Nature(London) 257, 465 (1975); , J. D. Breg-man, A. C. Hin, Astrophys. J. 213, 278 (1977;K. R. Lang and R. F. Willson, Nature (London)278, 24 (1979); in Radio Physics of the Sun(international Astronomical Union Symposium86), M. R. Kundu and T. E. Gergely, Eds.(Reidel, Dordrecht, 1980), p. 109; M. R. Kundu,E. J. Schmahl, M. Gerassimenko, Astron. As-trophys. 82, 265 (1980); M. Felli, K. R. Lang, R.F. Willson, Astrophys. J. 247, 325 (1981); R.Pallavacini, T. Sakurai, G. S. Vaiana, Astron.Astrophys. 98, 316 (1981).

4. M. R. Kundu, T. Velusamy, R. H. Becker, Sol.Phys. 34, 217 (1974); K. R. Lang, ibid. 36, 351(1974); C. E. Alissandrakis and M. R. Kundu,Astrophys. J. 222, 342 (1978); M. R. Kundu, inRadio Physics of the Sun (International Astro-nomical Union Symposium 86), M. R. Kunduand T. E. Gergely, Eds. (Reidel, Dordrecht,1980), p. 157; K. Marsh, G. J. Hurford, H. Zirin,ibid., p. 191; K. R. Lang, R. F. Willson, M.Felli, Astrophys. J. 247, 338 (1981).

5. K. A. Marsh and G. J. Hurford, Astrophys. J.240, LIIl (1980).

6. , Annu. Rev. Astron. Astrophys. 20, 497(1982); M. R. Kundu, Rep. Prog. Phys. 45, 1435(1982); _ and L. Vlahos, Space Sci. Rev.32, 405 (1982).

7. E. B. Fomalont, Proc. Inst. Elec. Eng. 61, 1211(1973).

8. K. R. Lang and R. F. Willson, in Advances inSpace Research-Proceedings ofthe 24th Meet-ing ofCOSPAR (Pergamon, London, 1983), vol.I P. 91; __ , V. Gai7auskas, Astrophes. J.26,455 (1983); R. K. Shevgaonkar andI. R.Kundu, ibid. 283, 413 (1984).

9. G. B. Gel'freikh and B. I. Lubyshev, Sov.Astron. AJ 23, 316 (1979); C. E. Alissandrakis,

M. R. Kundu, P. Lantos, Astron. Astrophys. 82,30 (1980); C. E. Alissandrakisand M. R. Kundu,Astrophys. J. 253, L49 (1982); K. R. Lang andR. F. Wilson, ibid. 255, LIII (1982).

10. M. R. Kundu and T. Velusamy, Astrophys. J.240, L63 (1980); T. Velusamy and M. R. Kundu,ibid. 243, L103 (1981); K. R. Lang, R. F. Wll-son, J. Rayrole, ibid. 258, 384 (1982); G. A. Dulkand D. E. Gary, Astron. Astrophys. 124, 103(1983); K. R. I ang and R. F. Willson, ibid. 127,135 (1983); D. McConnell and M. R. Kundu,Astrophys. J. 269, 698 (1983).

11. D. Rust, Sol. Phys. 47, 21(1976); M. R. Kunduet al., Astron. Astrophys. 108, 188 (1982); R. F.Willson, Sol. Phys. 83, 285 (1983); K. R. Langand R. F. Wilson, in Advances in Space Re-search-Proceedings of the 24th Meeting ofCOSPAR (Pergamon, London, 1983), vol. 2, p.91; M. R. Kundu, Proc. Int. Astron. UnionSymp. 107 (1984), p. 185.

12. T. Gold and F. Hoyle, Mon. Not. R. Astron.Soc. 120, 89 (1960); J. Heyvaerts, E. R. Priest,D. M. Rust, Astrophys. J. 216, 123 (1977); D. S.Spicer, Sol. Phys. 53, 305 (1977); S. 1. Syrovats-kii and V. D. Kuznetsov, in Radio Physics oftheSun (International Astronomical Union Sympo-sium 86), M. R. Kundu and T. E. Gergely, Eds.(Reidel, Dordrecht, 1980), p. 445; V. D. Kuznet-sov and S. I. Syrovatskii, Sol. Phys. 69, 361(1981); D. S. Spicer, ibid. 70, 149 (1981); V.Petrosian, Astrophys. J. 255, L85 (1982); B. V.Somov and S. I. Syrovatskii, Sol. Phys. 75, 237(1982); E. R. Priest, ibid. 86, 33 (1983).

13. K. R. Lang, Sol. Phys. 52, 63 (1977); M. R.Kundu, in Radio Physics of the Sun (Interna-tional Astronomical Union Symposium 86), M.R. Kundu and T. E. Gergely, Eds. (Reidel,Dordrecht, 1980), p. 157; G. Hurford and H.Zirin, Air Force Geophys. Lab. Rep. AFGL-TR-82-0017 (1982); R. K. Shevgaonkar and M. R.Kundu, Astrophys. J., in press; K. R. Lang andR. F. Willson, Advances in Space Research-Proceedings of the 25th Meeting of COSPAR(Pergamon, London, in press).

14. M. R. Kundu, E. J. Schmahl, T. Velusamy,Astrophys, J. 253, 963 (1982); , L. Vla-hos, Astron. Astrophys. 108, 188 (1982); T.Velusamy and M. R. Kundu, Astrophys. J. 258,388 (1982); M. R. Kundu, Sol. Phys. 86, 205(1983); M. R. Kundu, in Advances in SpaceResearch-Proceedings of the 24th Meeting ofCOSPAR (Pergamon, London, 1983), vol. 1, p.159; M. R. Kundu, D. M. Rust, M. Bobrowsky,Astrophys. J. 265, 1084 (1983); R. F. Willsonand K. R. Lang, Astrophys. J. 279, 427 (1984);R. F. Willson, Sol. Phys. 92, 189 (1984).

15. M. R. Kundu, V. Gaizauskas, B. Woodgte, E.J. Schmal, R. Shine, H. Jones, Astrophys. J.SuppI. Ser., in press.

16. M. R. Kundu, Proc. Int. Astron. Union Symp.107 (1984), p. 185.

17. J. C. Brown, D. B. Melrose, D. S. Spicer,Astrophks. J. 228, S92 (1979); D. F. Smith andC. G. Lllliquist, ibid. 232, 582 (1979); L. Vlahosand K. Papadopoulos, ibid. 233, 717 (1979); G.D. Holman, M. R. Kundu, K. Papadopoulos,ibid. 257, 354 (1984).

18. D. E. Gary and J. L. Linsky, ibid. 250, 284(1981); K. Topka and K. A. Marsh, ibid. 254,641 (1982); J. L. Linsky and D. E. Gary, ibid.274, 776 (1983).

19. D. E. Gary, J. L. Linsky, G. A. Dulk, ibid. 263,L79 (1982); D. B. Melrose and G. A. Dulk, ibid.259, 844 (1982); K. R. Lang, J. Bookbinder, L.Golub, M. M. Davis, ibid. 272, L1S (1983).

20. C. Slottje, Nature (London) 275, 520 (1978); inRadio Physics of the Sun (International Astro-nomical Union Symposium 86), M. R. Kunduand T. E. Gergely, Eds. (Reidel, Dordrecht,1980), p. 195; R. Zhao and S. Jin, Sci. Sin. A 25,422 (1982).

21. G. D. Holman, D. S. Eichler, M. R. Kundu, inRadio Physics of the Sun (International Astro-nomical Union Symposium 86), M. R. Kunduand T. E. Gergely, Eds. (Reidel, Dordrecht,1980), p. 457; G. D. Holman, Adv. Space Res. 2,181 (1982); R. R. Sharma, L. Vlahos, K. Papa-dopoulos, Astron. Astrophys. 112, 337(1982); L.Vlahos, R. R. Sharma, K. Papadopoulos, As-trophys. J. 275, 374 (1983).

22. Adapted from (5), plate 2.23. This review would have been impossible with-

out the fine contributions to solar radio astrono-my made by R. F. Willson at Tufts Universityand C. E. Alissandrakis, E. J. Schmahl, T.Velusamy, and L. Vlahos while working for theUniversity of Maryland. Radio astronomicalstudies of the sun and other active stars at TuftsUniversity are supported under Air Force Officeof Scientific Research grant AFOSR-83-0019-B.Investigations of flare stars at Tufts Universityare also supported by NASA grant NAG 5477;whereas comparisons of VLA and Solar Maxi-mum Mission satellite data are supported byNASA Guest Investigator grant NAG 5-501.Solar research in the Astronomy Program at theUniversity of Maryland is supported under NSFgrant ATM 84-15388, NASA grant NGR 21-002-199, and NASA contract NSG 5320. The VeryLarge Array is operated by Associated Univer-sities Inc., under contract with the NationalScience Foundation.

Nearly 80 years ago a book appearedin Paris under the title Physionomie Hu-maine: Son Mecanisme et son Role So-cial (1). The book, written by IsraelWaynbaum, a physician, offered a radi-cal theory of emotional expression, defy-ing all previous ones, including Darwin'sdominant theory. It clarified, for the firsttime, the function of emotional expres-sion in the emotional process-the fore-most problem in the study of emotions atthe turn ofthe century. Yet Waynbaum'sbook received no attention and it has5 APRIL 198S5

remained unknown until now. Neitherthe author nor his idea are to be found inthe Science Citation Index or in numer-ous reviews of research on emotion orfacial expression. In this article I reviewWaynbaum's theory, compare it withDarwin's, bring it up to date, and showthat it forms a promising basis for acomprehensive theory of the emotions.Waynbaum's analysis led him first to

question the term "emotional expres-sion." He feared that referring to facialmovements as "expressions," the stan-

dard term since Aristotle, reinforced byDarwin's classic work (2), implicitlyfixed their role in the emotional process,and "solved" the problem by definition.The term "expression" specifies a priorithe causal sequence among emotionalcorrelates, placing the efferent process atthe terminus. As such, therefore," expression" cannot be the cause of anyother aspect of the emotional process.The term "expression" also implies theexistence of an antecedent internal statewhich "expression" externalizes, mani-fests, and displays. It implies further thatthe antecedent internal state seeks exter-nalization that forces itself onto the sur-face. Hence, there also exists the term"suppression." In many cases the be-havioral output may well "express" aninternal state, and some reactions areindeed suppressed. But it is by no meansestablished that all facial gestures thatare classified as expressions are causedby internal subjective states. It may be

The author is a professor of psychology at theUniversity of Michigan, Ann Arbor 48104.

15

Emotion and Facial Efference:A Theory Reclaimed

R. B. Zajonc

best, therefore, to refer to these phenom-ena as "emotional efference"-a termthat has fewer a priori implications. Ofcourse, the term "expression" is con-sistent with all current theories of emo-tion; only Lange and James (3) ques-tioned the assumption that feeling pre-cedes efference, but they failed to pro-vide an explanatory and conceptualframework, and their argument was soon

vascular processes, Waynbaum pro-posed that the musculature of the face iscapable of compressing veins and arter-ies of the face and thus controlling facialblood flow, which he thought could actas a safety valve for CBF. Blood circula-tion was also implicated in the actions ofthe diaphragm that arise in sobbing orlaughing, or in tears shed when weepingor laughing. Waynbaum did not take

Summary. A theory of emotional expression, ignored since 1906, holds that facialmuscles act as ligatures on facial blood vessels and thereby regulate cerebral bloodflow, which, in turn, influences subjective feeling. The theory, developed by IsraelWaynbaum, a French physician, hypothesizes the subjective experence of emotionsas following facial expression rather than preceding it. It answers Darwin's question ofwhy different muscles contract or relax in different emotions better than Darwin's owntheory. When restated in terms of contemporary neurophysiological knowledge, itexplains and organizes several ill-understood emotional processes and phenomena.

rejected. Waynbaum's first contributionwas to question these 19th-centuryviews-views that still dominate currentthinking about emotion.According to Andrew (4, p. 1034),

facial expression has evolved "to com-

municate information about the probablefuture behavior of the displaying ani-mal." By expressing its emotions, one

animal could signal its intentions to an-

other. But why should humans, whohave such a powerful means of commu-nication-language-be the one animalto have also developed the most complexrepertoire of facial movements? Do we

need, in addition to speech, some 80facial muscles merely to broadcast ourintentions?Moreover, why should we project our

intentions on our faces in the first place?It is perhaps reasonable to suppose thatbaring teeth and growling in rage mightcause an intruder to retreat, and thusprevent violence. But what purposemight be served by displaying one's ownfear to an enemy, or one's own surpriseto an intruder? No doubt some evolu-tionary explanations might be suggested,but such explanations depend on conjec-ture, and it is difficult to imagine theevolutionary process whereby theycould have become universal. Hardlyany theory of emotion and facial expres-sion challenges or even questions thiscritical aspect of Darwin's theory.

In contrast to all contemporary theo-ries of emotion, Waynbaum offered thehypothesis that emotional responseshave as their principal function the auxil-iary control of cerebral blood flow(CBF). Noting that all overt emotionalresponses (blushing, sobbing, weeping,frowning, and so forth) are closely tied to

16

issue with the display function of facialmovements, but he considered this func-tion to be derivative and incapable ofexplaining them.To fully appreciate Waynbaum's con-

tribution, however, one must put it in thecontext of Darwin's work.Darwin's theory of emotional expres-

sion. To explain emotional expression,Darwin wrote, one must understand"'why different muscles are brought intoaction under different emotions; why, forinstance, the inner ends of the eyebrowsare raised, and the corners of the mouthdepressed, by a person suffering fromgrief or anxiety" (2, p. 3). However,Darwin's theory of emotional expressiondoes not begin to answer his own ques-tion.Darwin seems, by his empirical meth-

od, to have been less interested in expli-cating emotional expressions than in us-

ing these phenomena to substantiate theevolutionary hypothesis for behavior as

he did for structure. He did not seek tospecify the ongoing process of emotionalexpressions, nor to understand theirmechanisms. Instead, he solicited obser-vations about emotions from remoteparts of the world to establish the univer-sality of expressions. His book closeswith the assertion that his "theory ofexpression confirms to a certain limitedextent the conclusion that man is derivedfrom some lower animal form" (2, p.

365). Most subsequent research on emo-

tions has followed Darwin's interest inuniversality and taxonomy (5). This re-

search supports the hypothesis of theinnate basis of expression, but it doesnot address Darwin's "why" question.Darwin's theory consists of three prin-

ciples. The first-that of serviceable

habits-holds that some actions relievethe organisms's wants, gratify its needsand desires, and guide it in reacting tosensations and to internal states. Theseserviceable actions will be repeated byforce of habit, especially when they havedone so "during a long series of genera-tions" (2, 6). The second principle holdsthat for many actions there exist anti-thetical actions elicited by the oppositestimulus conditions. Darwin gives theexample of a dog mistaking a familiarperson for a stranger, and upon discov-ery of its error changing from a threaten-ing posture to the antithetical posture ofsubmission and affection. The third prin-ciple-that of the direct action of thenervous system-concerns behavior thatoccurs independently "of the Will, andindependently to a certain extent of Hab-it" (2). Tears, trembling, rage, andchanges in heart rate are such directproducts of the nervous system.Thus, Darwin's three basic principles

are a heuristic schema that directs theresearcher interested in knowing "whydifferent muscles are brought into actionunder different emotions" to conjure upany reasonable function that the givenexpression could have played at somepoint of evolution. If such a functioncannot be hypothesized, then the re-searcher must look for a function of anopposite expression. If both fail, then theexpression must be elicited by the directaction of the nervous system. But we arenot told by Darwin how or where to lookfor these functions, and it is not obviouswhat are "opposite" actions. Thus, thebaring of teeth is viewed as a threatsignal, even though teeth are also dis-played in the grin (4). Therefore, Dar-win's principles cannot be falsified. Dar-win revolutionized the thinking on emo-tional expression by placing it in thecontext of adaptive processes, and hewas an outstanding observer whoamassed a wealth of data. But it wouldbe false to credit him with a generaltheory of emotional expression.Waynbaum's vascular theory of emo-

tional expression. In contrast to Darwin,Waynbaum refused to view muscularmovements as the terminal stage of theemotional process. He attributed to thema much more significant internal regula-tory role. Waynbaum's thinking wasbased on a number of converging facts.(i) The supply of blood to the brain andto the face derives from one source, thecommon carotid artery. (ii) The supplyof cerebral blood must be stable. Therecan be no sudden changes even if the restof the circulatory system undergoes vio-lent variations. (iii) Although the bony

SCIENCE, VOL. 228

structure of the face is mostly rigid, theface has an inordinate number of mus-

cles. Why? (iv) The facial artery, a majorbranch of the external carotid, is rich inmuscular tissue. Again, why?Waynbaum argued that all emotional

reactions produce circulatory perturba-tions. Either they mobilize considerableenergy, or, as in depression, they re-

move energy demands. They may thusproduce a disequilibrium in CBF. Sincethe external and internal carotid have a

common origin, equilibrium in the CBFcan be maintained by directing more

blood to the face and skull or by divert-ing it toward the brain.Because facial muscles, when con-

tracting, push against the bony structure,they can act as tourniquets on arteriesand veins and thus regulate facial bloodflow. By modulating flow in the externalcarotid and in the facial veins, they regu-late CBF, reducing or complementing it.The same is true of other expressiveacts, such as those controlled by glandu-lar secretion or the diaphragm. For ex-

ample, the lachrymal gland is suppliedby the lachrymal artery which branchesoff from the internal carotid by way ofthe ophthalmic artery. Therefore, an

augmented blood flow in the lachrymalartery should reduce the flow in theinternal carotid, decreasing CBF, andhence causing momentary anesthesia ofthe corresponding regions of the nervous

system.If Waynbaum's theory is correct, it

can answer Darwin's "why" questionmore directly than the evolutionary the-ory of expression. Why are smiling andlaughing the major gestures of happinessand joy? Waynbaum asserted that mod-erate brain hyperemia is associated withhealthy and positive affective tonus,whereas the opposite-temporary brainanemia or ischemia-is associated withnegative affect, depressive moods, andunsound physical condition. But he alsoasserted that the subjective experienceof elation follows the smile, not the otherway around. The laughing person ap-

proaches a state of congestion. A hardlaugh makes the face quite red, andsometimes even violet. The return circu-lation is impeded by the contracted cer-vical skin muscles that press on thejugular veins. Thus, more blood remainsin the brain. The function of tears thatare often shed during hard laughter is torelieve the rising pressure of cerebralblood. These tears always come at thevery end of a laughing bout, and as in

crying they lead to a local anesthesia.Why is the zygomatic muscle involved

in smiling and in happiness? The con-

traction of the major zygomatic muscle,5 APRIL 1985

Israel Waynbaum

asserted Waynbaum, has a congestivecerebral circulatory function. The proofis simple. Pull the corners of your mouthapart by contracting the major zygomaticmuscle, as if in intense exaggeratedsmile. After several seconds, the frontalvein will be gorged with blood. Thus,claims Waynbaum, the zygomatic mus-

cle acts as a ligature on the branches ofthe external carotid and the slave actionof the corrugator blocks the returnblood. Cerebral blood is thus momentari-ly retained causing temporary intracere-bral hyperemia, which in turn leads to a

surge of subjectively felt positive effect.Waynbaum offered the opinion that,

given its beneficial circulatory effects,laughing must be healthy. It is like takingan oxygen bath. The cells and tissuesreceive an increased supply of oxygen,

causing a feeling of exuberance. Theconversion of venous blood into arterialblood is accelerated and, because of thespasmodic action of the diaphragm, thelungs oxygenate at a more rapid pace. Incontrast, sadness produces disoxygena-tion of tissues and attenuates vital pro-cesses. Happiness leaves the face youngbecause it involves only one major mus-

cle-the zygomatic. In sadness, manymuscles are contracted: the elevators,orbicularis oculi, orbicularis oris, corru-gator, frontalis, pyramidal, and others.Hence, frequent crying results in a pre-maturely wrinkled face.Why do we furrow our forehead when

we concentrate? The frontalis contractsand the forehead becomes furrowed bytransverse wrinkles. The eyeball is swol-len and pupils dilated. The eyes are oftenclosed, and the orbicularis oris as well as

the masseter are contracted to make the

jawbone project forward. By putting atourniquet on the external carotid and onfacial veins, all these actions, at the costof facial circulation, send more blood tothe brain. More cerebral blood meansbetter brain work. After 60 years, thishypothesis received empirical support(7). A host of other mannerisms, univer-sal in all cultures, are recognized asrevealing internal mental states, such asthinking, problem-solving, trying to re-member, or making decisions. There arerubbing one's chin, scratching one'shead, licking lips, pressing one's ocularregion, passing the hand over the fore-head, frowning, biting fingernails or pen-cils, and pulling one's earlobes or eye-brows. If facial musculature can to someextent control CBF, we would have anexplanation for phenomena that seemotherwise bizarre and for which no ex-planation has thus far been offered.While these efferents are peripheral tothe emotional process, they show thepervasive role of the vascular system inmental phenomena.

Had Waynbaum Worked Today

Waynbaum developed his theory near-ly 80 years ago, and he necessarily madesome assumptions now known to befalse. Had Waynbaum worked in a mod-ern laboratory he would have known, forexample, that the blood supply to thebrain does not derive from a singlesource but that it is distributed throughthe circle of Willis, which is supplied bya large network of vessels, and that theinterdependence between the internaland facial flow is much more limited thanhe suspected. He would also haveknown that neural circulatory controls,the profusion of arteries and veins, andthe presence of resistance beds create aredundancy in blood supply that cankeep CBF constant in a variety of ways,in spite of various muscular acts. Butmuscle action could be more significantwith respect to return circulation be-cause veins are more readily controlledby muscles. (Hence one notes the gorgedfrontal veins when straining excessivelyor when in rage.) Because blood from thebrain drains through the forehead andface, the muscular action in the face canbriefly delay the outflow of blood fromthe brain. Thus, Waynbaum might havefocused more on the influence of mus-cles on veins than on arterial flow, espe-cially since arteries abound in neuralcirculatory controls (vasoconstrictorsand vasodilators), while veins do not.This new knowledge about the vascularsystem, nevertheless, does not preolude

17

Waynbaum's basic hypothesis. The sta-bility of CBF, being of crucial impor-tance, may well be maintained by partial-ly redundant systems. Alterations inCBF that are under different time con-straints may be controlled by more thanone mechanism. Facial action also has adirect effect on CBF. CBF suppliesblood to those regions that are active,and those areas of the motor cortex thatcorrespond to a particular group of facialmuscles that are activated receive in-creased flow. Thus CBF can be regulat-ed by facial musculature, but not neces-sarily through facial blood flow.Had Waynbaum worked today, he

would not have suspected CBF changesto be the direct antecedents of mood andemotional effects. Rather, he may havedrawn a connection between emotionand brain temperature. Before enteringthe brain, the internal carotid passesthrough the cavernous sinus. One func-tion of this structure, the only one in thebody in which the artery is located insidea vein, is thermoregulation of arterialblood before it enters the brain. In desertungulates such as the camel, for exam-ple, the internal artery is divided intonumerous small vessels, creating a radia-tor pattern. The brain, which in the rest-ing adult organism produces one-fifth ofthe body's heat, is cooled by arterialblood (8).Temperature is important because it is

likely to influence the biochemical actionof neurotransmitters and enzymaticpathways. Thus a particular pattern ofregional blood flow, together with localrise and fall of brain temperature, mightenhance or impair the release and syn-thesis of different neurotransmitters andthereby produce different subjectivelyfelt states. These subjective states aredistinctive because different emotionalmuscular patterns can alter temperaturein different brain regions in differentways. Not only different brain regionsand different temperatures may be pro-duced by different muscular patterns,but different quantities of neurotransmit-ters (serotonin, enkephalin, and so forth)may be synthesized and released selec-tively.

Variations in the external flow causecorresponding complementary varia-tions in the internal flow (9), effectsachieved by direct ligatures on the exter-nal carotid. It has not been shown thatfacial musculature, by action on externalflow, can affect CBF. If it can, the effectis likely to be limited. Nevertheless,Waynbaum's hypothesis of facial effer-ence having subjective pleasurable con-sequences by affecting CBF, might be

18

true for reasons that he could not havesuspected. For if facial action instigateslocalized regional CBF, not by peripher-al but central processes, and if there areconcomitant effects on venous flow, theobtained temperature change may act onthe release and synthesis of neurotrans-mitters (10).

Migraine headaches are caused by avascular dysfunction, migraine sufferersmake a variety of unusual mouth move-ments, such as licking lips and biting theinside of their cheeks, and the externalcarotid flow rises during headache (11).These previously ignored facial move-ments may therefore play some role inreducing external vasodilation.Although Waynbaum was right in

many ways, his theory was necessarilyincomplete because he lacked knowl-edge that became available only decadeslater. He constructed his theory piece bypiece, creating a coherent and elegantstructure of assumed processes, aboutwhich he could no more than make intel-ligent guesses. Waynbaum's theory is aproduct of a superior imagination thatconceptualized the nature of emotionalprocesses almost entirely by the force oflogical necessity, for Waynbaum had nospecial training other than in medicineand never did research in a laboratory.

Tests of the vascular theory of expres-sion. The vascular theory answers Dar-win's "why" question of emotionalexpression directly and it is directly falsi-fiable. Modern methods of measuringblood flow, for example after xenon-133is inhaled (12), or thermography can beapplied to determine whether emotionalexpressions influence blood flow andCBF. It can now also be determinedwhether changes in CBF and brain tem-perature have the effects on emotion andmood that Waynbaum hypothesized.Many hypertensive drugs that producesignificant circulatory changes oftenhave serious depressive side effects, andprofound mood changes are associatedwith cerebral vascular disease and withstroke (13).The stability of CBF, suspected by

Waynbaum nearly 80 years ago, has alsobeen demonstrated. Globus et al. (14)found increases in heart rate, breathing,and blood pressure during heavy 10-minute exercise, yet there was no changein CBF over the same time interval.These findings need not contradict thevascular theory because different mea-sures of time are probably involved. Thesort of stability found in CBF by Globuset al. is obtained by comparing intervalsof several minutes. Therefore, these datacould conceal local changes in CBF that

occur within seconds and dissipate rap-idly. Little is known today about theeffects of brain temperature on the re-lease of neurotransmitters, although itwould be surprising if the optimum tem-perature for their synthesis and releasewere not confined to a narrow range,perhaps a fraction of a degree.

Toward an IntegratedTheory of Emotional Expression

Waynbaum's most significant contri-bution was to examine the role of facialmovements apart from their expressiveconsequences. His analysis providessome answers to the controversial prob-lem raised by Lange and James (3) aboutthe relative positions of muscular outputand subjective feeling in the causal struc-ture of the emotional process. BothWaynbaum and Lange however, beggedthe question of what causes bodily emo-tional movements in the first place. Theantecedents of facial muscular move-ments, glandular secretions, arrestedbreathing, or diaphragmatic spasms arenumerous.

1) Since several of these actions can beproduced at will, whatever moves a per-son to perform them-desire to please orfrighten another individual, craving foraffection, need for help, playful imita-tion, caprice-is a candidate for an ante-cedent condition for what might be per-ceived as "emotional expression."These voluntary acts can be performedeven though no emotion or an emotionother than the one displayed is experi-enced by the individual.

2) Among the involuntary antecedentsare fixed action patterns-instinctual re-actions that occur spontaneously, suchas fear reactions to strangers, withdraw-al of an injured limb, or retreat from arapidly looming object.

3) Expressive movements might beelicited as conditioned responses thathave been acquired in the past. A dogthat withdraws its leg in response to ashock that had been preceded by a bellcomes to withdraw the leg on hearing thebell alone.

4) Expressive acts can arise in mimic-ry either as instinctive reactions or asresponses established by previous rein-forcement. For example, if a child'ssmile is a response to the father's smileand the child, as a result, receives affec-tion, the child's likelihood of returningsmiles (and other expressions) is height-ened.

5) A class of antecedent conditions foremotional bodily movements derives

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from the organisms's orienting reactions.The theories of Piderit and of Gratiolet(15) specified these conditions. Accord-ing to Piderit, emotional expressions de-rive from the sensory and peripheralactivity elicited by emotional stimuli andfrom the hedonic reactions to these stim-uli. Piderit assumed that sensory eventsgive rise not only to peripheral orientingmuscular acts but also to consequentacts that are occasioned by their hedoniceffects. Orienting acts, such as squinting,drawing up one's nostrils, or lickingone's lips, optimize sensory receptivity.The consequent reactions, however, de-pend on the hedonic nature of the stimu-lation. When a bitter solution is placed inthe mouth, a person tends to make expel-ling motions. Piderit thus assumed thatsome sensory events are in themselvespleasurable, and so are the representa-tions that derive from these events.These pleasurable events evoke ap-proaching and accepting actions. Sensa-tions and representations that are dis-agreeable evoke rejecting actions.

Muscular reactions can occur not onlyto sensory events but to the memories ofthese events, to imaginary events, and,through generalization, to emotional ex-citation. When we imagine biting into alemon, we may form a rejecting buccalmotion, and similar facial gestures ex-press disdain for a silly idea. Gratioletnoted that bowlers contort their bodiesto "correct" the paths of their bowlingballs. We smile in joy because, by gener-alization, the mouth makes movementsthat are homologous to those when theindividual tastes a savory morsel. Lan-guage is replete with sensation-emotionmetaphors. We speak of "bitter ene-mies," "dark thoughts," and the "painof separation." And there are "honey,""sweetie," "6sugar," "tootsie," "but-tercup," among endearments whose ety-mology lies in gustatory pleasures.Whatever the antecedents of these fa-

cial and bodily movements, they arecritical for Waynbaum in affecting CBFand thereby changing the affective tonusand subjective hedonic experience of theindividual. A subjective state might existimmediately before what came to beknown as expressive movements, orthese movements could also be executedautomatically and without a prior subjec-tively felt experience. And if Waynbaumis correct, there is necessarily one after-ward. For the most part, for example,the onset of withdrawal and alarm reac-

gests that tears may act to relieve pain.The entire emotional process can there-fore be conceptualized as being triggeredby an internal sensory or cognitive eventthat leads to peripheral muscular, glan-dular, or vascular action that in turnresults in a change of the subjectivehedonic tone.

In this sense, the facial movementsassociated with emotion are no differentfrom sneezing, coughing, and yawning.The universality of emotional expressionis therefore no more surprising than theuniversality of yawning and sneezing.All have clear biological bases and canbe ascribed to corresponding neuroana-tomical structures and neurophysiologi-cal processes. What distinguishes themfrom emotions is that they are regardedas having no psychological instigatingcauses (although this cannot be alwayssaid of yawning). Moreover, being con-stant and universal, they can readilyacquire communicative and symbolicsignificance.Empathy. The expressions of basic

emotions can be universally recognizedby conspecifics through an empathicprocess. In case of fear expressions, forexample, "the eyes and mouth are wide-ly opened, and the eyebrows raised" (2,p. 289). Since opening of the eyes andmouth allows greater blood flow into thefacial artery, lower CBF, and a morevigorous draining from the brain, a tem-porary rapid rise in brain temperature is

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9gCirculatory system ofthe head. The arteriesof interest for Wayn- 20baum's theory are (1)

1^

the common carotid, (2)the internal carotid, and(3) the external carotid.[Reproduced from P.Sappey, Traite d'Ana-tomie Descriptive (De-lahaye Lecrosnier, Par-is, 1888/89)]. A

allowed. As a consequence, the orga-nism may experience momentary dys-phoria. An animal in close proximity willnotice the terrified neighbor because itschange in posture is conspicuous. Theattention of the neighbor turns into mim-icry by virtue of the empathic process,and the neighbor, too, experiences somedysphoria in association with its ownaltered brain temperature.Empathy is an important social mech-

anism whereby the feelings of one indi-vidual are transmitted and partially expe-rienced by another. It is not entirelyclear how such transmission takes place(17). The vascular theory, however, sug-gests a hypothesis that makes the puzzleof empathy less mystifying. If muscularmovements of the face, by virtue of theireffects on CBF and on the release ofparticular neurotransmitters, are suffi-cient to induce changes in hedonic toneand result in changed subjective states,then reproducing the expression of an-other may well produce in the onlooker asimilar emotional state. Of course, thefeeling is not experienced equally. Butthis might be so only because the move-ments are not all faithfully reproduced.The question of why should one imitateothers' emotional expressions remains,and the answer may come from the the-ory of evolution. Mimicry has beenshown in 11-day-old infants (18), and it isgenerally viewed as part of the innatebehavioral repertoire of many species.

tions often occurs before pain is actuallyfelt. Writhing, weeping, and thrashing oflimbs bring relief. Frey (16) reportedfinding enkephalin in tears, which sug-5 APRIL 1985 19

Theoretical Consequences of anExpanded Vascular Theory

Once Waynbaum's hypothesis that ex-pressive acts have positive and negativehedonic and subjective consequences isverified, a number of phenomena associ-ated with emotion can be explicated andthe theory of emotional processes en-riched.Blushing and pallor. Blushing and pal-

lor are emotional phenomena that arerelatively involuntary and uncontrolla-ble. Noting that "women blush muchmore than men" (2, p. 310), Darwinconcluded that blushing occurs becauseattention is focused on part of one's ownbody. Since blushing occurs "in relationto the opinion of others" (2, p. 325), itaffects primarily the exposed parts of thebody. These vascular phenomena had adifferent meaning for Waynbaum. Blush-ing occurs in the case of emotions thatare intense, often sending a sudden surgeof blood through the main artery. Hencea great deal of energy is deployed with-out a possibility of efferent output. Theperson is ashamed, wishes to flee, hide,conceal a previous act, or confoundsomeone's possible deprecating attribu-tion. But in situations that cause blush-ing, there is little that the individual canusefully do. The mobilized energy has nooutlet and, as in suppressed rage, facialblood flow takes up the surplus. Thus,blushing relieves CBF. The face blushes,according to Waynbaum, not because itis exposed but because the facial arteryis a branch of the external carotid.The same is true of pallor. Pallor oc-

curs in temporary cerebral anemia, andthe contraction of the facial capillariesremedies it by increasing CBF. Theseactions are possible because the facialartery is rich in muscular tissue and cancontract and expand rapidly. Pallorbrought about in pain is caused by thepeculiar pain grimace of the major mus-cles around the mouth and eyes thatdiminish facial blood flow, and redirect itto the brain to ease suffering. Wayn-baum's faith in his theory led him toassert that if the main carotid branchedoff not at the neck but at the shoulders,we would express our emotions with ourarms, and blush with our shoulders.Facial feedback. The facial feedback

theory (19) holds that feedback fromfacial musculature provides informationfor the subjective experience of emotion.The facial feedback hypothesis differsfrom Waynbaum's theory in that thisfeedback only furnishes informationabout what the individual must havepreviously felt. Feedback does not causehedonic subjective experiences-those

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are assumed to have taken place before-hand.Ekman et al. (20) have thrown a light

on the problem. Subjects (some of themprofessional actors) were instructed toform their muscles, one by one, into sixclassical emotional expressions. The re-sults showed striking changes in heartrate associated with the various expres-sions, even though the connection be-tween their muscular movements andemotions was not disclosed to the sub-jects. The muscular pattern that conveysdisgust, for example, reduced heart rate,whereas that related to sadness acceler-ated it. Ekman et al. suggested that theactivity of the facial muscles triggers theautonomic reactions directly, either bymeans of facial feedback or through thedirect excitation of the hypothalamus bythe motor cortex.

Neither the evolutionary theory ofemotional expression nor the sensorytheory have much to contribute to thefacial feedback hypothesis or to the un-derstanding of the Ekman et al. data. Butthe vascular theory may be useful here.To the extent that facial muscles modu-late arterial and venous facial bloodflow, thereby controlling CBF, heart ratemay have to respond to these changes.In expressions of disgust, cerebral bloodsupply is augmented by increased flowthrough the internal carotid and reduceddraining because the instructed subjectplaces a "tourniquet" on the branches ofthe facial artery and on the veins aroundthe mouth and forehead. Brain blood,receiving new supply that passedthrough the cavernous sinus, is thus mo-mentarily cooled. In sad expression, thesame facial muscles are relaxed allowinga greater flow in the facial artery, lesserCBF, and more profuse return. Braintemperature is thus allowed to rise sincemetabolic processes continue whilethere is no cooling (21).Physiognomics. Since Aristotle, nu-

merous scholars attempted to relate indi-vidual differences in temperament to ap-pearance, especially the face (22). Infact, much of the early work on emotion-al expression is closely allied to phys-iognomics, but because no plausible ex-planatory principles were proposed, in-terest in physiognomics died. A reason-able and testable physiognomic theorycan be derived from Waynbaum's ideas.

Substantial individual differences existin facial musculature. For example, insome people the risorius muscle, whichextends the angle of the mouth, is absentaltogether. If the facial muscles play asignificant role in CBF and the resultingneurotransmitter effects, and if musclesdiffer among people, then individual dif-

ferences in expression may emerge. Ifsome facial muscle configurations canmodulate brain temperature to optimizethe action of neurotransmitters that aredifferentially involved in moods andemotions, and others cannot, then differ-ent affective dispositions correlated withfacial expression should be found.

This conjecture is strengthened if weconsider that voluntary and spontaneousemotional expressions are controlled bydifferent neural pathways (23). Sponta-neous emotional expressions use theextrapyramidal motor system, whereas"acted" facial expressions receive theirimpulses from the cortical motor strip,passing through the corticobulbar pro-jections. The social value of a well-func-tioning voluntary expressive control is asimportant as spontaneous expression,since both are powerful communicatorsof internal states and both influence thebehavior of others. Inability to smile"*sincerely" invites, throughout one'slifetime, social reactions that produce adifferent personality predisposition thanthe capacity to break into a "sparklingsmile."Emotional expression and mental

health. Since emotions are central phe-nomena of mental health, the vasculartheory of expression can be examinedfor its usefulness. For example, if braintemperature can influence moods by fa-cilitating the release of particular neuro-transmitters, and if facial musculaturecan modify brain temperature, then ther-mal biofeedback should be useful inteaching anxious or depressed patientsto control the appropriate facial musclesto induce more favorable affectivestates. Yoga and various forms of medi-tation are based in part on such an as-sumption (24). The effectiveness of suchtreatments, however, depends on wheth-er voluntary movements of facial mus-cles have the same CBF effects as spon-taneous ones and if patients can betrained to reproduce the spontaneousones sufficiently well. Perhaps the studyof other affective disorders and vasculardiseases may draw upon Waynbaum'stheory for new research directions.

Postscript. It remains for historians ofscience to discover why Waynbaum'soriginal ideas have been so completelyignored for so long. Of course his theory,ostensibly implausible, is not congruentwith what is known today about thevascular system, and it was alreadydoubted when Waynbaum first present-ed it at a meeting of the Societe dePsychologie Expe'rimentale et Com-paree. He was then struck down by suchrising luminaries as Henri Pieron andGeorges Dumas (25), the former alluding

SCIENCE, VOL. 228

to serious physiological difficulties, andboth arguing his functional explanations.Yet his basic idea is ingenious and rich inconsequences; when modified in thelight of what is known and assumedtoday about these processes, it organizesan array of divergent facts. It thereforedeserves to be reclaimed.

References and Notes1. I. Waynbaum, La Physionomie Humaine: Son

Me'canisme et son R6le Social (Alcan, Paris,1907).

2. C. R. Darwin, The Expression of the Emotionsin Man and Animals (Univ. of Chicago Press,Chicago, 1965).

3. C. G. Lange and W. James, The Emotions(Williams & Wilkins, Baltimore, 1922).

4. R. J. Andrew, Science 142, 1034 (1963). An-drew's interpretation of Darwin's principles hasto be taken with care in the light of Darwin'spassing disclaimer that there is any muscle that"has been developed or even modified exclu-sively for the sake of expression" (2, p. 354).

5. See, for example, R. Plutchik and H. Keller-man, Eds., Emotion: Theory, Research, andExperience (Academic Press. New York, 1980).

6. Note the Lamarckian touch in this interest ofDarwin.

7. D. H. Ingvar and J. Risberg, Exp. Brain Res. 3,195 (1967).

8. D. Minard and L. Copman, in Temperature: ItsMeasurement and Control in Science and Indus-try, C. M. Herzfeld, Ed. (Reinhold, New York,1963), vol. 3, part 3, p. 527.

9. K. M. A. Welch, P. J. Spira, L. Knowles, J. W.Lance, Arch. Neurobiol. 37, 253 (1974).

10. R. W. Ross Russell, Ed., Brain and Blood Flow(Pitman, London, 1971). Studies that demon-strated increased regional CBF in the motorcortex that corresponds to the action of particu-lar muscle groups used measures that register atbest within 6 millimeters of the brain surface;deeper flow dynamics escape these measures. Inemotional facial movement, CBF effects mayreach deeper into the brain and perhaps touchupon structures such as the limbic system thatare involved in emotional processes.

11. M. D. O'Brien, Headache 10, 139 (1971).12. W. D. Obrist, H. K. Thompson, C. H. King, H.

S. Wang, Circ. Res. 20, 124 (1967).13. D. S. Bell, Med. J. Aust. 2, 829 (1966); R. G.

Robinson et al., Stroke 14, 736 (1983).14. M. Globus et al., J. Cereb. Blood Flow Metab.

3, 287 (1983).15. T. Piderit, Grundzuege der Mimik und Physiog-

nomik (Vieweg, Braunschweig, 1858); P. Gratio-let, De la Physionomie et des Mouvementsd'Expression (Hetzel, Paris, 1865).

16. W. H. Frey, II, D. DeSota-Johnson, C. Hoff-man, J. Ophthalmol. 92, 559 (1981).

17. M. L. Hoffman, in Emotions, Cognition, andBehavior, C. E. Izard et al., Eds. (CambridgeUniv. Press, Cambridge, 1984), p. 103.

18. A. N. Meltzoff and M. K. Moore, Science 198,75 (1977).

19. C. E. Izard, Human Emotions (Plenum, NewYork, 1977); S. S. Tomkins, Affect, Imagery,Consciousness, vol. 1, The Positive Affects(Springer, New York, 1962); J. D. Laird, J.Pers. Soc. Psychol. 24, 475 (1974); J. T. Lan-zetta and S. P. Orr, ibid. 39, 1081 (1980).

20. P. Ekman, R. W. Levenson, W. V. Friesen,Science 221, 1208 (1983). A similar, more exten-sive experiment, was carried out by M. N.Rusalova, C. E. Izard, and P. V. Simonov[Aviat. Space Environ. Med. 46, 1132 (1975)].

21. Heart rate is not reduced to avoid flooding theinternal artery, but rather to decrease arterialpressure outside the brain. When cerebral spinalfluid pressure reaches that of arterial pressure,CBF is generally decreased if that arterial pres-sure remains constant. With freely varying arte-rial pressure, the increase of intracranial pres-sure triggers the Cushing reflex, that is, a con-spicuous increase in arterial blood pressure. Asa consequence, heart rate is reduced to attenu-ate arterial blood pressure outside of the brain.

22. M. Stanton, The Encyclopaedia of Face andForm Reading (Davis, Philadelphia, 1924).

23. G. H. Monrad-Krohn, Brain 47, 22 (1924).24. G. E. Schwartz, Am. Sci. 3, 314 (1975).25. I. Waynbaum, J. Psychol. Norm. Pathol. 3, 467

(1906).26. Supported by NSF grant BS-8117977. I thank P.

Adelmann, L. G. D'Alecy, J. F. Greden, J. T.Hoff, C. E. Izard, and H. Markus for theirvaluable suggestions, and M. Waynbaum forinformation about his father.

RESEARCH ARTICLE

Expression, Glycosylation, and Secretionof an Aspergillus Glucoamylase by

Saccharomyces cerevisiae

M. A. Innis, M. J. Holland, P. C. McCabe, G. E. ColeV. P. Wittman, R. Tal, K. W. K. Watt, D. H. Gelfand

J. P. Holland, J. H. Meade

Glucoamylases (E.C. 3.2.1.3) catalyzethe release of glucose from starch andrelated malto-oligosaccharides (1). As-pergillus awamori and the related spe-cies A. niger secrete two glycosylatedforms of glucoamylase designated GAIand GAII (2-4). Both forms are encodedby a single gene, are immunologicallyrelated, and have the same amino termi-nal amino acid sequence (4-7). The twoforms differ in the primary structure andlength of their carboxyl terminal se-quences, and recent evidence suggeststhat these differences arise as a conse-quence of differential RNA splicing (8).Both enzymes hydrolyze a(l,4)- anda(l,6)-glycosidic linkages, and the larger(GAI) form differs functionally from thesmaller (GAII) form only by its capacityto degrade raw starch (9).5 APRIL 1985

We have reported the molecular clon-ing and DNA sequence of the glucoam-ylase structural gene and a complemen-tary DNA (cDNA) clone for GAI mes-senger RNA (mRNA) from A. awamori(5, 6). The primary structure of the glu-coamylase gene and of cDNA clones forGAI and GAII from A. niger have alsobeen reported (7, 8). Comparison of theprimary structure of the glucoamylasegene with the cDNA clones has estab-lished that four intervening sequencesare spliced from both the GAI and GAIImRNA's. A fifth intervening sequence isspliced from the GAII mRNA. Analysesof putative regulatory sequences withinthe 5'- and 3'-flanking regions, as well aswithin the intervening sequences, of theglucoamylase gene revealed striking sim-ilarities to consensus sequences defined

for structural genes of S. cerevisiae (6).Despite these structural homologies, wereport here that we were unable to detecteither initiation or termination of tran-scription or proper splicing of the inter-vening sequences of the A. awamoriglucoamylase gene in S. cerevisiae.

Construction ofa yeast expression plas-mid and modifications of the glucoam-ylase gene. A 15-kilobase (kb) Hind IIIfragment that includes the entire gluco-amylase structural gene was introducedinto laboratory strains of yeast onan autonomously replicating plasmid,YEpl3 (10). These transformants had nodetectable enzymatic activity, immu-noreactive peptide, or glucoamylasemRNA sequences (11). Because gluco-amylase transcripts were not detected inyeast with the native Aspergillus gene, avector containing yeast regulatory sig-nals was used for the expression of glu-coamylase in yeast (Fig. 1). This expres-sion vector (pACI) contains an Esche-richia coli origin of replication, the blagene from pBR322, the yeast 2,u origin ofreplication, and a yeast LEU2 structuralgene. These features.of the plasmid per-mit autonomous replication and selec-tion in E. coli and yeast. The vector alsocontains the promoter and terminationregions of one of the yeast enolase

M. A. Innis, P. C. McCabe, G. E. Cole, V. P.Wittman, R. Tal, K. W. K. Watt, D. H. Gelfand, andJ. H. Meade are in the Division of Molecular andBiological Research, Cetus Corporation, Emery-ville, California 94608. M. J. Holland and J. P.Holland are in the Department of Biological Chemis-try, School of Medicine, University of California,Davis 95616.

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