American Journal of Primatology 73:503–506 (2011)

INTRODUCTION Understanding in : In Honor of Darwin’s 200th Birthday à DOROTHY FRAGASZY AND ELIZABETH SIMPSON University of Georgia, Athens, Georgia In the bicentenary year of Darwin’s birth, the American of Primatologists honored his memory by convening a symposium entitled ‘‘Understanding emotions in primates: In honor of Darwin’s 200th birthday.’’ The four articles in this special section, excepting this introduction, derive from that symposium. The section confirms that the topic of is once again, as in Darwin’s lifetime, the subject of wide-ranging, theoretically exciting research, and that studies with nonhuman primates are at the leading edge of a rapidly changing field. Am. J. Primatol. 73:503–506, 2011. r 2011 Wiley-Liss, Inc.

Key words: health; behavior; ; well-being

In 2009, the world celebrated Darwin’s contribu- feverish pitch ever since On the Origin of Species tions to science on the bicentenary of his birth in appeared, and the of likewise 1809. Every student of knows that Charles has been developed extensively in modern evolu- Darwin published On the Origin of Species in 1859, tionary theory, Darwin’s last great treatise concern- and that the theory of that he advocated in ing and behavior has received far this slim volume generated vigorous debate among less . , in the introduction to the scientific community, the clergy, and the general the 3rd edition of The Expression, writes ‘‘y [U]ntil public in Britain and beyond for many years very recently the book had been studiously ignored. following—indeed, to the present day. We are all Yet it was a bestseller when it was published in familiar with the basic tenets of Darwin’s theory of England in 1872. Nine thousand copies were sold in evolution, including the linked hypotheses that the first four months. By the turn of the century it diverse forms of life arise through had also been published in the United States, the acting upon heritable variations, and thus that Netherlands, France, Germany, and Russia. y contemporary diversity reflects historical continuity. Today and layman alike know who Darwin Darwin made clear that this interpretation of is, but not his book on expression. Many biologists do biological diversity applied to humans, and posited not even know that Darwin wrote such a booky’’ a refined model of selection to account for certain [Ekman, 1998; p xxix]. Indeed, for most of the characteristics of sexually reproducing species, in a century after Darwin wrote about expression, his second great volume, The Descent of Man and the views were rejected or simply ignored. Selection in Relation to Sex, published in 1871. Although the topic of emotion seems to have Within days of finishing the page proofs for this languished in the doldrums of the sea of science for book, he began work on his final book concerning close to a century, it has resurfaced in recent humans, The Expression of the Emotions in Man and decades, and Darwin’s singular contribution to this , and finished it in a mere 4 months [Ekman, area of science is now better appreciated. Historians 1998]. This book appeared in 1872, and like his two of science may point to many threads of thinking and previous books, it was an immediate best seller. evidence that supported this change. We like to think In The Expression of the Emotions of Man and that the persistent effort of researchers studying the Animals (1872; now in its fourth edition, 2009), behavior of nonhuman primates played a role in this Darwin established emotion as a proper topic of renaissance. Thus, it seemed fitting, on the bicen- scientific study from a biological perspective, and he tenary of Darwin’s birth, to honor him by treating argued that humans display, in their expressions of emotion as in other aspects of their biology, ÃCorrespondence to: Dorothy Fragaszy, Department of , University of Georgia, Athens, GA 30602. their shared ancestry with other animals. He also E-mail: [email protected] proposed that emotions are discrete, that the face is Received 21 December 2010; revision accepted 22 December particularly expressive of emotions, and that facial 2010 expressions of emotion in humans are universal. DOI 10.1002/ajp.20933 Although scientific scrutiny and public debate of Published online 15 February 2011 in Wiley Online Library (wiley the general theory of evolution has continued at a onlinelibrary.com). r 2011 Wiley-Liss, Inc. 504 / Fragaszy and Simpson

the topic of emotions to a thoroughly public systems) brain activity can be measured indirectly consideration, to see in some measure where we using electroencephalogram, and locations of brain have been and where we are going in our efforts to activity can be measured indirectly using functional understand emotions in primates. For this purpose, magnetic resonance imaging [e.g., Hoffman et al., the American Society of Primatologist convened a 2007]. Physiological measures of autonomic symposium at our 2009 meeting entitled ‘‘Under- have been used with both human and nonhuman standing emotions in primates: In honor of Darwin’s animals, and include measures of facial temperature 200th birthday.’’ The symposium opened with a (e.g.,nosetemperatureinnonhumanprimates),heart major address by a featured speaker, J. Panksepp, rate,respiration,skinconductance,pupildilation,eye and continued with four additional presentations. blinks, and startle responses [e.g., Reefmann et al., 2009]. We can link behavioral indices of emotion (e.g., a particular component of maternal behavior) with STUDYING EMOTIONS AND PHYSIOLOGICAL a neurochemical state, as measured by titers of SYSTEMS THAT SUBSERVE THEM neurotransmitters, hormones, or certain proteins We take as our starting point Darwin’s conclu- [e.g., Campbell, 2010; Grigoriev et al., 2003]. Single sions that emotions in humans and nonhuman cell recordings can directly measure neural activity in reveal shared ancestry and function, and response to emotional stimuli [e.g., Maior et al., 2010]. that emotions are in many dimensions qualitatively Precise behavioral measures are available for similar across mammals. More specifically, basic studies with humans and other animals, and provide emotions—SEEKING, , , , maternal another dimension for comparison across species. CARE, separation distress /, and For example, the movements or activations of facial physical PLAY [Panksepp, 2011, this issue]—are musculature can be measured using facial electro- shared widely among mammals, and likely among an myography. Sometimes, such muscle movements are even wider array of species. Conditions or circum- not visible to the naked eye, yet can be measured stances that increase positive emotions—friendships, with this equipment and provide information about good food, status, attractive mates, safe and comfor- emotional responses and emotional interpretations. table shelter, caring for offspring—are things that The facial action coding system has been employed aid in our survival and reproduction. Experiences with human and nonhuman primates [e.g., Vick and stimuli that increase negative emotions— et al., 2007]. On a larger scale, one can quantify body , predators, rotten food, and disease— postures, or approach and avoidance movements, likewise survival and reproduction. For example, and preferences. Thus, even though paradigms that humans’ attention, and likely other animals’ attention rely on verbal report are relevant only to humans, as well, is captured relativelyeasilybythreatening we have many ways to study emotion comparably stimuli (e.g., loud noise, angry face). For many across species. animals—including humans—social interactions with conspecifics are of utmost importance. Social animals interpret the emotional signals (facial expressions, OVERVIEW OF THE SPECIAL SECTION vocal expressions, postures) of conspecifics. Situations This special section contains contributions by that compromise social connections temporarily four presenters in the 2009 symposium (J. Panksepp, enhance social perception in humans, and may do so J. Capitanio, D. Maestripieri, and M. Owren). in other animals as well. For example, in humans, J. Panksepp [2011] recounts the history of the increasing of social rejection improve the neuroscientific study of behavior to illustrate how, ability to recognize whether an expression (e.g., smile) until very recently, emotions in nonhuman animals is genuine or artificial, a characteristic which is were set aside as improper subjects of research. proposed to facilitate affiliation [Bernstein et al., 2008]. We now know from decades of careful scientific Given shared ancestry and shared function, inquiry that emotional experience in humans, as in emotion, such as other features of the organism, all other mammals, does not depend upon cortical can be profitably studied from an evolutionary and interpretation of bodily states; rather, emotional comparative perspective. For data on diverse species experiences in humans arise from the same (i.e., to be interpretable within a comparative framework, homologous) subcortical neural networks as in all it is important to have standardized methods of mammals that have been studied closely, reconfirm- assessing emotion and useful to have multiple measure- ing Darwin’s intuitive understanding of continuity of ment tools for a given assessment. Fortunately, we emotional process across species (at least, across have a variety of methods that are appropriate for mammals). The neuroscientific evidence clearly studying physiological underpinnings of emotions in shows that emotion is directly experienced (in many species. For example, select regions of the brain Panksepp’s words, ‘‘primary process’’). Panksepp can be stimulated or blocked from activity to measure [2011] suggests that we are now positioned to behavioral or other consequences [e.g., Krack et al., connect psychodynamics (aspects of brain function 2010]. The timing of larger scale (i.e., structures, that are experienced) to the neurodynamics of the

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brain. A challenge for contemporary neuroscience is production. Affectively triggered vocalizations share to study primary-process affective experiences in all the same neural pathway across mammals, involving mammals (both positively and negatively valenced subcortical structures in the limbic system. However, experiences) and, in this way, better understand the a functionally distinct vocal capacity to produce nature of human psychiatric disorders. novel sounds, present in humans and perhaps Capitanio [2011] shows how Panksepp’s call to present in rudimentary form in great , is asso- examine both positively and negatively valenced ciated with a second, cortically based neural path- emotions in nonhuman primates can yield advances way. The second pathway has counterparts in orders in understanding health in a broad sense. He reviews other than primates (e.g., bats and song birds, and evidence that temperament mediates individual differ- perhaps some marine mammals), suggesting conver- ences in health in captive rhesus monkeys. Capitanio gent evolution. Owren et al. suggest that affectively [2011] points to sociability (a general tendency to triggered vocalizations develop in the production- affiliate with others) as a feature of temperament first manner, whereas language develops in the associated with positive affect and with sensitivity of reception-first manner. According to this framework, brain systems to dopamine. Capitanio [2011] shows experience can play a different role in the develop- that sociability has both direct and indirect effects on ment of the two kinds of systems. The authors monkeys’ health, and that those indirect effects are interpret almost all the evidence for vocal flexibility mediated by how well individuals fit the situations in in nonhuman primates as concordant with a which they find themselves. As Panksepp [2011] production-first, affectively triggered system, which suggested would be the case, this insight about is shared with humans, as Darwin proposed. This emotion informs our understanding of health and interpretation differs importantly from the conven- coping in humans and in nonhuman primates. tional view of many researchers in this area that Maestripieri [2011] looks at a complex set of instead view elements of vocal flexibility in non- emotional processes relevant to maternal behavior human primates as shared with human language. in rhesus monkeys. Under normal circumstances, As in matters of health and maternal behavior, much maternal behavior in mammals waxes and wanes in about the role of affect in vocal communication in predictable ways in concert with infants’ needs for primates remains to be investigated. protection and nourishment. However, individuals vary considerably from one another in maternal behavior, as well as in general temperament. FUTURE DIRECTIONS Emotional reactivity is an important regulator of The articles in this special section have pre- maternal behavior. Individual differences in emo- sented an array of fundamental topics, including tional reactivity also correspond with individual differ- health, maternal behavior, social development, and ences in susceptibility to stress. Maestripieri [2011] communication, in which research with nonhuman reviews how emotional reactivity and stress interact to primates has already provided insights into the role affect maternal behavior in rhesus monkeys, a topic of emotions in biology. And, there is a bright future that calls out for further research. Furthermore, he for continuing research in emotions, both with points out that some negatively valenced features of respect to basic biology and to , as Panksepp Pryce’s [1992] widely cited model of maternal motiva- [2011] reminds. For example, characterizing indivi- tion in mammals seem not to be present in normally dual differences in , understanding reared rhesus monkeys, but rather are evident only in emotional expressions in others, and the develop- atypically reared rhesus monkeys. This finding marks mental and experiential origins of these differences an apparent important difference in maternal motiva- are important challenges. Another major challenge, tion between primates and rodents, and one that in the neurobiology of emotion, is to understand warrants careful scrutiny for the advancement of emotional processes. We are increasingly informed theory in this area. about the neural structures involved in emotions, Owren et al. [2011] address the role of emotion but much less so about the processes that take place, (affect) in vocalizations of monkeys and apes, and the nor about direct and indirect influences of these extent to which vocalizations can be voluntarily processes on the rest of the brain. modulated, topics of abiding relevance to the evolu- It is clear that the body, in addition to the brain, tion of language. They propose two principles, one participates in the perception of others actions, concerning development and the other concerning including emotional expressions. For example, recent neural pathways, which characterize vocalizations work with humans has found that body posture (e.g., across species, and they use these principles to supine position) and facial posture (e.g., holding interpret a broad literature concerning vocal flexi- a pencil between teeth) can each influence the bility in primates. The first principle is that there are perception of emotional stimuli, one’s emotional state, two patterns of vocal development, ‘‘production and emotional brain activation [e.g., Davis et al., first’’ and ‘‘reception first.’’ The second principle 2010]. It would be interesting to explore whether concerns the neural pathways associated with vocal similar modulation of occurs in

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nonhuman primates. Another rich avenue to explore Davis JI, Senghas A, Brandt F, Ochsner KN. 2010. The effects in comparative research is the role of the mirror of BOTOX injections on emotional experience. Emotion neuron system [Rizzolatti & Craighero, 2004] in 10:433–440. DOI: 10.1037/a0018690. Ekman P. 1998. Introduction to the third edition. emotional responsiveness in various species. For ex- In: Darwin C, editor. The expression of emotions in man ample, in humans, a match between an observer’s and animals. Third edition. Oxford: Oxford University posture and a target’s facilitates Press. emotional understanding [Niedenthal, 2007]. Grigoriev IV, Nikolaeva LV, Artamonov ID. 2003. Better understanding of emotions in nonhuman Protein content of human saliva in various psychoemotional states. Biochemistry 68:405–406. DOI: 10.1023/ primates can improve their care and management, A:1023695729019. thus improving their health and well-being. It is our Hoffman KL, Gothard KM, Schmid MC, Logothetis NK. ethical responsibility to provide for their well-being 2007. Facial-expression and gaze-selective responses in the and this includes promoting positive emotional monkey amygdala. Current Biology 17:766–772. DOI: 10.1016/ j.cub.2007.03.040. states. In addition, providing maximal well-being Krack P, Hariz M, Baunez C, Guridi G, Obeso JA. 2010. for captive animals in research is cost-effective. Deep brain : from to psychiatry? Emotionally healthy animals are more successful at Trends in Neuroscience 33:474–484. DOI: 10.1016/j.tins. reproducing, live longer and with fewer health 2010.07.002. complications, and provide better quality data. Maestripieri D. 2011. Emotions, stress, and maternal motiva- tion in primates. American Journal of Primatology Though emotions research historically has 73:516–529. focused on negative emotions in nonhuman animals, Maior RS, Hori E, Tomaz C, Ono T, Nishijo H. 2010. The a paradigm shift is underway, as is evident in all the monkey pulvinar neurons differentially respond to emo- articles in this section. We now realize that we need tional expressions of human faces. Behavioural Brain Research 215:129–135. DOI: 10.1016/j.bbr.2010.07.009. to study emotions in all animals in a balanced way, Niedenthal PM. 2007. Embodying emotion. Science with equal attention to positively and negatively 18:1002–1005. DOI: 10.1126/science.1136930. valenced emotions. Thus, we can expect to see our Owren M, Amoss T, Rendall D. 2011. Two organizing models and our studies of emotion in nonhuman principles of vocal production: implications for nonhuman animals expand to include play, social bonding, , and human primates. American Journal of Primatology 73:530–544. and other positive emotions. That is a pleasant Panksepp J. 2011. Toward a cross-species neuroscientific thought, as well as good science. understanding of the affective mind: do animals have emotional feelings? American Journal of Primatology 73:545–561. REFERENCES Pryce CR. 1992. A comparative systems model of the regulation of maternal motivation in mammals. Behaviour Bernstein MJ, Young SG, Brown CM, Sacco DF, Claypool HM. 43:417–441. DOI: 10.1016/S0003-3472(05)80102-2. 2008. Adaptive responses to social exclusion: social rejection Reefmann N, Wechsler B, Gygax L. 2009. Behavioural and improves detection of real and fake smiles. Psychological physiological assessment of positive and negative emotion in Science 19:181–983. DOI: 10.1111/j.1467-9280.2008.02187.x. sheep. Animal Behaviour 78:651–659. DOI: 10.1016/j.anbehav. Campbell A. 2010. Oxytocin and human social behavior. 2009.06.015. Personality and Review 14:281–295. Rizzolatti G, Craighero L. 2004. The mirror-neuron system. DOI: 10.1177/1088868310363594. Annual Review of Neuroscience 27:169–192. DOI: 10.1146/ Capitanio JP. 2011. Individual differences in emotionality: annurev.neuro.27.070203.144230. social temperament and health. American Journal of Prima- Vick S, Waller BM, Parr LA, Smith-Pasqualini MC, Bard KA. tology 73:507–515. 2007. A cross-species comparison of facial morphology and Darwin C. 2009. The expression of emotions in man and movement in humans and using the Facial animals. Oxford: Oxford University Press. Fourth edition. Action Coding System (FACS). Journal of Nonverbal First published 1872, John Murray, London. Behavior 31:1–20. DOI: 10.1007/s10919-006-0017-z.

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