The physiology of empathy: Linking oxytocin to empathic responding
viii TABLE OF CONTENTS CHAPTER ONE: BACKGROUND 1 Distinguishing Empathic Concern and Personal Distress 2 Empathic Emotions 2 Empathy and Altruistic Helping 3 Arousal and the Physiology of Empathic Emotions 4 Conclusion 5 Oxytocin and How it Operates to Promote Empathy 6 Oxytocin in Response to Arousal 7 Oxytocin, Cognition, and Empathy 8 Oxytocin and Prosocial Behavior 11 Empathy and Oxytocin: Existing Studies 13 Conclusion 15 Current Research 15 CHAPTER TWO: STUDY 1 17 Study 1 Overview 17 Hypotheses 17 Methods 19 Results 25 Discussion 35 CHAPTER THREE: STUDY 2 39 Study 2 Overview 39 Hypotheses 40
ix Methods 41 Results 46 Discussion 58 Chapter 4: General Discussion 60 Study 1 Review 60 Study 2 Review 62 Strengths and Limitations 64 Implications 67 References 71
X TABLES Table 1: Study 1 intercorrelations 27 Table 2: Mean comparisons between donors and non-donors 28 Table 3: Regression: Empathic emotions predicting change in oxytocin... 31 Table 4: Regression: Trait empathy predicting change in oxytocin 33 Table 5: Study 2 mean comparisons between conditions 47 Table 6: Study 2 binary choice comparisons between conditions 47 Table 7: Study 2 intercorrelations 50 Table 8: Logistic regression analysis of condition by empathic concern interaction for altruism 52 Table 9: Logistic regression analysis of condition by personal distress interaction for altruism 53
xi TABLES FIGURES Figure 1: Study 1 design and procedures 20 Figure 2: Comparison of mean emotional ratings across conditions 26 Figure 3: Comparison of the mean change in oxytocin from baseline 30 Figure 4: Study 2 design and procedures 42 Figure 5: Donation size frequency by condition 48 Figure 6: Mean amount donated across treatment conditions for those high versus low in trait empathic concern 57
1 CHAPTER ONE BACKGROUND Why human beings help others, often at considerable costs to themselves, remains an enduring question that has been approached using science, philosophy, and religion. Although multiple motives may drive individuals to help others (e.g., Omoto & Snyder, 1995; Penner, Dovidio, & Schroeder, 2005), empathy has long been considered a key motivation (Eisenberg & Miller, 1987; Penner et al., 2005; for a review related to altruism see Batson, Ahmad, & Lishner, 2009; Piliavin & Charng, 1990). Broadly defined, empathy is an innate human capacity referring to the response of one individual to the experiences of another (Davis, 1996). Psychologists have suggested that empathy is an affective and cognitive phenomenon with physiological correlates (e.g., Eisenberg, Valiente, Champion, & Miller, 2004). Researchers have identified the hormone oxytocin as a potential physiological correlate of empathy (Rodrigues, Saslow, Garcia, John, & Keltner, 2009; Reyes & Mateo, 2008; Singer Snozzi, Bird, Petrovic, Silani, Heinrichs et al, 2008; Zak, 2008; Zak, Stanton, & Ahmadi, 2007). This dissertation furthers this suggestion by explicitly outlining and testing the relationship between empathy and oxytocin (OT). It is hypothesized that OT is an important part of the physiological process involved in the empathic response, including the subjective experience of distinct empathic emotions - empathic concern and personal distress- as well as subsequent prosocial behaviors (behaviors that are directed for the benefit others) associated with these emotions. Likewise, individual differences in dispositional empathy may reflect variations in oxytocinergic system functioning. If this is correct, it is possible that experimentally
2 augmenting OT levels may lead to greater OT-induced behavior for those high in dispositional empathy to a greater degree than those lower in empathy. This dissertation takes into consideration that there are different concepts encompassed by the term empathy by reviewing and making predictions specific to distinct empathic emotions. From Arousal to Emotion to Helping: Distinguishing Empathic Concern and Personal Distress People are affected by the suffering of others to the degree that they will at times act upon those feelings at a considerable cost to themselves. Indeed, there is no other outcome of empathy that has received as much attention from researchers and theorists as helping (e.g., Batson, 1991; Batson et al., 2009; Davis, 1996). Empathy serves as a motivational source for helping others (e.g., Batson & Oleson, 1991; Eisenberg & Miller, 1987; Penner et al., 2005; Dovidio, Piliavin, Schroeder, & Penner, 2006). In order for people to be empathically motivated to help, they have to first become aware of the need of others for help (e.g., Dovidio, 1984; Dovidio, Piliavin, Gaertner, Schroeder, & Clark, 1991). Awareness can come from witnessing distress in others, which is physiologically arousing for the observer (Dovidio et al., 1991; Piliavin, Dovidio, Gaertner, & Clark, 1981). However, witnessing others in distress can lead to two distinct empathetic emotional responses in humans (Batson, Fultz, & Schoenrade, 1987): feelings of self- focused personal distress and other-focused feelings of empathic concern (feelings of compassion, tenderness, and sympathy). Empathic Emotions Empathy as personal distress, or empathic distress, is typically referred to as an aversive state brought on by witnessing an aversive state in another (Batson, 1991; Davis,
3 1983; 1996). Personal distress is also described as a collection of aversive feelings (e.g., worry, anxiety, discomfort) that are focused on the self (e.g., Batson, 1991; Davis, 1996). Psychologist William McDougall (1926) referred to this state as "sympathetic pain"- an immediate reaction to the aversive emotional state of others that (when experienced) is identical or similar in state. Personal distress serves as a motive to reduce one's own negative state either by avoiding the source of the distress or, when that is not possible, by acting on behalf of others to reduce their aversive state. Whereas personal distress is primarily a self-focused affective or emotional state, the second form of empathy is an other-focused emotion that is ultimately felt for another person (Batson, 2009; Batson et al., 2009). Deriving from the "parental instinct," empathic concern generates an impulse to protect others and is perhaps the "root of all altruism" (McDougall, 1926). Empathic concern involves an active attempt to place oneself inside the other, versus passively experiencing another's state (Davis, 1996), as is considered to be the case with personal distress. Many refer to this affective state as compassion (also "pity," "sympathy," and "empathy," see Batson, 2009), which is classified as one of the virtues of humanity (Peterson & Seligman, 2004) and resides in the family of moral emotions (Haidt, 2003). Empathic concern allows humans to overcome the potential for self-focused considerations in turn for other-oriented concerns when presented with the plight of others. Empathy and Altruistic Helping The empathy-altruism hypothesis is helpful in understanding how the two distinct reactions to the needs of others affect a person's motivations to help (e.g., Batson, 1991; Batson & Oleson, 1991). The empathy-altruism hypothesis states that when a person
4 becomes aware of another's distress the perceiver may experience two distinct affective reactions similar to personal distress and empathic concern. These affective states lead to divergent motivations to help others- the former to reduce the arousal (or distress) elicited by the other (egoistic motivation), and the latter to reduce the need of the other (altruistic motivation). Among the vicariously distressed, those who can easily escape the arousing situation will do so (either psychologically or physically) when it is less costly than staying involved (Batson, 1987). On the other hand, a perceiver who reacts with concern would find it difficult to disengage without relieving the other's distress, directly or indirectly. Research testing the empathy-altruism hypothesis has generally been supportive while refuting alternative explanations and competing hypotheses (Batson et al., 1981; Batson et al., 1983; Batson et al., 1988; Batson et al., 1989; Batson et al., 1991; Batson et al., 1997; Batson & Weeks, 1996; Dovidio, Allen, & Schroeder, 1990; Schroeder, Dovidio, Sibicky, & Matthews, 1988). Arousal and the Physiology of Empathic Emotions Eisenberg and colleagues have investigated how physiologic arousal leads to and distinguishes these distinct empathic emotions. This body of work supports the notion that those who become physiologically overaroused experience personal distress, and become motivated to address egoistic concerns (e.g., Eisenberg & Fabes, 1990; Eisenberg et al., 2004; Hoffman, 1981). Alternatively, those who are aware of distress in others and are able to regulate the arousal that arises from it are likely to experience empathic concern (i.e., sympathy; Eisenberg & Fabes, 1990). Studies by Eisenberg and colleagues have found physiological correlates of empathic concern and personal distress based on autonomic activity, particularly heart
5 rate and skin conductance, which are indexes of physiological arousal. These studies find that increased heart rate and skin conductance are associated with viewing distressing segments of films (Eisenberg & Fabes, 1990; Eisenberg, Fabes, & Clark, 1991; Eisenberg et al., 2004). In addition, skin conductance tends to be positively related to self-reported distress (Eisnberg, Fabes, Schaler, Miller, et al., 1991) and indices of facial distress observed in the participant (Eisenberg, Fabes, Schaller, Carlo, & Miller, 1991). Empathic concern, on the other hand, is associated with a lower heart rate (Eisenberg et al., 1988) and greater heart rate variability. Those with higher heart rate variability are found to be more responsive to affective stimuli, but are also likely to have the regulatory skills necessary to modulate arousal (Fabes, Eisenberg, & Eisenbud, 1993; Eisenberg, Fabes, Schaller, & Carlo, 1991). In other words, it is not that those with greater heart rate variability were less reactive to the stimulus, but that they were able to attenuate their response to the arousing stimulus once it occurred. This work by Eisenberg and colleagues directly links to the work of Batson and colleagues who found that those who are able to down-regulate arousal are also those who are likely to engage in prosocial behavior (e.g., Eisenberg et al., 1989; Eisenberg et al., 1990; Fabes et al.; 1994; Fabes et al., 1993; Holmgren, Eisenberg, & Fabes, 1998). Conclusion Two distinct affective reactions to the perception of distress in others are identified in the literature. Although both are likely to elicit helping behavior, personal distress and empathic concern lead to differing motivations and consequences for helping (Batson, 1991; Eisenberg & Fabes, 1990). Physiologic arousal from observing distress in another is greater in the subjective experience of personal distress than with empathic
6 concern (see Eisenberg & Fabes, 1990; Eisenberg et al., 2004). If a person is aroused by the experience (especially the suffering) of another, and it is not attenuated, increased physiological stress may lead to an aversive affective reaction to another's plight, eliciting a more self-focused emotional, and perhaps behavioral, response. Oxytocin and How it Operates to Promote Empathy A hypothesis of the current studies is that oxytocin is involved in shifting people from self-focused feelings to feelings focused on others, thereby facilitating prosocial behavior. Oxytocin (OT) is a neuropeptide that is directly synthesized in the hypothalamus and projects to brain areas such as the amygdala and into the central nervous system (Sofroniew, 1983). OT is believed to be involved in a range of social behaviors via down-regulation of the avoidance/attack response and the induction of reward and learning of "approach" behaviors (see Carter, 2003; Insel & Young, 2001). In animal studies, OT has been found to be a crucial component of the mammalian attachment system, causally supporting the costly care of offspring (for reviews see Carter, 2003; Insel, 1997; Insel & Young, 2001; Keverne & Curley, 2004). Likewise, care for offspring is believed to have been the basis of human altruism and empathy (e.g., Batson, Ahmad, & Lishner, 2009; de Waal, 2008; Preston & de Waal, 2002; Sober & Wilson, 1998). The research presented next supports a link between oxytocin and empathic concern by arguing that oxytocin a) reduces social distress, b) enhances perspective- taking (also see Zak & Barraza, 2009), and c) promotes a key outcome of empathic concern- prosocial behavior.
7 Oxytocin in Response to Arousal McDougall (1926) proposed that the instinct of tender emotion is the strongest of all instincts, overriding even people's instinct for fear. Whether people experience distress or concern in response to distress in others may partly be determined by physiological events. Aversive arousal serves as a catalyst to draw attention to the state of another. In turn, oxytocin is released into the bloodstream when low to moderate levels of Cortisol (a hormone associated with stress and arousal) are present (Jezova et al., 1995). Oxytocin has a stress-reducing effect strongly supported in the animal literature (see Carter, 1998). This anxiolytic effect is believed to be the result of the interaction of oxytocin and amygdala activation and down-regulation of hypothalamic-pituitary-adrenal (HPA) response to stress (e.g., Carter, 1998; Henry & Wang, 1998). Moreover, administration of exogenous oxytocin leads to reduced basal and laboratory-induced levels of stress hormones such as Cortisol (e.g., Bartz & Hollander, 2006). The 'tend and befriend' stress model proposed by Taylor and colleagues (Taylor, 2006; Taylor et al., 2000) describes the role of OT in attenuating stress by outlining behavioral outcomes. The model states that women on average respond to stress in a physiologically (and in turn behaviorally) different manner than men, exhibiting more approach/nurturing behaviors than the withdrawal/aggressive behaviors typically elicited by a fight or flight response. This process relies on oxytocin inhibition of both Cortisol and hypothalamic-pituitary-adrenal axis activation. Specifically, when women are presented with a stress-inducing stimulus, such as the awareness of a child's distress, a cascade of stress responses occurs whereby oxytocin attenuates the actual stress experienced. This process not only inhibits the avoidance-aggressive behaviors
8 instigated by Cortisol, but also encourages nurturing and affiliative behaviors toward those in danger. Although the model identifies gender differences in relation to stress, these differences are based physiological events that, although more likely to occur in women, are ones that occur in both men and women. A number of studies indicate that oxytocin attenuates a person's response to distressing stimuli by reducing amygdala activation. Humans receiving intranasal OT infusion (versus placebo) show a significant reduction in amygdala activation when viewing faces expressing fear and distress (Kirsch et al., 2005). This effect is more pronounced for social stimuli (faces) than in other types of images (i.e., threatening non- social scenes, shapes). OT infusion is also found to attenuate amygdala activation to social stimuli that have been conditioned with an aversive shock (Petrovic, Kalisch, Singer, & Dolan, 2008), and to signals of social non-cooperation in an economic game (Baumgartner et al., 2008). What these studies tell us is that OT not only reduces the impact of distress, but this effect may be especially pronounced for social stimuli. Oxytocin, Cognition, and Empathy In addition to the affective forms of empathy, empathy has also been viewed as a cognitive event where a person is able to imagine the feeling state of the other, without sharing the particular state themselves or simply feeling for the person (e.g., Davis, 2005; Wispe, 1986). Davis (1983) describes the process of placing oneself in the shoes of the other as perspective-taking. Although cognitive empathy is not in itself emotional, the natural response of individuals when they place themselves in the other person's perspective is to experience empathic concern towards them (see Davis et al., 2004). For instance, asking research participants to place themselves in the shoes of others (i.e.,
9 perspective-taking) is widely used to elicit empathy toward others (for a review, see Batson, 1991). Perspective-taking has been found to increase empathy for people belonging to different stigmatized social groups like the homeless, persons with AIDS, and drug users (e.g., Batson et al., 1997; Batson et al. 2002). Perspective-taking instructions have also been found to decrease brain activity in pain regions when witnessing pain in others (Lamm, Batson, & Decety, 2007), possibly enhancing the likelihood of experiencing concern versus distress. Oxytocin may facilitate the processing of social information that is required in perspective-taking. Research indirectly supports this view, finding that OT improves social memory, recognition, and emotional regulation of social information, which is discussed next. Domes and colleagues (2007) tested if OT affected the ability to read another person's affective state. The "mind reading" task included 36 pictures of the area surrounding the eyes of different persons expressing various affective states. When given OT intranasally, participants were able to accurately identify the emotional states of others more so than when given placebo. Additionally, people given an OT infusion have been found to spend more time gazing toward the eye region of a face (Guastella, Mitchell, & Dadds, 2007). Interestingly, work by Eisenberg and colleagues finds that people tend to avert their gaze when experiencing distress, but not empathic concern (Eisenberg, Fabes, et al., 1988; Eisenberg, McCreath et al., 1988; Guthrie et al., 1997). As described earlier, Kirsch and colleagues (2005) found that OT infusion reduced amygdala activity related to processing fearful stimuli. In a related study, Petrovic et al. (2008) found a similar effect, whereby an OT infusion group showed less amygdala activation to faces conditioned with an electric shock than a placebo group.
10 This study added to the previous study by comparing social face information (direct gaze of the person in the photograph) versus non-social face information (averted gaze of the person in the photograph) and rating the likeability of that face before and after shock conditioning. As predicted, likeability ratings were lower for the faces paired with shock. Differences elicited by aversive conditioning were eliminated after OT treatment, but no such improvements were seen in the placebo group over the same time. Oxytocin is important for linking social signals to cognition and behavior (Insel & Ferland, 2004). For instance, mice that do not have the gene for OT receptors appear to have social amnesia- behaving toward familiar mice as if they were unfamiliar (Ferguson et al., 2000). This has led some to believe that OT may be involved in an array of social disorders such as autism and social phobia (see Bartz & Hollander, 2006). Research shows that OT infusion improves the retention of social information from an emotional processing task (Hollander et al., 2007) and increases interaction and feelings of trust (Andari, Duhamel, Zalla, Herbrecht, Leboyer, & Sirigu, 2010) for individuals with autism and Asperger's disorders. Additionally, in healthy males OT infusion has been found to increase recognition of faces (Savaskan et al., 2008). The process of inferring the mental state of others is believed to promote the experience of empathic concern (e.g., Batson, Early, & Salvarani, 1997; Davis, 2005; Davis et al., 2004; Lamm, Batson, & Decety, 2007). There is evidence that OT may enhance other-focusing. While OT reduces the effects of fear and fear conditioning of social stimuli (faces), OT also increases retention, perhaps through increased attention, of social information. OT may therefore be involved in the processing of social information
11 without being impeded by distressing stimuli, thus enhancing the likelihood of exposure to the suffering of another. Oxytocin and Prosocial Behavior Prosocial behaviors are "acts that are defined by some significant segment of society and/or one's social group as generally beneficial to other people" (Penner et al., 2005). In other words, a behavior that is prosocial is one whose outcome is generally positive to another person. Studies of human behavior in variants of the prisoner's dilemma (e.g., trust, ultimatum, dictator game) have revealed that oxytocin (OT) directly promotes prosocial behaviors including engaging in behaviors requiring trust, reciprocity, sacrifice (Kosfeld, et al., 2005; Morhenn, et al., 2008; Zak et al., 2004; 2005), and generosity (Zak et al., 2007). Participants who were given intranasal oxytocin were twice as likely to trust a stranger with all of their money in an economic cooperation game (trust game) than those receiving placebo (Kosfeld et al., 2005). Endogenous oxytocin release is also associated with reciprocity after trusting behavior is shown. Participants who received a signal of trust from a partner in an economic game showed 41% higher levels of plasma OT than those who did not receive such a signal, and this increase in OT was also positively correlated to the amount returned (reciprocated) to the trusting partner (Zak et al., 2005). The intranasal infusion of OT was found to raise the number of generous offers (offers above the minimally accepted range) by 80% over placebo in a A study using the ultimatum game (Zak et al., 2007). The ultimatum game is a decision task where two people can choose how much to cooperate with one another. Player 1 is given a sum of money and Player 2 is informed of the amount. Player 1 is asked to decide how much of the money will be shared with Player 2; however, Player 2 has the option of rejecting the offer, in which case neither player receives anything. As Player 1, participants decide how much money they will
12 Some research has found that touch during interactions may serve to communicate empathic concern (compassion) to an interaction partner (Hertenstein et al., 2006). Interestingly, touch has been found to promote both OT release and costly reciprocity. In an experiment testing the association between human touch, OT release, and subsequent behavior, participants received a 15-minute back massage by licensed massage therapists. Relative to a rest control group, those in the massage group had a 16% increase in OT relative to baseline, on average, and returned 243% more money to those who trusted them (Morhenn et al., 2008). Moreover, the change in OT predicted the degree of monetary reciprocity. These studies provide direct evidence that OT is positively associated, and perhaps causally, to at least money-based prosocial behaviors. It is possible that OT rewards, and thus motivates, engagement in prosocial behaviors associated with empathy (Zak & Barraza, 2009). Apart from reducing social anxiety, OT may motivate prosocial behaviors via neural reward systems that positively reinforce these behaviors (e.g., Bartels & Zeki, 2004; Insel & Ferland, 2004). Oxytocin is an element in opioid systems, which are responsible for developing and maintaining social dependencies and attachment (Panksepp et al., 1980). OT is found to co-release with dopamine in brain regions associated with reward (Liu & Wang, 2003), which likely reinforces interpersonal bonds. transfer to Player 2, and as Player 2 how much is the minimum amount they would accept from Player 1. The amount an individual gives as Player 1 minus their minimum acceptance as Player 2 is defined by the authors as generosity (Zak et al., 2007).
13 Empathy and Oxytocin: Existing Studies Three studies can be identified that closely relate to this proposed relationship between empathy and oxytocin. The first was a study conducted by Silvers and Haidt (2008) testing for a relationship between oxytocin and another moral emotion, moral elevation. Moral elevation is the positive and uplifting emotional response to witnessing good deeds which, as with empathy, promotes prosocial behavior. The authors exposed women who nurse their baby to morally elevating film clip of a musician paying tribute to his mentor. Because of OT's direct relationship with milk let-down, lactation was used as a proxy for OT release. In comparison to a comedic clip of comedian Jerry Seinfeld, the researchers found that women who watched a morally elevating video were more likely to lactate as well as hug and nurse their infant than those who viewed a positive control video. Although the study did not measure OT release directly, this study provides preliminary evidence that OT is associated with exposure to (and experience of) morally emotional stimuli. Singer and colleagues (2008) set out to test directly the effects of OT on the experience of empathy and engagement in prosocial behavior in an fMRI study. This study used the empathy-for-pain paradigm in which participants see either their romantic partner's hand or experience their own hand receiving a painful shock while undergoing functional brain imaging. Twenty male participants received either an OT or a placebo infusion intranasally prior to the pain procedure. A task in which participants are able to earn more money if they are willing to trust another to reciprocate (the trust game) was used to assess prosocial behavior. The authors found no support for the hypothesis that OT affected brain activation in regions previously found to be associated with empathy
14 (especially the anterior insula which is associated with the affective experience of pain) as defined by shared activation in self-experienced pain and other-experienced pain conditions. Moreover, no support was found for the hypothesized links between OT, or an empathic brain response (greater anterior insula activation), to subsequent prosocial behavior in the trust game. The conclusion based on these findings that OT does not promote empathy would be premature at best. The definition used by Singer and colleagues for empathy is extremely narrow (an affective state that is similar to the other person's observed state; see also Vignemont & Singer, 2006), thus not addressing other concepts that are identified by the term empathy, like empathic concern. In addition, the main author herself (see Singer & Lamm, 2009) has noted that reliance on empathy-for-pain paradigm makes empathy indistinguishable from related phenomena like emotional contagion and personal distress. Moreover, using shared brain activation (and mainly in one particular region) as the only measure of empathy does not address the subjective experience of empathy. Most relevant to the dissertation, researchers have tested the relationship between the oxytocin receptor polymorphism (rs53576) and empathy in a general population (Rodrigues et al., 2009). People with the homozygous GG of rs53576, compared to individuals with the one of the other two combinations AA or AG, have been found to exhibit greater ability to in the "Reading the Mind in the Eyes" test, a measure of empathic accuracy. Moreover, GG individuals score higher in a composite of dispositional empathy using Perspective-Taking, Empathic Concern, and Fantasy subscales of the Davis (1983) Interpersonal Reactivity Index. Speculatively, this study