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Emotional Linkage in Animals

When Zahn-Waxler visited homes to find out how children respond to family members who were instructed to feign sadness (sobbing), pain (crying), or distress (choking), she discovered that children a little over one year of age already comfort others. This is a milestone in their development: an aversive experience in another person draws out a concerned response. An unplanned side-bar to this classical study, however, was that some household pets appeared as worried as the children by the "distress" of a family member. They hovered over them or put their heads in their laps (Zahn-Waxler et al. 1984).

Intersubjectvitity has many aspects apart from emotional linkage, such as an appraisal of the other's situation, experience-based predictions about the other's behavior, extraction of information from the other that is valuable to the self, and an understanding of the other's knowledge and intentions. When the emotional state of one individual induces a matching or related state in another, we speak of emotional contagion (Hatfield et al. 1993). With increasing differentiation between self and other, and an increasing appreciation of the precise circumstances underlying the emotional states of others, emotional contagion develops into empathy. Empathy encompasses - and could not possibly exist without - emotional contagion, yet empathy goes beyond it in that it places filters between the other's state and the subject's own state and adds a cognitive layer. In empathy, the subject does not confuse its own internal state with the other's. These various levels of empathy, including personal distress and sympathetic concern, are defined and discussed in detail by Eisenberg (2000).

Empathy is a social phenomenon with great adaptive significance for animals in groups. The fact that most modern textbooks on animal cognition do not index empathy or sympathy does not mean that these capacities are not essential; it only means that they have been overlooked by a science traditionally focused on individual rather than inter-individual capacities. Inasmuch as the survival of many animals depends on concerted action, mutual aid, and information transfer, selection must have favored proximate mechanisms to evaluate the emotional states of others and quickly respond to them in adaptive ways. Even though the human empathy literature often emphasizes the cognitive side of this ability, Hoffman (1981, p. 79) rightly noted early on that "humans must be equipped biologically to function effectively in many social situations without undue reliance on cognitive processes."

Empathy allows us to relate to the emotional states of others. This ability is critical for the regulation of social interactions, such as coordinated activity, cooperation towards a common goal, social bonding, and care of others. It would be strange indeed if a survival mechanism that arises so early in life in all members of our species would be without animal parallels.

Early Experiments

An interesting older literature by experimental psychologists addresses empathy (reviewed by Preston and de Waal 2002a,b). In a paper provocatively entitled "Emotional reactions of rats to the pain of others," Church (1959) established that rats that had learned to press a lever to obtain food would stop doing so if their response was paired with the delivery of an electric shock to a neighboring rat. Even though this inhibition habituated rapidly, it suggested something aversive about the pain reactions of others. Perhaps such reactions arouse negative emotions in those who see and hear them.

In the same year as Church's rat study, Miller et al. (1959) published the first of a series of pioneering papers on the transmission of affect in rhesus macaques. They found that monkeys react with avoidance to pictures of conspecifics in a fearful pose, and that this reaction is stronger than that towards a negatively conditioned stimulus. This discovery was astonishing, suggesting that seeing the fear of a two-dimensional, soundless representation of another monkey is more disturbing than the anticipation of an actual electric shock.

Perhaps the most compelling evidence for the strength of the empathic reaction in monkeys came from Wetchkin et al. (1964) and Masserman et al. (1964). They found that rhesus monkeys refuse to pull a chain that delivers food to themselves if doing so shocks a companion. One monkey stopped pulling for five days, and another one for twelve days, after witnessing shock-delivery to a companion. These monkeys were literally starving themselves to avoid inflicting pain upon another, and they maintained this response to a far greater degree than has been reported for rats.

Evidence ofPrimate Empathy

Qualitative accounts of great apes support the view that these animals show strong emotional reactions to others in pain or need. Yerkes (1925, p. 246) reported how his bonobo, Prince Chim, was so extraordinarily concerned and protective towards his sickly chimpanzee companion, Panzee, that the scientific establishment might not accept his claims: "If I were to tell of his altruistic and obviously sympathetic behavior towards Panzee I should be suspected of idealizing an ape" (Fig. 3). Ladygina-Kohts (1935, p. 121) noticed similar empathie tendencies in her young chimpanzee, Joni, whom she raised at the beginning of the previous century, in Moscow. Kohts, who analyzed Joni's behavior in the minutest detail, discovered that the only way to get him off the roof of her house after an escape

Chim Panzee

Fig. 3. Robert Yerkes with two apes in his lap. This photo was taken in 1923, before the discovery of the bonobo as a distinct species. We know now that the ape on the right, named Prince Chim, was a bonobo. Prince Chim was described by Yerkes as gentler and more empathic than any other ape he knew. In debates about human evolution, the bonobo is largely ignored, however. (Photograph by Lee Russell, courtesy of the Yerkes National Primate Research Center).

Fig. 3. Robert Yerkes with two apes in his lap. This photo was taken in 1923, before the discovery of the bonobo as a distinct species. We know now that the ape on the right, named Prince Chim, was a bonobo. Prince Chim was described by Yerkes as gentler and more empathic than any other ape he knew. In debates about human evolution, the bonobo is largely ignored, however. (Photograph by Lee Russell, courtesy of the Yerkes National Primate Research Center).

(much better than any reward or threat of punishment) was by appealing to his sympathy:

"If I pretend to be crying, close my eyes and weep, Joni immediately stops his plays or any other activities, quickly runs over to me, all excited and shagged, from the most remote places in the house, such as the roof or the ceiling ofhis cage, from where I could not drive him down despite my persistent calls and entreaties. He hastily runs around me, as if looking for the offender; looking at my face, he tenderly takes my chin in his palm, lightly touches my face with his finger, as though trying to understand what is happening, and turns around, clenching his toes into firm fists."

Similar reports are discussed by de Waal (1996a, 1997a), who suggests that, apart from emotional connectedness, apes have an appreciation of the other's situation and a degree of perspective-taking. Apes show the same empathic capacity that was so enduringly described by Smith (1759, p. 10) as "changing places in fancy with the sufferer."

O'Connell (1995) conducted a content analysis of thousands of qualitative reports, counting the frequency of three types of empathy, from emotional contagion to more cognitive forms, including an appreciation of the other's situation. Understanding the emotional state of another was particularly common in the chimpanzee, with most outcomes resulting in the subject comforting the object of distress. Monkey displays of empathy were far more restricted but did include the adoption of orphans and reactions to illness, handicaps, and wounding.

This difference between monkey and ape empathy is also evident from systematic studies of behavior known as "consolation," first documented by de Waal and van Roosmalen (1979). Consolation is defined as friendly, reassuring contact directed by an uninvolved bystander at one of the combatants in a previous aggressive incident. For example, a third party goes over to the loser of a fight and gently puts an arm around his shoulders (Fig. 4). Consolation is not to be confused with

Fig. 4. Consolation among chimpanzees: ajuvenile puts an arm around a screaming adult male who has just been defeated in a fight with a rival. (Photograph by the author).

Fig. 4. Consolation among chimpanzees: ajuvenile puts an arm around a screaming adult male who has just been defeated in a fight with a rival. (Photograph by the author).

Fig. 5. The rate with which third parties contact victims of aggression in chimpanzees, comparing recipients of serious and mild aggression. Especially in the first two minutes following the incident, recipients of serious aggression receive more contacts than baseline. After de Waal and Aureli (1996).

Fig. 5. The rate with which third parties contact victims of aggression in chimpanzees, comparing recipients of serious and mild aggression. Especially in the first two minutes following the incident, recipients of serious aggression receive more contacts than baseline. After de Waal and Aureli (1996).

reconciliation, which seems selfishly motivated (see above). The advantages of consolation for the actor remain unclear. The actor could probably walk away from the scene without negative consequences.

Chimpanzee consolation is well quantified. De Waal and van Roosmalen (1979) based their conclusions on an analysis ofhundreds of post-conflict observations, and a replication by de Waal and Aureli (1996) included an even larger sample in which the authors sought to test two relatively simple predictions. If third-party contacts indeed serve to alleviate the distress of conflict participants, these contacts should be directed more at recipients of aggression than at aggressors, and more at recipients of intense rather than mild aggression. Comparing third-party contact rates with baseline levels, we found support for both predictions (Fig. 5).

Consolation has thus far been demonstrated only in great apes. When de Waal and Aureli (1996) set out to apply exactly the same observation protocols as used on chimpanzees to detect consolation in macaques, they failed to find any (see also Watts et al. 2000). This finding came as a surprise, because reconciliation studies, which employ essentially the same design, have shown reconciliation in species after species. Why, then, would consolation be restricted to apes?

Targeted helping in response to specific, sometimes novel situations may require a distinction between self and other that allows the other's situation to be divorced from one's own while maintaining the emotional link that motivates behavior. Possibly, one cannot achieve cognitive empathy without a high degree of self awareness. In other words, to understand that the source of a vicarious affective state is not oneself but the other, and to understand why the other's state arose (e.g., the specific cause of the other's distress), one needs a distinction between self and other. Based on these assumptions, Gallup (1982) was the first to speculate about a possible connection between cognitive empathy and mirror self-recognition (MSR). This view is supported both developmentally, by a correlation between the emergence of MSR in children and their helping tendencies

(Bischof-Kohler 1988; Zahn-Waxler et al. 1992), and phylogenetically, by the presence of complex helping and consolation in hominoids (i.e., humans and apes) but not monkeys. Hominoids are also the only primates with MSR.

I have argued before that, apart from consolation behavior, targeted helping reflects cognitive empathy. Targeted helping is defined as altruistic behavior tailored to the specific needs of the other even in novel situations, such as the highly publicized case of Binti-Jua, a gorilla female who rescued a human boy at the Brookfield Zoo, in Chicago (de Waal 1996a, 1999). Targeted helping is common in the great apes but is also striking in dolphins (Caldwell and Caldwell, 1966). The recent discovery of MSR in dolphins (Reiss and Marino, 2001) thus fits the proposed connection between increased self-awareness, on the one hand, and cognitive empathy, on the other.

Russian Doll model

The literature includes accounts of empathy as a cognitive affair, even to the point that apes, let alone other animals, probably lack it (Povinelli 1998; Hauser 2000). This "top-down" view equates empathy with mental state attribution and theory-of-mind (ToM). The opposite position has recently been defended, however, in relation to autistic children. In contrast to earlier assumptions that autism reflects a deficit in ToM (Baron-Cohen 2000), autism is noticeable well before the age of four, at which time ToM typically emerges. Williams et al. (2001) argue that the main deficit of autism concerns the socio-affective level, which then negatively impacts more sophisticated down-stream forms of inter-personal perception, such as ToM (see also Baron-Cohen 2004).

Preston and de Waal (2002a) propose that at the core of the empathic capacity is a relatively simple mechanism that provides an observer (the "subject") with access to the subjective state of another (the "object") through the subject's own neural and bodily representations. When the subject attends to the object's state, the subject's neural representations of similar states are automatically activated. The more similar the subject and object, the more the object will activate matching peripheral motor and autonomic responses in the subject (e.g., changes in heart rate, skin conductance, facial expression, body posture). This activation allows the subject to understand that the object also has an extended consciousness, including thoughts, feelings, and needs, which in turn fosters sympathy, compassion, and helping. Preston and de Waal (2002b) and de Waal (2003) propose evolutionary continuity between humans and other mammals in this regard. Their Perception-Action Model (PAM) fits Damasio's (1994) somatic marker hypothesis of emotions as well as recent evidence for a link at the cellular level between perception and action (e.g,. "mirror neurons;" di Pelligrino et al. 1992).

The idea that perception and action share common representations is anything but new: it goes as far back as the first treatise on "Einf├╝hlung," the German concept later translated into English as "empathy" (Wispe 1991). When Lipps (1903) introduced Einf├╝hlung, which literally means "feeling into," he speculated about "innere Nachahmung" (inner mimicry) of another's feelings along the same lines as proposed by the PAM. Accordingly, empathy is often an automatic, insuppress-

ible process, as demonstrated by electromyographic studies of invisible muscle contractions in people's faces in response to pictures of human facial expressions (Dimberg et al. 2000). Accounts of empathy as a higher cognitive process neglect these "gut level" reactions, which are far too rapid to be under voluntary control.

Perception-action mechanisms are well known for motor perception (Prinz and Hommel, 2002), causing researchers to assume that similar processes underlie emotion perception (Gallese 2001; Wolpert et al. 2001). Data suggest that observing and experiencing an emotion involve similar physiological substrates (Adolphs et al. 1997, 2000), and that affect communication creates similar physiological activity in subject and object (Dimberg 1982, 1990; Levenson and Reuf, 1992). Recent investigations of neural mechanisms of empathy (Carr et al. 2003; Preston et al, 2002; Wicker et al., 2003; Singer et al. 2004; de Gelder et al, 2004) lend support to, or are at least consistent with, the PAM.

This "bottom-up" view was depicted as a Russian doll by de Waal (2003). Accordingly, empathy covers all forms of one individual's emotional state affecting another's, with simple mechanisms at its core and more complex mechanisms, cognitive filters, and perspective-taking abilities built on top. Autism may be reflected in deficient outer layers of the Russian doll, but such deficiencies most likely go back to deficient inner layers.

This is not to say that higher cognitive levels of empathy are irrelevant, but they are built on top of this firm, hard-wired basis without which we would be at a loss about what moves others. Thus, at the core of the Russian doll we find emotional contagion around which cognitive empathy and attribution are constructed. Cognitive empathy implies appraisal of another's predicament or situation (cf. de Waal,1996a). The subject not only responds to the signals emitted by the object but seeks to understand the reasons for these signals, looking for clues in the other's behavior and circumstances. Cognitive empathy makes it possible to furnish targeted helping that takes the needs of the other into account. These responses go well beyond emotional contagion, yet they would be hard to explain without an emotional motivational component.

Whereas monkeys (and many other social mammals) clearly seem to possess emotional contagion and some forms of targeted helping, the latter phenomenon is not nearly as robust as in the great apes. For example, at Jigokudani monkey park, in Japan, first-time mother macaques are kept out of the hot water springs by park wardens because of their experience that these females will accidentally drown their infants. They fail to pay attention to them when submerging themselves in the ponds (de Waal 1996b). This behavior is something they apparently learn to do over time, showing that they do not automatically take their offspring's perspective. Ape mothers, in contrast, respond immediately and appropriately to the specific needs of their offspring and are very careful to keep them away from water (personal observations).

In conclusion, empathy is not an all-or-nothing phenomenon: it covers a wide range of emotional linkage patterns, from the very simple and automatic to the very sophisticated. It seems logical to first try to understand the more basic forms, which are widespread indeed, before addressing the interesting variations that cognitive evolution has constructed on top of this foundation.

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