BEHAVIORAL AND BRAIN SCIENCES (2002) 25, 1–72 Printed in the United States of America Empathy: Its ultimate and proximate bases Stephanie D. Prestona and Frans B. M. de Waalb aUniversity of Iowa Hospital and Clinics, 2RCP – Neurology Clinic, Iowa City, IA 52242; bLiving Links, Yerkes Primate Center and Psychology Department, Emory University, Atlanta, GA 30322 [email protected] [email protected] http://www.medicine.uiowa.edu/prestonresearch http://www.emory.edu/LIVING_LINKS/ Abstract: There is disagreement in the literature about the exact nature of the phenomenon of empathy. There are emotional, cogni- tive, and conditioning views, applying in varying degrees across species. An adequate description of the ultimate and proximate mecha- nism can integrate these views. Proximately, the perception of an object’s state activates the subject’s corresponding representations, which in turn activate somatic and autonomic responses. This mechanism supports basic behaviors (e.g., alarm, social facilitation, vicar- iousness of emotions, mother-infant responsiveness, and the modeling of competitors and predators) that are crucial for the reproduc- tive success of animals living in groups. The Perception-Action Model (PAM), together with an understanding of how representations change with experience, can explain the major empirical effects in the literature (similarity, familiarity, past experience, explicit teach- ing, and salience). It can also predict a variety of empathy disorders. The interaction between the PAM and prefrontal functioning can also explain different levels of empathy across species and age groups. This view can advance our evolutionary understanding of empa- thy beyond inclusive fitness and reciprocal altruism and can explain different levels of empathy across individuals, species, stages of de- velopment, and situations. Keywords: altruism; cognitive empathy; comparative; emotion; emotional contagion; empathy; evolution; human; perception-action; perspective taking 1. Introduction key in sight of the subject to be shocked. After the subjects witnessed the shock of the conspecific, two-thirds pre- The concept empathy has had a difficult history, marked by ferred the nonshock chain even though it resulted in half as disagreement and discrepancy. Although it has been stud- many rewards. Of the remaining third, one stopped pulling ied for hundreds of years, with contributions from philoso- the chains altogether for 5 days and another for 12 days af- phy, theology, developmental psychology, social and per- ter witnessing the shock of the object. These monkeys were sonality psychology, ethology, and neuroscience, the field literally starving themselves to prevent the shock to the con- suffers from a lack of consensus regarding the nature of the specific. Starvation was induced more by visual than audi- phenomenon. Despite this disagreement, the empirical tory cues, was more likely in animals that had experienced data on empathy are very consistent, across a wide range of shock themselves, and was enhanced by familiarity with the species. Consider the following examples: shocked individual (Masserman et al. 1964). An albino rat sees a distressed conspecific suspended in Human infants orient to the distress of others, often re- the air by a harness; he presses a bar to lower the rat back sponding with their own distress cries from infancy to 14 to safe ground, staying close to and oriented toward him months (e.g., Sagi & Hoffman 1976; Ungerer 1990; Zahn- (Rice & Gainer 1962). Another rat sees a distressed con- Waxler & Radke-Yarrow 1982). After the first year, children specific receiving electric shocks and does not press the bar start to show helping behaviors, even when they have be- to terminate the shock, he instead “retreat[s] to the cor- come distressed. They also imitate the distress behaviors of ner... farthest from the distressed, squeaking, and danc- the other, possibly “trying on” the expressions to better un- ing animal and crouch[es] there, motionless” (Rice 1964, derstand them (Zahn-Waxler et al. 1977, in Thompson p. 167). The response of a rat to shock of a conspecific oc- 1987). With age, the level of personal distress decreases curs without any prior experience with shock, is stronger af- while appropriateness of helping behaviors increases (e.g., ter prior experience with shock, and strongest when prior Zahn-Waxler et al. 1983). shock occurred at the same time as to the conspecific These examples, all from empirical reports, show that in- (Church 1959). dividuals of many species are distressed by the distress of a In an experiment with rhesus monkeys, subjects were conspecific and will act to terminate the object’s distress, trained to pull two chains that delivered different amounts even incurring risk to themselves. Humans and other ani- of food. The experimenters then altered the situation so mals exhibit the same robust effects of familiarity, past ex- that pulling the chain with the larger reward caused a mon- perience, and cue salience (Table 1), and parallels exist be- © 2002 Cambridge University Press 0140-525X/02 $12.50 1 Preston & de Waal: Empathy: Its ultimate and proximate bases tween the development of empathy in young humans and 1.1. Terminology the phylogenetic emergence of empathy (de Waal 1996; Hoffman 1990, respectively). These facts suggest that em- 1.1.1. Proximate versus ultimate. Ernst Mayr first created pathy is a phylogenetically continuous phenomenon, as the distinction between proximate and ultimate causes of suggested by Charles Darwin more than a century ago behavior. According to Mayr, “proximate causes govern the (1871/1982). responses of the individual (and his organs) to immediate The goal of this theoretical review is to present data factors of the environment while ultimate causes are re- across disciplines so that the continuity is apparent. More- sponsible for the evolution of the particular DNA code of over, this paper aims to show that consistencies exist be- information with which every individual of every species is cause all empathic processes rely on a general perception- endowed” (Mayr 1961, p. 1503). Causes exist at each of action design of the nervous system that has been postulated these levels; therefore, theories that refer to different lev- for over a century, is adaptive for myriad reasons, and exists els are not in conflict. For example, when you help your dis- across species. Recent advances in interdisciplinary re- tressed neighbor, is it because you “feel their pain,” or be- search and tools for understanding the brain provide strong cause you will eventually need them to reciprocate? Given support for the Perception-Action Model (PAM), warrant- Mayr’s levels of causality, these hypotheses are not in con- ing its application to emotional domains. This Perception- flict; the former is a proximate explanation, the latter an ul- Action Model also sheds light on the ultimate level de- timate one. scription, placing the emphasis on direct effects on reproductive success from the general design of the ner- 1.1.2. Definitional distinctions. Much of the empathy lit- vous system, rather than on indirect effects from helping erature focuses on whether empathy is an emotional or cog- behaviors. Thus, by fleshing out the phenomenon along nitive process and distinguishes empathy from emotional both proximate and ultimate levels, and by combining data contagion, sympathy, and perspective taking (e.g., Eisen- across fields, a unified story emerges. berg 1986; Feshbach 1975; Hoffman 1978a; 1982a; Horn- blow 1980; Omdahl 1995; Shantz 1975; Wispé 1986). These distinctions are empirically based and help to categorize be- havior (Batson et al. 1987; Doherty 1997; Eisenberg et al. 1994; 1998; Eisenberg & Okun 1996; Rice 1964; distinc- tions summarized in Table 2), but they have been overem- phasized to the point of distraction. This overemphasis on definition reflects the deeper problem that empathy lacks Stephanie Preston received her doctorate in Psy- a proximate mechanism. Abstract and elusive definitions chology in 2001 from the University of California, like “putting oneself in the place of another” or “imagina- Berkeley. Her dissertation investigated the effects of so- tively projecting oneself into the situation of another” (All- cial and metabolic stress on food-hoarding decisions in kangaroo rats. Her interdisciplinary research combines port 1937; Buchheimer 1963; Demos 1984; Goldie 1999; techniques and ideas across fields, and uses naturalistic Smith 1989) indicate an insufficient understanding of the paradigms, in order to study how emotion and cognition way the nervous system instantiates empathy. Thirty years interact to produce behavior. She is currently a post- ago G. W. Allport said it best when he concluded, “the doctoral fellow at the University of Iowa with Antoine process of empathy remains a riddle in social psychol- Bechara, doing behavioral, psychophysiological, and ogy . The nature of the mechanism is not yet understood” brain imaging research on empathy, decision-making, (Allport 1968, p. 30 from Wispé 1987, original emphasis). and hoarding. The original German word Einfühlung, of which the Eng- Frans B. M. de Waal is a Dutch-born ethologist/ lish “empathy” is Titchener’s translation (1909; Wispé 1991, zoologist renowned for his work on the social intelli- p. 78), literally means “feeling into” (Wispé 1986). Einfüh- gence of primates, such as chimpanzees, bonobos, ca- lung was thought to result from a process where observers puchin