HEALTH

Relationship neuRoscience

Lane Beckes and James A. Coan

The study of interpersonal relationships is now a part of the burgeoning field of social neuroscience (cf. Coan, Beckes, & Allen, 2013; Coan, Schaefer,

& Davidson, 2006). Social proximity and close interpersonal relationships are critical for optimal human brain functioning (Beckes & Coan, 2011).

Positive relationships are now well known to benefit health and well-being (House, Landis, & Umberson, 1988; Holt-Lunstad, Smith, & Layton, 2010; Robles

& Kiecolt-Glaser, 2003; Uchino, Cacioppo, &

Kiecolt-Glaser, 1996; Uvnäs-Moberg, 1998). However, the neural mechanisms linking relationships to health and well-being are not well understood.

In this chapter, we review much of the latest research on the neural correlates of social relationships and attempt to integrate much of it into a set of basic principles. First, we discuss issues relating to neural modularity and the interpretation of neuroscientific findings. Second, we discuss how the brain manages self-representation, other-representation, and their overlap in neural circuitry. Third, we review and discuss the literature on behavioral systems and their instantiation in neural activity. Fourth, we out-line and discuss some proposed principles of rela-tionship neuroscience and briefly describe social baseline theory (SBT; Beckes & Coan, 2011). We conclude with proposals for the future of

relationship neuroscience.

MODULARITY AND INTERPRETATION A persistent problem in the neurosciences concerns the functional specificity of neural circuits (cf. Bunzl,

Hanson, & Poldrack, 2010; Fodor, 1983; Kanwisher, 2010). The oversimplified version of this debate pits those who believe the brain is composed of discrete functional modules against those who believe the brain is more functionally generalized in its design.

The question of whether specific psychological func-tions can be located in specific neural circuits has been a core debate in the brain sciences since the early 1800s (see Kanwisher, 2010). Perhaps the most egregious mistake one can make in interpreting brain data is to assume that whatever regions are active during a given psychological task are intrinsic to whatever construct one is exploring. Most readers have probably seen such inferential errors in popular press write-ups. For example, one article (Zinkova, 2009) suggested that “researchers have identified four regions of the brain that are believed to form the love circuit” (p. 1). These identified regions are asso-ciated with reward processing and are part of the dopamine-rich ventral striatum, but they are not part of a “love” circuit in any meaningful sense.

Despite these difficulties, much of the brain is at least weakly modular (cf. Kanwisher, 2010;

Karmiloff-Smith, 2010). For example, much of the processing of different sensory modalities is done in distinct regions of the brain. The difficulty arises when discussing higher order psychological con-structs, which are more likely to emerge out of the interaction of multiple neural networks. Emergence, in this context, refers to a relatively irreducible qual-ity that arises out of the interaction and integration of signals from multiple systems (as in a gestalt; see Coan, 2010b, for a detailed discussion). Activation

across such networks can frequently be understood as indexing processing that is critically related to a psychological construct. For example, theory-of-mind tasks consistently activate regions such as the superior temporal sulcus (STS; cf. Allison, Puce, &

McCarthy, 2000; Grossman & Blake, 2002; Pel-phrey, Morris, Michelich, Allison, & McCarthy, 2005; Morris, Pelphrey, & McCarthy, 2008) and the temporoparietal junction (Saxe & Kanwisher, 2003), even though it is unlikely that either the STS or the temporoparietal junction can be construed as theory-of-mind circuits per se.

It is important to emphasize that this problem of identifying the function of a given brain region and associating it with a specific conceptual process is difficult, rarely intuitive, and frequently impossible if one hopes to find one simple process that exists in either the psychological or the lay lexicon. Thus, we urge readers to keep in mind that functional descrip-tions of specific brain regions are approximadescrip-tions at best and subject to change with further evidence. A good example is the emerging understanding of the amygdala. Early investigations focused on its role in fear and fear conditioning (cf. Davis, 1992; Ledoux, 2000), with it often being referred to as the “fear center” in popular media (e.g., Walker, 2010).

Subsequently, it has been found to be sensitive to positive stimuli in some contexts (Hamann, Ely, Hoffman, & Kilts, 2002) and strongly associated with vigilance to ambiguous stimuli (Davis &

Whalen, 2001). More recently, Ralph Adolphs (2010) has marshaled compelling evidence that the amygdala is best characterized as sensitive to the biological relevance, salience, and value of stimuli, and it may be critical for determining the biological value of ambiguous stimuli. Thus, our understanding of the function of individual regions of the brain is ongoing and complex.

SELF-EXPANSION, SELF–OTHER OVERLAP, AND EMPATHY

Over the past decade, social neuroscience has taken on the question of how people understand the minds of others and how that understanding is related to the self (cf. Lamm, Batson, & Decety, 2007; Lamm, Meltzoff, & Decety, 2010; Singer &

Lamm, 2009; Singer et al., 2004; see also Keysers &

Gazzola, 2009). One of the interesting outcomes of this research is evidence that, during empathic tasks, the “self” and “other” are processed similarly and in regions implicated in processing social infor-mation more generally (e.g., Singer et al., 2006).

Such findings were anticipated by earlier research on relationships. For example, self-expansion theory (cf. Aron & Aron, 1996) posits that self-concepts and self-representations become more intertwined with people’s representations of others as they grow closer to them. In the following section, we explore research dedicated to understanding how the brain constructs the self, how the brain understands others, and how those two processes converge as relationships develop.

Self-Expansion and Self–Other Overlap in Relationship and Social Psychological Theory

Theorists have long argued that the self is at least partially defined by one’s social relationships (Andersen & Chen, 2002; Aron & Aron, 1996).

Self-expansion theory (Aron & Aron, 1996) sug-gests that love is the process or output of a motiva-tion to expand the self. The theory has largely been promoted as a heuristically useful metaphor that describes the intertwining of the self with the other in an intuitively accessible manner. Although aspects of the model lack formal specification and, therefore, falsifiability, it has inspired considerable research and has led to meaningful insights. Inspired by George Lakoff’s (Lakoff & Johnson, 1999) ideas regarding embodied metaphors, the model was designed as a heuristic for guiding research about how the self becomes entangled with others in mem-ory. In many ways, self-expansion theory presaged the explosion in embodiment research, which pro-vides evidence for the idea that people understand themselves, others, and the world through embod-ied cognitive and affective representations (cf. Dam-asio, 1999; Niedenthal, 2007). At its core, the model proposes three ideas:

1) people seek to expand the self, 2) one way they seek to do so is by attempting to include others in the self through close

relationships, 3) people seek situations and experiences that have become associ-ated with experiences of expansion of the self. (Aron & Aron, 1996, p. 49)

Aron, Aron, Tudor, and Nelson (1991) have found that close others are more likely to be treated like the self in resource distribution scenarios, and attributions for the self versus the other are more similar for close others. Furthermore, self–other confusion in memory is more common with close others (Aron & Fraley, 1999; Mashek, Aron, &

Boncimino, 2003). The Inclusion of the Other in the Self (IOS) Scale (Aron, Aron, & Smollan, 1992), which allows people to identify how close they sub-jectively feel to another by choosing one of a series of progressively overlapping circles, measures psycho-logical closeness quite well. It is, perhaps, the best measure of relationship closeness in predictive terms, with the possible exception of the Relationship Closeness Inventory (Berscheid, Snyder, & Omoto, 1989, 2004), an extensive self-report measure of closeness-related behaviors.

Although it is difficult to determine how the model could be tested neuroscientifically, Aron and Aron (1996) provided some general hypotheses that are promising in terms of advancing the understand-ing of self–other dynamics. For example, they argued that it is difficult to imagine why people would behave in truly altruistic ways toward others (i.e., sacrificing the self for another) unless one con-siders that self-expansion theory predicts that the other is a part of the self. In this sense, selfless acts are more likely given that the other person is simply an extension of the self. Testing such hypotheses would require operationalization of self–other over-lap or inclusion of other in the self that mapped onto neural activity to be useful for neuroscientists, but as we discuss, recent research on empathy is building some potential ways to test these ideas more directly.

We now discuss what is already known about the neural representation of the self and others.

Neural Representations of the Self

Many socially relevant brain processes are supported by neural substrates that represent the body, the subjective self, the agentic self, and the self’s various

feeling states, including emotions and sensations.

Two contemporary theories represent the state of the art in understanding the neural manifestation of the self, each of which is highly compatible with the other. In this section, we discuss Antonio Damasio’s (1994) somatic marker hypothesis and Bud Craig’s (2002, 2009) theory regarding meta-representation of the self in the anterior insular cortex (AIC).

Somatic marker hypothesis. This theoretical formulation of decision making and reasoning (e.g., Damasio, 1994; Bechara & Damasio, 2004) argues that emotion and affective states are a critical foun-dation for decision making. Emotions are created through unified changes in somatic states (physio-logical states of the body such as heart rate changes, musculoskeletal action, and endocrine release), the release of neurotransmitters and neuromodulators such as dopamine or serotonin, the activation of somatosensory maps in regions such as the insula, and the modification of signals being transmitted from the body to regions of the brain involved in somatosensory processing. Affective stimuli, accord-ing to this theory, are frequently distaccord-inguished as either primary or secondary inducers. Primary inducers elicit an automatic and obligatory somatic response in the individual and are innate response elicitors (e.g., food, snakes, soothing touch), learned elicitors such as conditioned stimuli (e.g., a type of food that has been associated with illness and vomit-ing), or stimuli of sufficiently strong affective value to warrant explicit knowledge (e.g., learning that your bank account has been cleared of money by an imposter). Secondary inducers are usually a memory or thought that elicits an emotional response, such as remembering a car accident or imagining learn-ing that one has a terminal illness. It is argued that states elicited by primary inducers are mediated through the amygdala, whereas secondary inducers are primarily associated with the ventromedial pre-frontal cortex (vmPFC).

In this formulation, information regarding pri-mary inducers is sent from sensory receptors to the amygdala through either sensory cortex or a more direct thalamic pathway. The amygdala sends this information to effector structures such as the hypothalamus, the ventral striatum, and brain stem

nuclei (e.g., the periaqueductal gray), which trigger changes in peripheral physiological systems such as muscles involved in facial expressions, approach or avoidance behaviors, and endocrine and cardiovas-cular systems. The somatic states induced by changes in the body are then signaled back to regions in the brain stem such as the parabrachial nucleus of the brain stem, which then relays somatic patterns to somatosensory-related cortices including the insula, primary and secondary somatosensory cortices, and cingulate cortex. Secondary inducers are generated largely by vmPFC, which can couple memories encoded in higher order association corti-ces with effector structures that initiate somatic states, such as the amygdala, and neural regions that process the somatic states, such as those in the brain stem (e.g., parabrachial nucleus of the brain stem) and cortical somatosensory regions (e.g., primary somatosensory cortex, insula).

The vmPFC plays a critical role in activating regions in the brain stem and hypothalamus, which act in turn to “rerepresent” or model the somatic states as they were originally experienced. This pro-cess, in which the peripheral effects are not occur-ring directly in the body, has been described as the as-if body loop. This as-if loop mimics the original somatic state, even in the absence of that state in the body. The vmPFC can trigger such as-if body loop processes to select for and attend to different alterna-tives for potential action. For example, the vmPFC can use memory to trigger somatic representations of the body from previous experiences, often in rapid succession, and use rerepresentations of earlier experiences to make decisions about appropriate responses given situational goals and constraints. In this way, emotional information is used to select responses to external stimuli and internal states, biasing and frequently improving decision making.

Anterior insula and human awareness. Bud Craig (2002, 2009) has presented a similar model, emphasizing insular cortex involvement in human awareness and self-representation. He notes that the posterior insula receives interoceptive informa-tion about the body (informainforma-tion about the state of the body, including heart rate, pain, temperature, etc.) and forwards it to the AIC to be integrated

with other sources of neural information. Subjective reports of bodily feelings are most strongly associ-ated with the AIC and the adjacent orbitofrontal cortex (OFC), suggesting that the insula contains a somatotopic rerepresentation or model of the body.

This rerepresentation can be influenced by a host of factors over and above those associated with sensory afferent information. Moreover, it is this integrated and modified rerepresentation of the body that is subjectively experienced in consciousness, which leads to a subjective sense of one’s body as one’s self.

One critical feature of the structural organization of the insula is its unique access to peripheral infor-mation as represented by a phylogenetically new afferent pathway from the brain stem (i.e., lamina I and solitary nucleus) to the insula, a pathway seen only in higher order primates. This pathway allows for a direct representation of the body’s homeostatic physiological state in the posterior insula. The mid-insula then creates a rerepresentation of the body state that includes representations of emotionally salient stimuli from higher cortical areas, the amyg-dala, the ventral striatum and nucleus accumbens, and the temporal pole. At this point, the self- representation in the amygdala includes the homeo-static state of the body, emotionally relevant environmental stimuli, and motivational impulses.

Finally, all salient information is rerepresented with the homeostatic conditions of the body, its fit in the environment (or the degree to which the individual is able to achieve goals and meet basic needs), important social features of the environment, and the person’s current motivational state in the AIC and the junction between the AIC and the frontal operculum. One can view all of this as a meta- representation of the self-in-context or, as Craig (2009) argued, a meta-representation of the

“global emotional moment” or “an image of ‘the material me’” (p. 67).

Self-in-context. Despite these insightful and useful accounts of the neural basis of the self, self- representation is likely to be highly context dependent, and elements of self-representation may be difficult, if not impossible, to extract from prevailing physical, psychological, and social circumstances. This idea should be familiar to

social psychologists, who study the social-cognitive underpinnings of the self. For example, Markus and colleagues (e.g., Markus & Kunda, 1986; Markus

& Wurf, 1987) have proposed that people hold working self-concepts that are sensitive to the cur-rent social environment. Thus, neural processing of the self may similarly shift as a function of context.

One context that has received much attention in the neurosciences is the self when threatened with or experiencing some sort of physical or social pain. As we discuss in depth shortly, this domain of research is particularly useful for making self–other compari-sons because threatening and painful contexts have been extensively explored both when individuals are the targets of threat or pain and when other people are the targets of threat or pain. The neural literature on empathy has provided a window through which self–other comparisons can be made within a spe-cific context. This context provides an opportunity for exploring the neural evidence for relationship theories that posit greater overlap in self and other representations as a function of closeness, inter-dependence, identification, or other social cues of similarity or group membership.

A common pattern of neural activity is typically identified during threat and pain (cf. Coan, Schaefer,

& Davidson, 2006; Dalton, Kalin, Grist, & Davidson, 2005; Price, 2000). This pattern includes subcortical and midbrain regions involved in motivation and affect, such as the periaqueductal gray, amygdala, putamen, caudate, hypothalamus, and thalamus; cor-tical regions involved in problem-solving, goal and motor planning, somatosensation, self-regulation, emotional processing, interoception, and rerepresen-tation processes in regions such as the OFC and vmPFC, anterior cingulate cortex, posterior cingulate cortex, insula, and superior, medial, and inferior frontal gyri; and parietal regions such as the angular and supramarginal gyri. These neural regions are activated by threats of shock and can be thought of as constituting a threat matrix. It is important to note that none of these regions processes threats exclu-sively. Each of these brain regions responds to a dif-ferent aspect of the threat, and most or all of them are involved in a host of non–threat-related processes.

Fascinatingly, many of the regions involved in responding to threat are also involved in processing

self-focus. Similar to threat responding, the self is a complicated concept that is not easily mapped onto a simple (or a single) neural substrate.

Despite this complexity, the models we have described give one some sense of what neural substrates might most closely match what psychol-ogists and philosophers often mean by the term the self. William James (1890) made a distinction between the “me” self, or the self as known, and the “I” self, or the self as knower. It is difficult to link James’s selves to neural substrates, but it is possible to think of the vmPFC and the AIC as representing two aspects of the self that directly relate to the distinction between the “I” and the “me,”

respectively. The vmPFC seems to act as a decision maker, a selector of actions. In a sense, this region can be thought of as a candidate region for a neu-ral “I” that acts on the world. The AIC, alternatively, represents the body and its fit in the environment and a sense of self that is most closely aligned with the “me.” More important, both of these conceptu-alizations of the self suggest that both the agentic self and the material self are rerepresentations that summarize the activity of distributed neural activ-ity related to a variety of interoceptive, motiva-tional, perceptual, affective, and cognitive processes. The neural processes and regions involved in these different representations of the self are critical in a variety of social and relationship-based cognitive, motivational, and affective pro-cesses. As such, it will be useful to consider how frequently areas involved in self-representation are also involved in the representation of close others and how closeness and other social factors change the degree to which contextualized representation is more or less similar between the self and other.

Neural Representations of Others Social perception has been studied in numerous ways by those using neuroscience methods. Here, we only briefly review social perception research.

Instead, we focus on the portions of the literature that are more directly applicable to self-expansion and related theories (e.g., Andersen & Chen, 2002;

Aron & Aron, 1996; Brewer & Gardner, 1996), which address the way in which self-representations

overlap with other-representations. We emphasize, however, that important ideas may also emerge from the social perception literature. Indeed, we would not be surprised if lower level social perception processes capture and explain important psychologi-cal and interpersonal dynamics that one might not expect to be linked to more basic social perception processes.

A tremendous amount of research has investi-gated how people understand the minds and inten-tions of others, an area of inquiry commonly called theory of mind (cf. Allison et al., 2000; Frith &

Frith, 1999; Saxe & Kanwisher, 2003). Multiple brain systems are involved in understanding the mental states of others, including the STS, which appears to decode biological motion and implied biological motion (e.g., Allison et al., 2000), and the temporoparietal junction, located in the same general region of the brain as the STS, which Saxe and Kanwisher (2003) have argued is involved in reasoning about the content of others’ mental states. Also involved is the amygdala, which is asso-ciated with emotional perception (e.g., Adolphs, 2002, 2010; Whalen et al., 2009) and determina-tion of the trustworthiness of others (Engell, Haxby, & Todorov, 2007; Koscik & Tranel, 2011;

Platek, Krill, & Wilson, 2009).

Allison et al. (2000) proposed a model of the neural control of social cognition in which the STS plays an early role in detecting biologically relevant cues and integrating object recognition with spatial location and movement (cf. Unger-leider & Haxby, 1994). The STS forwards this information to the amygdala and OFC, which determine the biological and affective value of the stimulus (cf. Adolphs, 1999). Subsequently, the PFC uses this integrated information to make decisions, deploy resources such as attention, and engage other systems in the brain (cf. Miller &

Cohen, 2001). This general-purpose theory of mind and social cognition network, however, is not the only system involved in social cognition or the process by which people understand the mental states of others. Indeed, another intensely studied system that appears to be critical in some instances of social cognition is an empathy net-work (cf. Singer & Lamm, 2009).

Neural networks supporting empathy. According to de Vignemont and Singer (2006), empathy occurs when

(i) one is in an affective state; (ii) this state is isomorphic to another person’s affective state; (iii) this state is elicited by the observation or imagination of another person’s affective state; (iv) one knows that the other person is the source of one’s own affective state. (p. 435)

It is important to note that there are other classes of affective and cognitive response to the affective states of others, including emotional contagion (Hatfield, Caccioppo, & Rapson, 1994), sympathy, empathic concern, and compassion. Empathic con-cern, sympathy, and compassion are all seen as lacking affective isomorphism (isomorphism refers to a similarity in form with a one-to-one match in individual components or elements), and emotional contagion occurs when the isomorphic emotional state is not attributed to the other person. Therefore, Singer and Lamm (2009) have argued that these types of processes do not constitute empathy in a strict sense. Most neuroscience investigations of these processes have focused exclusively on empathy.

Moreover, most studies on empathy have investi-gated empathy within a negatively valenced context.

A thorough reading of the literature suggests that most of these studies use either painful or threaten-ing stimuli applied to someone other than the par-ticipant to elicit empathic responses, or they show images of others expressing or experiencing pain or fear. A groundbreaking study by Tania Singer et al.

(2004) subjected participants and their romantic partners to a painful stimulus and then examined which regions of the participants’ brains were active when both they and their partners were in pain.

They found substantial spatial overlap in the neural response to self-pain and other-pain in regions typically associated with affective processing, including the AIC and the anterior cingulate cortex.

Additionally, they noted that the extent of activation in parts of this network was positively associated with participants’ self-reports of empathy. This finding, that many of the same brain structures

commonly activated in the firsthand experience of pain and threat are also active in vicarious

experience of pain and threat, has been replicated numerous times (e.g., Beckes, Coan, & Hasselmo, 2013; Lamm et al., 2007, 2010).

Subsequent research has begun to define the boundary conditions and generalizability of this effect. For example, children show the same pattern of empathic response as adults (Decety, Michalska,

& Akitsuki, 2008), and adults process the unusual pain of others (pain the participant has never expe-rienced personally) in these same general regions (Lamm et al., 2010). Despite this general pattern, Lamm et al. (2010) found that empathy for unusual pain elicited a weaker response in participants.

Other studies have found similarly weakened empathic responses to the pain in AIDS patients believed to have contracted the disease through ille-gal drug use (Decety, Echols, & Correll, 2010) and to the pain of others who are perceived to have behaved in an unfair manner in an economic game (Singer et al., 2006). Additionally, vicarious pain responses to displays of chronic pain are weaker than those to displays of acute pain (Saarela et al., 2007), and inferior parietal activations (e.g., supra-marginal and angular gyri) are greater for similar targets than for dissimilar targets.

State-of-the-art research has suggested that empathy is supported by shared networks of activ-ity, meaning that self-related processing occurs in very similar regions to other-related processing in situations that invoke an empathic response. Singer and Lamm (2009) argued for a dual-component-style model composed of subcortical regions that are involved in motivational affective processing, such as the amygdala or ventral striatum, and another component composed of areas involved in integra-tive and higher level processing (e.g., goals, intero-ception, planning) such as anterior cingulate cortex, OFC, prefrontal cortex (PFC), AIC, inferior and superior frontal regions, supplementary motor cortex, and somatosensory components (e.g., Singer

& Lamm, 2009). Interestingly, one of the few studies to investigate empathy in a positive context found that highly pleasant smells experienced vicariously are represented in the AIC and adjacent frontal operculum (Jabbi, Swart, & Keysers, 2007).

Self–other overlap. There are several ways to interpret the empathy literature in terms of support for psychological theories that argue for intertwin-ing self–other representations. First, however, it is important to note the interesting consistency with which other-threat activations are topographically similar to self-threat activations. To extend this observation further, the areas identified as self- relevant in the somatic marker hypothesis (Damasio, 1994) and Craig’s (2009) AIC self-representation theory are heavily included in those regions identi-fied as part of the putative empathy network (as well as the threat matrix). Indeed, the AIC is almost always detected as active in empathy studies dur-ing vicarious emotional experience. Does this mean that people are including others in the self when they are empathizing? Perhaps, but it is not so simple. Frequently, these results are discussed in terms of whether they represent simulation (cf.

Gallese & Goldman, 1998) of the state of others, an idea that is heavily debated (cf. Decety, 2011).

Complicating matters, there is ambiguity regarding what simulation even means. For example, it may be that the brain simply uses self-related processes, including embodied representations, to calculate or understand the current emotional state of others (Jacob, 2008) rather than actually treating others as if they were similar to, or an extension of, the self.

Additionally, the method used to identify overlap-ping brain regions in empathy tasks is more descrip-tive than quantitadescrip-tive. For example, the fact that the same brain region is recruited to process the self and others is not direct evidence for self–other overlap as is often meant in social psychological terms. Rather, it would be better evidence to find that not only the location of activity is similar but also the degree of activation is more similar within individuals in those regions when the other is a significant other than when the other is a random stranger. This would give stronger credence to the idea that people are treating close others as if they are the self than most studies to date can claim.

The current evidence suggests that this network of regions is involved in processing threat and pain in both the self and others but is not engaged when the other appears to be unworthy of empathy for one reason or another (i.e., selfishness or acting in