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Psychoanalytic Psychology 2010, Vol. 27, No.

4, 410 441

2010 American Psychological Association 0736-9735/10/$12.00 DOI: 10.1037/a0019510

ATTACHMENT IS ABOUT SAFETY AND PROTECTION, INTERSUBJECTIVITY IS ABOUT SHARING AND SOCIAL UNDERSTANDING
The Relationships Between Attachment and Intersubjectivity
Mauricio Cortina, MD
Attachment and Human Development Center, Washington School of Psychiatry, Washington, DC

Giovanni Liotti, MD
Association for the Research of Attachment and Development, Rome

The relationships between intersubjectivity and attachment are beginning to be explored within the psychoanalytic and developmental literature. We contribute to this comparative effort by exploring the different evolutionary origins of attachment and intersubjectivity. Five interlocking themes are central to this article. First, from an evolutionary perspective, attachment and intersubjectivity serve different functions. The main function of attachment is to seek protection, whereas the main function of intersubjectivity is to communicate, at intuitive and automatic levels, with members of the same species and to facilitate social understanding. Second, to survive in changing and highly competitive environments, an evolutionary strategy emerged among our human ancestors based on developing high levels of cooperation within small bands of hunters and gatherers. In turn, high levels of cooperation and social complexity put selective pressures toward developing effective modes of communication and more complex forms of social understanding (mindreading/ mentalizing/intersubjective abilities). These abilities far surpass mindreading abilities among our closest Great Ape relatives. Third, we provide further evidence for this hypothesis showing that in comparison with other Great Apes, young children show qualitatively different levels of collaboration and altruism. Fourth, we provide an overview of the development of attachment and intersubjective abilities during the rst 2 years of life that support the hypothesis of a cooperative origin of intersubjectivity. Fifth,

Mauricio Cortina, MD, Attachment and Human Development Center, Washington School of Psychiatry, Washington, DC; Seminario de sociopsicoanalisis, A.C. Mexico City, Mexico; Institute for Contemporary Psychotherapy and Psychoanalysis, Washington, DC; Giovanni Liotti, MD, Association for the Research of Attachment and Development, Rome. Correspondence concerning this article should be addressed to Mauricio Cortina, 8737 Colesville Road, Suite 303, Silver Spring, MD 20910. E-mail: mauriciocortina@starpower.net

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we return to the main theme of this article showing three ways in which attachment and intersubjective abilities can be distinguished. We conclude by exploring some clinical implications of this cooperativeintersubjective model of human development. Keywords: attachment, intersubjectivity, cooperation, motivation, group selection, cultural evolution

The Relations Between Attachment and Intersubjectivity


Theories in regard to attachment and intersubjectivity developed independently from each other as can be seen in the classic contributions on attachment (Ainsworth, Blehar, Waters, & Wall, 1978; Bowlby, 1969/1982, 1973, 1980) and on intersubjectivity (Aron, 1996; Attwood & Stolorow, 1984; Benjamin, 1992; Ogden, 1994; Stern, 1985). Several authors have begun to approach the relation between attachment and intersubjectivity (Cortina, 2008; Diamond & Marrone, 2003; Fonagy, 2001; Fonagy, Gergely, Jurist, & Target, 2002; Fonagy & Target, 2008; Gergely & Unoka, 2008; Jurist, 2008; Lyons-Ruth, 1999, 2006; Stern, 2004; Stern et al., 1990). Three distinct approaches can be discerned.

Is Mentalization Intrinsic to the Attachment System?


The rst approach, taken by Fonagy and his collaborators (2001), revises the classic formulation of the function of attachment as protection in moments of danger to a mentalizing function (we use the terms advanced intersubjective abilities, mindreading abilities, mentalizing functions, metacognitive monitoring, and theory of mind (ToM) more or less interchangeably).1 Bateman and Fonagy dene mentalizing as the ability

We think concepts of theory of mind (ToM), metacognitive monitoring, mentalization or mindreading abilities, and advanced intersubjective abilitiesthat have different research and intellectual originsare nonetheless all pointing to the same basic phenomena, namely the ability to read the intentions, emotions, and goals of others and the ability to observe and reect on ones own internal experience. This is less obvious with ToM that has a strong cognitive slant and is measured by the use of false-belief tasks. Here is a simple example of a false-belief task (Hrdy, 2009, p. 136). Ask a 2- to 5-year-old that is sitting in mothers lap to watch carefully while setting a cookie on a table. Then ask the mother to close her eyes and then hide the cookie in your lap. With mothers eyes still shut, now ask the child where his mother thinks the cookie is. Typically developing 3- and 4-year-old children will answer that the mother will look in your leg. Almost all 5-year-olds are able to put themselves in their mothers place and say she will look for the cookie on the table (for review, see Wellman, Cross, & Watson, 2001). In the past few years, several studies show that young children can pass false-belief tests if they do not rely on languagelanguage may have a causal role in ToM development (Astington & Jenkins, 1999; Lohmann & Tomasello, 2003). These nonverbal tests elicit childrens spontaneous responses (as opposed to elicited responses that use language) and are based on anticipationlooking tasks and violation-of expectation tasks that operate on the principle that infants and young children will look longer at an event that violates their expectations. Based on these nonverbal tests, it is clear that by the second year of life typically developing children can pass false belief tests (for review, see Scott & Baillargeon, 2009). Using another experimental design that builds on infants desire to help others, Butterman, Carpenter and Tomasello (2009) demonstrate that 18-month-old infants clearly can understand false beliefs. Recognizing that ToM has a developmental progression has made it possible to begin to align ToM research with developmental intersubjective theories (Beebe, Knoblauch, Rustin, & Sorter, 2005; Benjamin, 2004; Lyons-Ruth & Jacobvitz, 1999; Stern, 1985, 2006; Trevarthen, 1980; Trevarthen & Hubley, 1978) and with theories of mentalization that are also developmental (Fonagy et al., 2002)but see Gergely and Zsolt (2008) for a different point of view that sees mentalization as an innate social-cognitive evolutionary adaptation that emerges by 12 months of age.

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to understand the intentions, goals, and emotional states of self and others (Bateman & Fonagy, 2004). According to Fonagy (2001):
. . . . . . the early relationship environment is crucial not because it shapes the quality of subsequent relationships (for which evidence is lacking, as we have seen) but because it serves to equip the individual with a mental processing system that will subsequently generate mental representation, including relationship representations. The creation of this representational system is arguably the most important evolutionary function of the attachment to the caregiver. Adopting this perspective helps redress the prevailing bias against the centrality of the family as the major force in socialization, but it also shifts the emphasis from content of experience to psychological structure or mental mechanisms and involves expanding on current ideas of the evolutionary function of attachment. (our italics, p. 31)

Contrary to what Fonagy asserts, there is some very good longitudinal evidence showing the effects of the early attachment relation on subsequent relations (Sroufe, Egeland, Carlson, & Collins, 2005). Yet, our main disagreement with Fonagy is his revision of attachment theory as serving a primary function of being able to read the minds of others (the mentalizing function). Fonagy does not deny the protective function of attachment, but he moves in the direction of making attachment theory into a theory of mental representations of attachment-based relations. It is the case that the ability to develop coherent representational models of the attachment relation is one of the most important outcomes of a secure attachment history in humans. It is also the case that the nature of these representational models strongly predicts the quality of attachment that person will develop with their offspring (Fonagy, Steele, & Steele, 1991). However, this does not mean that intensive parental care and the formation of attachment bonds emerged during the course of evolution to have coherent representations of attachment relations. Many mammals, like mice, exhibit vigorous attachment behaviors yet lack sophisticated representational models of attachment relationships. Even primate species, like the baboons, with a complex social life, lack full-blown mindreading abilities of humans that allow them to understand attachment behaviors of juveniles from their perspective (Cheney & Seyfarth, 2007). Here is an example based on an observation that the authors dubbed the Lord of the Flies incident (pp. 163164). Annual oods in the Okavanga Delta in Botswana produce islands. Baboons have to swim to get around the ooded areas. Adult baboons carry the juveniles who cannot swim on their backs. On one occasion, the adults crossed to another island, leaving almost all the groups juveniles behind. Not surprisingly, the juveniles found this separation very distressing, and they gave agitated bark and scream calls that signal separation distress and huddled together at night. To the consternation of the research team, the adult baboons heard the calls and looked toward the juveniles, but except for one baboon, none answered the calls nor made an effort to swim back to get the juveniles (the danger is real because lions often take advantage of these situations). The authors interpretation is that baboons do not appear to understand that their knowledge and abilities are different from someone elses (p. 165). This observation should serve as a cautionary tale suggesting that what constitutes an adaptive attachment system in one species might look quite different in other species. This is particularly so for humans, in whom intersubjective forms of communication are much more complex and sophisticated than in other primate species, a point that we elaborate in this article.

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More recently, Fonagy and Target (2008) seem to have modied their position by noting that in cases of trauma produced by attachment gures, the attachment system and mentalizing abilities operate in an inverse relation. That is, a hyperactivation of the attachment system induced by trauma dramatically reduces the capacity for mentalizing functions. They point to an article by Arnsten (1998) that helps explain the neurobiological basis for this inverse relationship. The attachment system and the mentalizing abilities might be associated with a bimodal reaction to stress that turns on some parts of the brain and peripheral nervous system while turning off others. During conditions of uncontrollable stresslearned helplessness induced by trauma is an example catecholamine neuromodulators (dopamine, norepinephrine, and epinephrine) are released in the central and peripheral nervous system. In the central nervous system, these catecholamines turn on the amygdala and turn off the prefrontal cortex. In the peripheral nervous system, the heart and skeletal muscles are turned on and the stomach is turned off to prepare for ght or ight. Fonagy and Target note that the attachment system is closely associated with the subcortical right brain structures, whereas mentalizing activities are linked to the prefrontal cortex and left brain. Supporting the latter, recent evidence in 4- to 6-year-old children engaged in false-belief tasks shows increased neural activity in the prefrontal cortex as measured by recording surface electrical activity in the brain of those children who pass false-beliefs tests correctly, but not in children who do not (Liu, Saggagh, Gehring, & Wellman, 2009). Although Fonagy and Target dont say so explicitly, all this would support the view that the attachment system and mindreading abilities are functionally, physiologically and anatomically distinct systems. Gyorgy Gergelywho had collaborated with Fonagy and others in a previous book supporting a strong view of the causal and functional connection between attachment and mentalizing function (Fonagy et al., 2002) has now taken the position similar to ours that attachment and intersubjective mentalizing abilities are functionally and developmentally distinct but interrelated systems (Gergely & Unoka, 2008). Without denying that in some situations, such as the case of attachment-related trauma, there are very clear adverse effects on mentalizing functions, Gergely and Unoka dispute the view that there is an inherent, causal and functional link between the quality of infant attachment on one hand, and the development of the ability for mindreading on the other (p. 51). In support of this view they note that the correlation between secure attachment and higher-order mentalizing activitiesas measured in theory of mind tasks using the false-belief testing paradigmare not very robust. They also note that there are many developmental factors that strongly predict false-belief understanding by age four that have little or no connection to attachment. For instance, there is strong longitudinal evidence showing that language has a causal role in theory of mind development (Astington & Jenkins, 1999; Lohmann & Tomasello, 2003). There is also evidence showing that complementary role playing, or the frequent use of words to name feelings used in some families (Cutting & Dunn, 1999), or that having older siblings (Ruffman, Perner, Naito, Parkin, & Clements, 1999) also facilitate theory of mind development. All this supports the view that intersubjective mentalizing abilities have a line of development that is independent from (but intertwined with) the development of secure or insecure attachment relationships. In sum, we completely agree that in cases of trauma involving attachment gures, there is a collapse of mentalizing abilities. But this adverse effect is very specic to relations that may cue for traumatic memories and activate an already hyperaroused attachment systemas can easily happen in psychotherapy (Liotti, 2004; Liotti, Cortina, & Farina, 2008).

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Competition and Cooperation and the Evolution of the Social Brain


There are other points of agreement and disagreement between Fonagy and Target (2008) on one hand and with Gergely and Unoka (2008) on the other that we would like to address, but this would require prolonging an already long article. Nonetheless, there is one more point we want to discuss that is germane to a central hypothesis in this article. Fonagy and Target support Alexanders hypothesis (1989) that as humans became a dominant species during the Pleistocene era, our main competitors became other nomadic hunter gatherer groups. In this scenario, mindreading abilities evolved as the result of an arms race that put selective pressures on mutations that fostered mindreading abilities among our human ancestors in competition with other groups. That is, what drove the evolution of mindreading were strategies aimed at outwitting competitors by use of subterfuge and deceit. This idea is often referred to in evolutionary literature as the Machiavellian brain hypothesis (Byrne & Whitten, 1988). We do not doubt that competitive evolutionary strategies supported the expansion of the neocortex and mindreading abilities among our Great Ape relatives. What we want to add to this evolutionary hypothesis is that the rst step that allowed our human ancestors to become a dominant species might have been their ability to cooperate together in ways that far surpass any known primate species. High levels of cooperation (rather than competition) put selective pressures on mutations that increased social understanding and advanced intersubjective communication. This idea is beginning to be referred to as the cultural intelligence hypothesis (Boyd & Richerson, 2005; Tomasello, Carpenter, Call, Behne, & Henrike, 2005) or the Vygotskian intelligence hypothesis in honor of the great Russian psychologist (Moll & Tomasello, 2007). That is, the arms race with other groups initiated a mutually reinforcing synergy between greater degrees of cooperation, mentalizing abilities and cultural diversity (Richerson & Boyd, 2005; Tomasello, 1999). The need to compute this level of social complexity within highly cooperative groups might have a causal effect on the expansion of the neocortex in humans (Dunbar & Shultz, 2007).

Life History Strategies, Prolonged Dependency, and Developmental Plasticity


In addition to a within-group cooperation/outer-group competition evolutionary model (with selection taking place at the level of groups), there is some evidence that another important evolutionary strategy responsible for the expansion of the neocortex was change in the onset and timing of development processes, referred to in the evolutionary literature as heterochrony (hetero different, chronos time; that is, changes in the timing of development) or life history strategies. One important example of a life history strategy is the slowing down or accelerating of development (Gould, 1977; McKinney, 1998; McKinney & McNamara, 1991). Among our human ancestors there was a very signicant slowing down of maturational processes, creating a very long period of development, the most protracted of any known species (for review, see Flin & Ward, 2005; Gibbons, 2008). A slow maturation required intensive parental care of very immature (altricial) offspring over a very long period of development. An important consequence of this tinkering was maintaining rapid rates of brain development (more neurons and greater synaptic and dendritic growth) into the third year of life (Finlay & Darlington, 1995; Finlay, Darlington, & Nicastro, 2001). The very high cost of taking care of altricial offspring over a very long period of development, had to produce a very signicant gain in order for this evolutionary strategy to succeed. We think that the main gain was to

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produce an unprecedented degree of developmental plasticity and adaptive exibility among our human ancestors (Bjorklund & Rosenberg, 2005; Hrdy, 2009).

Are Selfobject Functions Part of the Attachment System?


A second approach integrating attachment and intersubjectivity taken by Joseph Lichtenberg (1989, 1992), expands the concept of attachment as providing security, to include many other important functions, such as affect regulation, validation, and recognition; that is, selfobject functions (broadly speaking) proposed by Kohut and his followers (Kohut, 1971, 1977). Our objection to this approach is that it conates the attachment system with the caregiving system and with selfobject functions. It is the case that attachment gures do much more than provide protection for their infants during periods of distress. Parents abilities to help regulate their infants arousal levels and emotions, to read their signals and respond empathically to their needswhat Ainsworth described as sensitive responsivenessare essential to help infants become secure in their attachment to caregivers. But these are parental functions that are associated with the caregiving system, not the attachment system. In the best of cases, attachment gures are able to integrate their own attachment histories with intersubjective mind-reading and empathic abilities. Lichtenberg agrees that the attachment system and caregiving system need to be conceptualized as distinct but related systems (personal communication with Joseph Lichtenberg on March 23, 2009). Making this distinction addresses some of the issues that get entangled in thinking about attachment, parental functions, and intersubjectivity, and narrows considerably some of the differences between our approach and Lichtenbergs. What about attachment and selfobject functions? Kohut proposed three selfobject experiences that could be expressed as idealizing, mirroring and twinship transferences (Kohut, 1971, 1977). The idealizing transference consists of seeing the other (often a parent in childhood) as being stronger and wiser than self and ts with Bowlbys denition of an attachment gure (being perceived as stronger and wiser). Idealizing, in this sense, is directly connected to the attachment system. The mirroring transference, however, is based on the experience of being (or not having been) adequately recognized, validated and admired by parental gures. The mirroring selfobject experience probably evolved out of the need to recognize members of the same species as unique individuals, a need that was particularly important among our human ancestors who evolved in rich and complex social groups. The need to be mirrored has a very different function than the safety function of attachment. Of course, attachment gures that are sensitive to the need to recognize, validate, and admire (when appropriate) their infants and childrens unique emotions, intentions and mental states are more likely to develop a secure attachment with them. Twinship transferences are based on the ability to see others like me while assuming that others will also see me. This is not an attachment function, but an intersubjective ability based on the capacity to imagine others as having desires, intentions and mental states similar to ones own (Meltzoff, 2007). This is the basis for the human ability to collaborate and share with others as equals. We agree that these are all important needs, but we think it is better not to lump them all together as attachment but maintain a distinction between security and protection (attachment), affect sharing/validation (intersubjectivity) and cooperation based on a sense of mutuality and shared basic needs, desires and aspirations. From the perspective of the infant, being able to integrate these two lines of developmentattachment and intersubjectivityis a challenge that will depend heavily on the quality of their relationship with

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their caregivers and caregivers ability to respond to their infants as subjects in their own right.

Attachment and Intersubjectivity Have Distinct Functions, But Become Intertwined During the Course of Development
A third approach consistent with our general thesis of distinct but related functions between attachment behaviors and intersubjective abilities has been developed by Daniel Stern (1985, 2004, 2004) and Karlen Lyons-Ruth (2006). Our general approach is very similar to the one taken by Stern and Lyons Ruth in seeing attachment and intersubjectivity as two distinct domains with different evolutionary origins that are closely intertwined during typical development, but become disjointed during atypical development. We also agree with Stern that intersubjective sharing becomes an emergent motivation in humans. According to Stern intersubjectivity is not only a condition of our humanness, it is also an innate primary motivation system, essential for species survival and has a status like sex or attachment (Stern, 2004, p. 97). According to Stern by the end of the rst year intersubjective relatedness begins to exhibit a quality that is experienced as a felt desire or need. He describes two main types of need: rst, a need or desire to share with others and the need to dene and maintain self-identity or self-cohesion. This latter need echoes the enormous importance that Kohut placed on self-cohesion as an overall principle of psychic functioning. Stern supports his view of intersubjectivity as a source of motivation by noting that intersubjective motives have two characteristics that we usually attribute to a motivational system: a quality of need or desire, and specic sets of conditions under which these needs or desires become activated. According to Stern intersubjective motives can be specically activated when (1) ones place in a group is thrown into question or when rapidly coordinated group functions are needed, (2) self-identity or self-cohesion is threatened, and (3) the desire for psychic intimacy is greatas in falling in lovea need that ts the broader function of regulating psychological closeness and distance. To understand the rst pointwhy intersubjective communication and social understanding is related to group functionsrequires situating the emergence of advanced intersubjective functions in a larger evolutionary context of a multilevel view of selection that focuses on the importance of group selection for human evolution (Bowles, 2006; Bowles, 2009; Dunbar & Shultz, 2007; Wilson, 2002). We will not address the second point in regard to self-cohesion because it would take us too far aeld, but we think it is also related to the importance of the group as a unit of survival during human evolution. In terms of the third point about the need for psychic intimacy, we agree with Stern that intersubjectivity becomes a motive that may be felt as a need for intimacy, but this agreement has an important caveat. From an evolutionary perspective, attachment and intersubjective motives belong to different levels of organization and have very different degrees of specicity. By different degrees of specicity we mean two things. Motives that emerge from the intersubjective matrix (intimate sharing and altruistically cooperating with others) have a less intense quality than attachment or sexual needs, and the conditions under which intersubjective motives become active are more general than the more specic conditions that activate attachment, caregiving or sexual motives. Lyons Ruth (2006) makes a similar point, noting that intersubjective communication is not a motivational system in the same way attachment is a motivational system, since in humans intersubjective communication has a ubiquitous role that permeates all other mental functions and makes us uniquely human. We completely agree with her, and we will provide evolutionary and developmental arguments and empirical data that

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support this position. For now, we want to emphasize that these distinctions are not just an academic exercise, but have important clinical implications that we will address later. In keeping with Tomasellos ground breaking theoretical and empirical agenda (1999, 2003, 2005, 2008), in addition to the desire to share experience with others, there is another important motivation that emerges in humans during the second year of life: A cooperative/altruistic motive to engage with others (mostly caregivers, but strangers too) in the pursuit of joint goals and plans of action. This motive builds on the ability to understand the intentions of others, a we or shared form of intentionality (Searle, 1995; Tomasello et al., 2005). As Tomasello and his collaborators show (2008), this joint intentional (and attentional) format becomes in humans the basis for a cooperative infrastructure in our species. Tomasello and his collaborators have developed an impressive research agenda showing how this cooperative infrastructure is fundamental to understanding how high order intersubjective (mindreading) abilities, language and culture might have emerged during the course of human evolution (Tomasello, 1999, 2008). Despite some differences with Stern in regard to whether intersubjective motives for intimacy and sharing have the same degree of urgency and specicity as attachment, caregiving, or sexual motives, we think Sterns proposals are bold and break new ground in several directions by considering intersubjectivity as a source of human motivation (a proposal which has many similarities to Tomasellos and Colwyn Trevarthens work) and by linking intersubjectivity with group survival functions that enhance group functioning. According to Stern (2004, p. 105) intersubjectivity contributes to group survival. It promotes group formation and coherence. It permits more efcient, rapid, exible, and coordinated group functioning and it provides the basis for morality to act in maintaining group cohesion and language to act in group communication. Stern does not offer much evidence to support these interesting thoughts, a gap we will try to ll in the next section of this article.

Human Forms of Cooperation far Surpass Cooperative Behaviors Observed Among Our Closest Primate Relatives
This section is divided in to four parts. The rst three parts examine the possible origins of human hypercooperativeness from several evolutionary perspectives. In the fourth part we turn to comparative data between humans and chimpanzees that supports the view that human cooperation is qualitatively different from cooperative behaviors observed among the Great Apes.

The Evolution of Human Cooperation


We think that the crucial adaptation responsible for the evolution of advanced forms of intersubjective mindreading abilities has been the extraordinary increase in the level of cooperation that took place among our homo ancestors (perhaps starting with Homo erectus) during Pleistocene era or the era of ancestral humans1.8 million years to 10,000 years ago (Boehm, 1999; Bowles, 2006; Boyd & Richerson, 2005). A fundamental shift occurred during the course of human evolution from a social organization based primarily on competition and dominant hierarchies that is prevalent among other primates to a social organization based on equality and cooperation, as observed among the few surviving bands of nomadic hunter gatherers that still exist in the world (Boehm, 1999). To avoid misunderstandings, we want to stress that although the main form of social organization among primates is based on dominance hierarchies, this does not mean

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that primates do not cooperate in many ways. They do, and the range of cooperation is quite extensive. For instance, chimpanzees can establish alliances with others to maintain their rank or to reach a higher rank (de Waal, 1982), and chimpanzees and bonobos have been shown to engage in peacemaking activities (de Waal, 1989). Chimpanzees have even been observed going out in hunting expeditions and will protect territorial boundaries as a group (Goodall, 1986; Mitani, 2006).2 Why would contemporary hunter gatherers serve as a model for Paleolithic hunters and gatherers? A number of similar characteristics and conditions, such as patterns of radiation, hunting for large mammals, unpredictable food supplies, investment in technologies that reect seasonal changes, and tools use (gadget technologies) point to a common matrix (Kuhn & Stiner, 2001). Moreover, Boehms review of available anthropological data shows that the egalitarian organization can remain remarkably similar across continents as long as hunter gatherer societies continue a nomadic existence (Boehm, 1999). We acknowledge, however, that the hypothesized continuity of adaptive strategies during middle to late Pleistocene era and contemporary hunter gatherers must remain as a place holder until further evidence comes from different sources supporting this linkage. If selection favors individuals that look out for their own self-interest, how could this level of cooperative and altruistic behaviors have evolved? Cooperative and altruistic behaviors among closely related kin has had a solid evolutionary explanation ever since Hamilton (1963, 1964) came up with the brilliant idea that altruism can evolve by altruistic individuals passing on their genes to blood relatives. One can think of this strategy as a form of genetic nepotism, the closer the genetic relation, the more likely that the benets of altruism will be passed on to the next generation. This theory is known as kin selection or inclusive tness. In contrast to the ubiquity of the role kin selection has had among many species of animals, including eusocial (truly social) insects such as ants, wasps and bees (Hughes, Oldroyd, Beekman, & Ratnieks, 2008), cooperation and altruism toward nonkin members of a groupsuch as the case of human hunter gatherersis a relatively rare evolutionary occurrence. The most widely accepted evolutionary explanation for cooperative social behavior among members that are not related genetically is based on the concept of reciprocal altruism (Axelrod & Hamilton, 1981; Trivers, 1971). Reciprocal altruism can be modeled on a tit for tat exchange of the type I will cooperate with you as long as you cooperate with me: either person will resort to selshness at the rst signs of noncooperation. This is a conditional strategy that is only supercially altruistic since it is primarily motivated by self-interest. While we do not doubt that different forms of cooperation might have evolved from these conditional strategies (such as the ability of many apes to form strategic alliances in order to maintain or gain an upper hand within social hierarchies), we think that they do not account for the type of altruism seen in humans as observed among nomadic hunters and gatherers, nor do conditional strategies explain the spontaneous helping gestures that 18-month-olds exhibit toward strangers: these spontaneous gestures are not based on rewards (Warneken & Tomasello,

2 As Tomasello points out (2008, p. 173), this type or group hunting does not mean, as some have adduced (Boesch, 2005), that chimpanzees have coordinated plans with different roles to play as is the case among human hunter gatherers. This type of group hunting is more akin to similar group hunting activities among wolves, that rst surround their prey. Each individual member who is closest to the prey will attack in sequence. This might seem like a coordinated plan of attack, but it is not.

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2006) nor do they t well with infant researchers observations of the sheer delight linked to intersubjective sharing among infants and their mothers (Hobson, 2002; Trevarthen, 1988). Another source of data that puts into question whether conditional strategies can account for advanced forms of cooperation seen in humans are based on experiments in adult populations using the Ultimatum Game. In this game, individuals are given the choice to make more money (the self-interest strategy) or make less or no money at all depending on how their opposite number behaves in each round of the Ultimatum Game. In others words, the game pits self-interest against a sense of cooperation and fairness. The results of many experiments using this game show that a sense of fairness (a strong form of reciprocity) often defeats strategies based on self-interest (Gintis, Bowles, Boyd, & Fehr, 2003). If individuals playing the game perceive that the offer is grossly unfair and greedy, they will often refuse it, even if doing so means that they will not receive any money at all. This strong form of reciprocity has been demonstrated in many different human groups and cultures, a nding that supports the hypothesis that it is a stable strategy inuenced by culturally mediated norms of cooperation and fairness (Henrich et al., 2005). A reciprocal sense of fairness is uniquely human. An experiment done with chimpanzees engaged in a simplied version of the Ultimatum Game found that they are selfmaximizers. That is, they operate on the principal of maximizing gains in competitive situations and make decisions based on self-interest (Jensen, Call, & Tomasello, 2007). It is not that evolutionary game theories, such a reciprocal altruism are wrong. Reciprocal altruism might account for the type of cooperation seen among nonhuman apes in competitive situations involving forming alliances and coalitions with others, but do not explain the strong tendency of humans to cooperate as equals based on a sense of reciprocity and fair play, nor do game theories explain the human desire to cooperate for the sole pleasure of sharing with others in joint activities (Stern, 2004; Trevarthen, 1988; Trevarthen & Hubley, 1978). An alternative hypothesis to reciprocal altruism to explain these deeper forms of altruism and cooperation toward nonkin members is based on the resurgent theories of group selection. Simply put, in competing against other groups, groups with more cooperative and altruistic members will outcompete groups that are less cooperative and altruistic. Group selection theories had been discredited for years, but they are now receiving renewed interest thanks to the emerging multilevel view of selection. This perspective sees selective processes operating at multiple and often competing levels: genes within individuals, individuals within groups, and groups within a metapopulation of groups (Boyd, 2006; Boyd & Richerson, 2005; Okasha, 2006; Sober & Wilson, 1998). The multilevel view of selection preserves some of the insights and discoveries made by kin selection (Hamilton, 1963) and of game theories (Axelrod & Hamilton, 1981; Maynard Smith, 1982; Trivers, 1971) but situates these insights within a more general and inclusive theory that sees selection operating at multiple and at times competing hierarchical levels. A more precise denition of what is meant by a group from an evolutionary perspective (based on a focus on traits such as altruism) as well as more precise and clear sets of conditions under which group selection may prevailin order to counteract strong selective forces operating at lower levels of individuals have made it possible to empirically test group selection for any given trait. There is now a growing scientic consensus that group selection has played a signicant role during the course of evolution, and is particularly relevant to explain the case of human evolution (Boehm, 1999; Bowles, 2006; Bowles, 2009; Boyd & Richerson, 2005; Moll & Tomasello, 2007; Okasha, 2006; Sober & Wilson, 1998; Wilson, 2002; Wilson & Sober, 1994).

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Empirical Support for Group Selection


Samuel Bowles, from the Santa Fe Institute in New Mexico, has recently provided robust empirical data that supports the importance of group selection on the evolution of altruism and cooperation in humans (Bowles, 2006; Bowles, 2009). Two conditions that mathematical modeling indicate would be necessary for group selection to prevail are present in human hunter gatherer societies. First, there must be frequent contests among groups. Contrary to what was believed, many nomadic hunter gatherer groups are not so peaceful, and battles between groups have a high incidence of mortality because of the nature of hand-to-hand combat. Successful groups will also reap the benets of colonizing the territories of their adversaries. Second, there must be a system of sanctions and punishment that spread the high costs of the enforcement of prosocial values (altruism, cooperation) to the group as a whole. Hunter gatherer groups perform this function efciently by the use of leveling mechanisms that function as a social tax and permit the high costs of enforcing altruistic norms (and punishments for violators of these norms) to be spread though the group as a whole, so that the high costs of enforcement does not fall on just a few individuals (Boyd, 2006). This leveling function is accomplished through shared cultural norms or values (an egalitarian ethos) enforced through shame, guilt and ostracism, and occasionally even murder (Boehm, 1999). Cultural values among hunter gatherer groups also stress the importance of sharing foods and socially imposed monogamy, thus reducing the tness differences within groups (that otherwise will strongly favor selsh individuals). Group sanctions against free loaders to become effective require a long time to become institutionalized, but recent modeling suggests that this condition was met during the course of human evolution (Ga chter, Renner, & Martin, 2008). But once in place, these sanctions become voluntarily accepted and do not have to be compulsorily imposed (Hauert, Traulsen, Brandt, Nowak, & Sigmund, 2007).

It Takes a Village to Raise a Child: Other Evolutionary Adaptations That Made Humans an Ultra-cooperative and Altruistic Type of Primate
Cooperative breeding refers to an evolutionary strategy in which the biological mother (occasionally the father too) are assisted by other members of the group (alloparents) in the care of their offspring. Cooperative breeding was rst studied in social insects and birds, but it is in mammals and particularly primates that comparisons with humans are meaningful. Of the 175 or so primate species, only half provide some type rudimentary biparental care where mother and father do the protecting (Hrdy, 2005) and in only one fth of primate species is alloparenting accompanied by provisioning (feeding) the young. Only the members of the subfamily Callitrichidae and humans are full-edged cooperative breeders combining substantial alloparenting and provisioning (Hrdy, 2009 p. 275). An alloparent can be any member of a group, but most alloparenting is done by closely related kin, as predicted by Hamiltons theory of inclusive tness. Hamilton was also the rst to predict that cooperative breading would be associated with slow maturing, altricial infants, a prediction that has proven to be roughly correct (Hrdy, 2005). Why cooperative breeding? Shared care frees the mother to engage in foraging activities with the result that they can breed at a faster pace. In humans, life history strategies might also play a major role. As we noted earlier, altricial (relatively helpless) infants, long childhoods and bigger brains go together. According to Hrdy, alloparental care allowed humans to provide the support to feed the large brain that consumes half of all metabolic needs in infancy. It requires 13 million calories to raise a human infant to the stage where they are nutritionally independent (Hrdy, 2005, p.1516). What is even more interesting is that we are the

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only members of the Great Ape family who are cooperative breeders (Hrdy, 1999, 2009). Other apes, like chimpanzee mothers, are extremely possessive, and do not allow others to take care of their infant. There are very good reasons for this. Other males who might want to mate with the mother often resort to infanticide to restore the mothers reproductive capacity inhibited by lactation. In some groups, if the mother and the infant are unfamiliar to the group, other females might kill the infant and the mother. The fact is that infanticide is a very frequent cause of infant mortality in many species of primates (Cheney & Seyfarth, 2007; Hrdy, 1999). Hrdy believes that for the combination of bigger brains, prolonged childhoods and mindreading abilities to have emerged, cooperative breeding would have had to come rst. We agree, but would add that cooperative breeding was not the only or even the most important evolutionary strategy that led to this complex set of traits. Other species with smaller brains can be cooperative breeders. A transitionvia group selectionto societies composed of groups of highly cooperative and egalitarian hunter gatherers was also essential. It was probably the combination of several evolutionary strategies working together (life history strategies, group selection, kin selection and cooperative breeding) that led to human ultracooperative, mindreading abilities.

Experiments Comparing Chimpanzees With Human Children in Their Abilities to Cooperate and Share in Role-Playing Activities
Many might treat the hypothesis of cooperative origins of mindreading abilities based on group selection and the signicance of alloparenting as another example of a just so story. To counter this critique we have pointed to the population structure (in-group cooperation out-group competition) and evolutionary mechanisms that support this hypothesis, as well as evidence from contemporary hunter gatherer groups that is consistent with it (Bowles, 2006; Bowles, 2009). But to carry weight converging evidence from other elds is needed. We now turn to three articles comparing human children with chimpanzees in a variety of cooperative tasks (for review see Tomasello, 2008, 2009) that support the claim than humans are a hypercooperative type of primate. In the rst study Warneken and Tomasello (2006) presented 18- to 24-month-old human infants and three humanraised chimpanzees with four experimental tasks, two that were instrumental in nature and had concrete goals and two social games in which there was no specic goal except for cooperating for the sake of keeping a social game goinglike bouncing a ball together and catching it with a can. The other important feature of the experiment was that the adult partners would quit these tasks at a certain point and wait until their partner signaled a willingness to continue the activity. In the instrumental tasks the human infants and the chimpanzees did equally well. Chimpanzees were able to coordinate their behavior with a human partner in order to succeed in the task. In the social games there was a marked difference between the species. Humans took delight in the social games, whereas chimpanzees did not engage at all. When the adult partner stopped the instrumental tasks or the social games, human infants tried to reengage the adult, and even made the instrumental task into a game. In contrast, chimpanzees did not try to reengage the human partner in any of the four tasks. This was particularly noteworthy because food was built into one of the tasks and chimpanzees are notoriously driven to obtain food. The second study had a longitudinal design and involved three human raised chimpanzees (Tomasello & Carpenter, 2005). Among many interesting ndings, the authors showed that chimpanzees were equally adept as human infants in understanding goals and perceptions in simple cooperative tasks that involved exchanging roles. However, when

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humans forced a complementary role exchange on the human infants and the chimpanzees, human infants were able to exchange roles, whereas chimpanzees simply repeated the same task with no reference to the human partner. Humans joint intentional and attentional abilities allow them to exchange complementary roles. For example, chase ee, buysell, come go, borrowlend, or complementary social roles, such as careseeking caregiving, studentteacher, victimpersecutoran ability that implies the emergence of a reciprocal type of imitation. Chimpanzees lack the ability for reciprocal role imitation and cannot exchange complementary roles. The third article is very revealing in another way. Hare and Tomasello (2004) introduced apes to a game in which a human hides food in one of three buckets. A second human, who acts as a helper, assists the ape to nd the food. Apes know from experience that there is only one bucket that contains food and they have only one chance in picking the right bucket. The experiment consists in the helper peeking while the food is being hiddenthe ape can see that the human helper is peeking. The helper then points toward the bucket where the food is hidden. Amazingly, apes chose randomly. They dont seem to understand that the human helper is pointing to the food. The game is then modied, but this time a competitive version is introduced in which in a warm up trial another human begins to compete with a chimpanzee for food in the bucket. Without looking at the chimpanzee, the human competitor reaches toward the bucket containing the food in each try. After several rounds of this warm up, a Plexiglas is put between the human that is competing for the food and the buckets. Because the hole is not big enough, the human cannot quite reach the bucket that has the food, but the thwarted effort of an arm trying to reach for the bucket containing the food clearly shows what the human is up to. In this situation the ape will immediately reach toward the bucket with the food when the buckets are pushed toward the chimpanzee. Why do apes not reach toward the bucket in the cooperative/helping situation, yet immediately reach to the bucket in the competitive situation? It is not that chimpanzees do not understand pointing gestures, as long as they are raised by humans as was this casesee below. Several experiments have also shown that apes understand the intentions of others in a variety of situations (Buttelman, Carpenter, Call, & Tomasello, 2007; Call & Tomasello, 2003; Warneken & Tomasello, 2006). The only possible inference from this experiment is that in the helping situation chimpanzees do not understand that the human is communicating with an altruistic motive, but in the competitive situation they immediately grasp what is going on (Tomasello, Carpenter, & Liszkowski, 2007). The overall pattern suggests a qualitative difference in cooperation and social understanding between the two species. The rst difference has to do with motivation. Human children are not only motivated to reach goals, but they are also motivated to cooperate for the sake of cooperation. Chimpanzees are only interested in reaching a goal that is self-serving as we saw in the last example. It is not in their nature to understand altruistic helping except among closely related kin, as when mothers take care of their infants but they do understand competitive situations and are very motivated to respond in these situations. The second important difference has to do with social cognitive abilities. In the rst example, children understand there is a joint goal involved in all these tasks. When this joint goal is breached (by stopping the activity) human infants try to reengage their partners, whereas chimpanzees do not, even when the task involves a reward that they are motivated to reach such as food. This suggests that the ability to engage in the pursuit of joint goals is absent in chimpanzees. As can be inferred from the second study, chimpanzees lack abilities for a reciprocal form of imitation that would allow them to

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exchange complementary roles. Chimpanzees are goal oriented and they do understand intentions, but despite their remarkable social abilities, social understanding is primarily adapted to situations that involve competitive interactions. Chimpanzees simply dont get it when they are called upon to interact for the sake of sharing experience or helping others in situations that call for a type of altruism and cooperation that seems to be uniquely human.

The Ontogenetic Roots of Intersubjective Sharing and Cooperation in Humans Primary Intersubjectivity
Another body of evidence that supports the hypothesis of the cooperative origins of mindreading abilities is based on infant research. Colwyn Trevarthen is a pioneer in tracking the development of intersubjective cooperation, sharing and companionship (Trevarthen, 1979, 1988), describing primary and secondary forms (Trevarthen, 1980, 1988; Trevarthen & Aitken, 1994; Trevarthen & Hubley, 1978). During the course of the rst year of life, parent-infant dyads respond to each others nonverbal cues, vocalizations, gestures and emotions. The intricacy and subtlety of these protoconversations have all the hallmarks of a well orchestrated dance. Infant cues are matched in timing, form and intensity (all integrated cross-modally) by their caregivers (for review see Beebe, Knoblauch, Rustin, & Sorter, 2003). This match, however, is not an exact mirroring response. Even at its best, there are minor cycles of disruption and repair even with parents that are sensitively responsive and attuned to their babies communications (Beebe & Lachmann, 2002). In addition, caregivers responses to infants cues and vocalizations use a simplied and redundant grammar, a high pitched voice and exaggerated gestures. This form of speech, motherese or child-directed speech (CDS), seems to be universal (Ferguson, 1962). Several functions have been attributed to CDS, such as facilitating language development (Snow, 1972), emotional communication, capturing babies attention and soothing childrens distress (Sroufe, Cooper, & DeHart, 1992). Another possible function of CDS has been suggested by Fonagy et al. (2002). The marked emotional tone of these interactions may help babies differentiate their emotional responses from their caregivers exaggerated responses during these protoconversations. Stern (1985, 2004 and Hobson (2004) have emphasized the affective core of intersubjectivity. Not only is there a correspondence of gestures and vocalizations, but there is also an affective interchange that operates across different perceptual and expressive modalities. This emotional correspondence, that Stern calls affect attunement concerns how inner feeling states are shared (Stern, 1985, 2006).3 Most likely, the affective core of intersubjectivity provides a sense of continuity that bridges the dramatic changes in social cognition that take place between the rst and second year of life. By the end of the rst year and rapidly accelerating during the second year, infants use mothers emotional responses to assess how they should react to unfamiliar situations, a phenomena described as social referencing (Emde, 1992). Emotions play an essential role in the emergence of primary and secondary forms of intersubjective sharingme, you, and the shared world

This correspondence in gestures and emotions is likely rooted neurobiologically in a mirror neuron system (Gallese, 2003, 2005, 2009), while the turn-taking abilities may have their roots in the presence of adaptive oscillators (Port & van Gelder, 1995; Stern, 2004).

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that is being explored. It is no exaggeration to say that infants begin to see the world from the emotional perspective of their primary caregivers (Hobson, 2004).

Secondary Intersubjectivity: Why Pointing Matters


There is a scientic consensus that between 9 to 12 months of age there is a revolution in human development that corresponds roughly to Trevarthens description of a secondary form of intersubjectivity (Trevarthen, 1980, 1988; Trevarthen & Hubley, 1978). A very illuminating way to grasp what the revolution is all about is by examining the seemingly simple and humble gesture of pointing. Bates, Camaioni, and Volterras (1975) classic article set the stage for all subsequent literature on the signicance of pointing as a tool and as a prelinguistic form of communication. Elizabeth Bates and her coworkers made the distinction between a pointing that is a request from the infant to obtain an object from an adult: give me the toy mommy (imperative pointing), and pointing that is a request to attend to some external object look at that ower mom (declarative pointing). The rst type of pointing develops toward the end of the rst year of life, once infants have developed the capacity to understand goal-directed behaviors and discover that goals can be reached through different means (Piaget, 1952). Infants use imperative pointing instrumentally to obtain objects from adults. This type of imperative pointing can also be seen among nonhuman primates that have been raised in captivity or raised by humans. (Tomasello & Carpenter, 2005), but it has only been observed once in the wild (Call & Tomasello, 2003). The second type of pointing, which is declarative and triadic in nature, involves infants sharing events or objects of interest with caregivers. Infants begin to explore the world with others. Jerome Bruner (1977) was the rst to note that this type of declarative pointing joins infant and parent in a meaningful social exchange that is motivated by a desire to share attention toward an object with an adult. Declarative pointing is brought about by new abilities: the capacity to maintain a joint attention toward objects of interest, by the emergence of a bidirectional understanding of goals and intentions between infants and caregivers, a we form of intentionality (Searle, 1995; Tomasello et al., 2005). At its simplest, joint attention can be seen when infants begin to follow the gaze of others. But infants ability to follow adults gaze or point to a target does not necessarily imply that the infants understand that others have intentions similar to their own. The ability to understand the intentions of others is a necessary step for declarative pointing to emerge. Declarative pointing is emblematic of a new form of mutuality that develops during the second year of life, but soon expands to other behaviors, such as holding objects up to show them to others and bringing others to locations so they can observe interesting things (Trevarthen, 2005: Hobson, 2004). The emergence of a role-reversal form of imitation (Meltzoff, 2005, 2007) and the related ability to identify with the intentions of others (Hobson, 2004) during the second year of life also allows infants to engage in games that involve reciprocal roles, such as taking turns rolling a ball back and forth with an adult, taking turns in feeding, or more complex games like peek-a-boo. By the time infants are 18 months old, a shared form of intentionality and role reversal imitation set the stage for collaborating in joint plans and shared goals, such as building a tower with blocks, or in tasks like picking up toys together (Moll & Tomasello, 2007; Tomasello & Carpenter, 2005).

The Emergence of Perspective Taking Abilities


The ability to share intentional states with others has another fundamental consequence by creating the possibility to take on the perspective of others (Barresi & Moore, 1996; Moll

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& Tomasello, 2007). This is already implicit in the ability of 14- to18-month-old infants to assume the role of others in social games and to coordinate activities and develop joint plans of action. As Moll and Tomasello (2007) point out, by 18 months infants begin to develop the capacity to see the same thing from their own point of view and the point of view of others. Barresi and Moore (1996) believe that the ability to have a birds eye view of rst and third person perspectives implies a representational capacity to view self and others perspectives simultaneously. This hypothesis connects with ideas put forward by Jessica Benjamin of an intersubjective third (Benjamin, 2004: Aron, 2006). A collapse of the ability to maintain simultaneously the representation of self and other causes a reversion to a position where one can only see interpersonal exchanges from a rst person perspective (its all about me), or a third-person perspective (its all about the other). According to Benjamin (2004), this collapse of the intersubjective third leads into a doer/done to dynamic and according to Liotti the collapse of metarepresentational abilities leads to multiple and fragmented representations of self and other induced by trauma and a history of disorganized attachment (Liotti, 1992, 2004). Unfortunately we will have to leave further exploration of these important clinical issues for another occasion. As language takes off in earnest by the second year of life, shared intentionality and perspective taking abilities take another giant step forward. With language humans can imagine how others might feel or think from many more perspectives. We can time travel and imagine what it might have been to live in the past and imagine worlds that might not even exist. We can create narratives that include different cultural perspectives. Examining how intersubjective sharing and a shared form of intentionality create a common ground upon which language will ourish, and how language expands the perspective taking abilities by leaps and bounds is still virgin territory and an area of study that is ripe for further exploration (Farrant, Fletcher, & Maybery, 2006; Hobson, 2004; Tomasello, 2003, 2008).

The Emergence of Intersubjective Motives


The early signs of sociability are ushered in by the emergence of the social smile that appears 4 or 5 weeks after birth and progressively becomes more prevalent and differentiated in the following months (Sroufe, 1996). At rst, the smile is released by high arousal states such as REM dreaming states, but by the fourth week of life the smile is released by seeing a human face or the gestalt of the human face. By second to third month of age the emotion that accompanies the social smile is also transformed from expressions of pleasure to categorical expressions of joy (Sroufe, 1996). In contrast to attachment behaviors that are powerfully directed at one or two attachment gures, by the end of the rst year of life (only you can comfort me), the social smile is indiscriminate. Infants will smile to anybody who smiles at them. Most adults nd these smiles, giggles and babbling endearing and irresistible. The social smile powerfully promotes affective sharing between infants and caregivers and unequivocally shows that infants come equipped to engage socially with others soon after birth. In keeping with Stern, we think that this form of engagement ushered in by the social smile is part and parcel of a larger system of intersubjective communication that is present soon after birth, and continues to develop throughout life. The communicative system has built into it a motivational component. First, a desire to share feelings and by the end of the second year of life a desire to share in more complex interactions such as social games and high levels of collaboration required to construct joint projects, large and small. Trevarthen (1988, 2005)

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and Tomasello (Tomasello, 2008; Tomasello & Carpenter, 2005) have proposed similar ideas. Trevarthen has insisted on motives for cooperation and companionship that are the key to the acquisition of culture and emotional expressiveness (Trevarthen, 2005). Along very similar lines Tomasello (2005) has argued that a motivation to share intentions and psychological states goes hand in hand with the enormous capacity for cooperation that is the hallmark of our species and the basis for acquiring language and for cultural evolution (Hobson, 2004; Tomasello, 1999, 2003, 2008). As Lyons-Ruth (2006) notes, intersubjective abilities and motives permeate all other motivational systems, including the attachment system. The evolutionary and developmental framework that we have discussed allows us to return to a further examination of the differences between intersubjective abilities and motives and the attachment system.4

Three Differences Between Attachment and Intersubjectivity Attachment Is a Domain Specic Adaptation. Intersubjective Abilities and Motives Are Domain General Adaptations
The attachment system is one of several functionally discrete interpersonal motivational systems observed in primates that serve vital adaptive functions such as providing intensive parental care (the caregiving system), developing sexual partnerships (the sexual system), and having privileged access to resources by establishing dominance over others (the ranking system). In contrast to these more discrete functions, the main function of intersubjective mindreading abilities is to provide an automatic and emotionally intuitive system of communication among conspecics. In the parlance of contemporary evolutionary psychology attachment, caregiving, sexuality, and competition are domain specic adaptations, whereas intersubjective mindreading abilities and intersubjective sharing motives are domain-general adaptations. Cognitive psychology (Fodor, 1994) and evolutionary psychology (Cosmides & Tooby, 1997) use the concept of modularity to refer to these domain-specic adaptations. Modules are brain functions that evolved to solve specic adaptation problems and are segregated from other brain functions. From an engineering perspective, segregated modular systems have the great advantage of making it less likely that their activation will interfere with other important functions that are essential for overall functioning. From this point of view, social systems such as attachment, caregiving, competition or sexual pair bonding have modular characteristics in that they serve discrete needs and show signs of specialization and have their own neural circuitry. This does not mean we are committed to a modular point of view. However appealing, the modular view based on engineering principles can be misleading when applied to complex organisms. Engineering systems, no matter how sophisticated or complex, are all dependent on preprogrammed information that is fed into the system. Living organisms are the product of selective and evolutionary mechanisms and have conserved solutions that have worked well over the course of millions of years. In simple organisms, some of these evolutionary and developmental solutions can be assembled as independent modules

4 This analysis could also be extended to examine the relation between intersubjective abilities and motives and other basic interpersonal motives associated with the caregiving, ranking and sexual pair-bonding systems, but such an exploration is beyond the scope of this article (see Cortina & Liotti, 2007a, 2007b; Liotti & Monticelli, 2008).

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with little need of overall coordination. But in complex animals like primates, the type of massive modularity evolutionary psychologists such as Cosmides and Tooby advocate seems too simplistic and cumbersomemore than 30 modules have been proposed (Buller, 2005). It is the case that if we examine adult brains, there are clear signs of specialization. This has misled many to think that this specialization is a feature of the innate modularity of the brain. Karmiloff-Smith (1992) has made the very cogent point that the specialization in the brain may be an emergent phenomena rather than an example of innate modularity. The specialization is the result of a general developmental process that proceeds from relative undifferentiation to greater degrees of differentiation and specializations of functions. Lately, Karmiloff-Smith had been calling for an approach that recognizes the presence of innate biases or proclivities that interact with the environment at every level of the organism. A similar model has been proposed by Edelman (1987, 1989) with his concept of values that are built into the brain (such as affective responses) and help organize the emerging complexity of the brain. A commitment to a modular brain with a multitude of specialized functions misses the point that perhaps the most important characteristic of our species is its enormous potential for developmental plasticity and adaptive exibility. This plasticity is typical of generalist species in which selective pressures produced a brain in which conspecics can learn consciously and deliberately from each other and can adapt to changing local environments (Gotlieb, 1997, 2002; Westen, 1999). In short, we are in agreement with Karmiloff-Smith that domain specic or domain general functions must be understood within an epigenetic perspective, in which there are ongoing interactions with the environment at every level of the organism (Gotlieb, 1997, 2002). From this point of view we propose that advanced intersubjective cooperative and mindreading abilities can be understood as domain general functions that are characteristic of a species such as ours with slow maturing individuals with a very prolonged development that promotes developmental plasticity and adaptive exibility (Bjorklund & Rosenberg, 2005).

Advanced Intersubjective Abilities Are Evolutionarily Newer Adaptations With Respect to Attachment
MacLeans model of the triune brain (1985) is a dated but still useful model that depicts the hierarchical organization of the brain and helps situate attachment and intersubjectivity as belonging to different levels of organization.5 MacLaen organizes the brain in three levels. The oldest brain (the R Complex) evolved among reptiles and amphibians and contains anatomical structures such as the brain stem, the basal nuclei, and the cerebellum. The functions of the R complex include regulation of essential physiological functions and primitive instincts that involve minimal social interaction such primitive types of sexuality and ght/ight/freezing reactions. The next level, the midbrain or mammalian brain, contains structures such as the amygdala, the hypothalamus, and temporal lobe cortex that regulate emotions and all systems of social interaction. The last level, the neocortex or neomammalian brain, is found in the brain of higher mammals and is responsible for

5 This division of the brain is only a rough approximation, and contemporary neuroimaging data show that the orbitofrontal cortex is in fact an integral part of the limbic brain in humans (Decety, Jackson, Sommerville, Chaminade, & Meltzoff, 2004; Shore, 1994). Nonetheless, this quick and dirty way of looking at the hierarchical organization of the brain is a useful heuristic.

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higher-order thinking skills and language. More advanced domain-general intersubjective motives and abilities (shared intentionality, mentalizing functions) are part of the neomammalian brain. If advanced forms of intersubjectivity that are uniquely human operate at a different hierarchical level of mental functioning than attachment, we should expect in the infant and the growing child differential effects on each of these systems as a consequence of bidirectional inuences on the other.6 In a hierarchical system such as the one we are hypothesizing for the organization of human interpersonal motives, one could hypothesize that bottom-up inuences stemming from right brain limbic structures that are part of the attachment system (Shore, 1994) are emotionally more immediate than advanced top down intersubjective abilities such as intersubjective sharing, cooperation and perspective taking that involve neocortical structures.7 The developmental principle that we support is that adverse inuences and disruptions of evolutionary lower-order interpersonal systems, such as the attachment system, will quickly and necessarily inuence higher-order motivational processes and advanced intersubjective abilities such as sharing and cooperation. The reverse is not necessarily the case. Adverse inuences and disruptions of evolutionary higher-order abilities and motives, such as intersubjective sharing and cooperation, will not necessarily impede the function of more basic interpersonal systems such as the attachment system even though these disruptions will produce atypical attachment patterns. As we noted earlier examples of the rst situationsignicant dysfunction of a lower-level social system, such as attachment, will have an immediate effect on a higher-order social system, such as intersubjective understanding have been well documented. Fonagy and his colleagues have shown that the ability to mentalize (a higher-order function) attachment related experiences is signicantly affected by attachment related trauma (Bateman & Fonagy, 2004; Fonagy et al., 2002). In our way

6 In principle, the same type of reasoning can be applied to the relations between intersubjectivity and other nonattachment-related (domain-specic) interpersonal motivational systems such as the caregiving system, the sexual mating system and social interactions based on competition with siblings and peers. During the second year of life, only three interpersonal systems are fully operational: the attachment system, intersubjective sharing, and the emerging capacity to cooperate extensively with others by taking into account their perspective and to some extent the ranking system as expressed in sibling rivalry. The other interpersonal motivations we just mentioned require more prolonged maturational processes and experience and become fully operative only later in life. The study of the interactions between intersubjectivity and these other interpersonal motivations are therefore less relevant for an understanding of the early reciprocal inuences (particularly during the second year of life) between attachment and intersubjectivity. 7 Neuroimaging data support the view that neocortical structures, such as the prefrontal cortex, become activated when individuals are involved in interchanges that call for advanced forms of cooperation that require judgments in regard to reciprocal fairness. In a recent study the research team disrupted an area of the prefrontal cortex, the dorsolateral prefrontal cortex (DLPFC), thought to be involved in judgments of fairness (Knoch, Pascual-Leone, Meyer, Treyer, & Fehr, 2006) in individuals playing the Ultimatum Game. As we noted before, the Ultimatum Game requires that individuals make a judgment of whether their partners are proposing fair offers. The disruption of the DLPFC was achieved by local low-frequency repetitive transcranial stimulation. The disruption of the right DLPFC reduced subjects willingness to reject their partners unfair offers, even though they still judged the offers as unfair. That is, the local stimulation of the DLPFC temporarily disrupted the ability to engage in fair play. The stimulation of the left DLPFC did not have the same effect. This indicates that interference with right brain DLFPC function interferes with maintaining a sense of reciprocal fairness and mutuality that is required in order to cooperate at higher levels.

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of putting it, individuals with a history of disorganized attachment construct poorly integrated internal working models of self and others. New stressful situations or trauma activate the attachment system, producing a collapse of advanced intersubjective abilities and further fragmentation (Liotti et al., 2008). For instance Hill, Leideken, & Sharp (2008) observe that insecure attachment at 18 months was associated, in 5-year old children, with indices of low mentalizing in an emotionally laden dolls house scenario (Bad and Nasty Time), but not in a neutral scenario (Bed Time). This nding suggests that the activation of insecure or traumatic internal working models of attachment, and the activation of strong emotion linked to separation anxiety, adversely inuence one of the crucial aspects of intersubjectivity, namely, the ability to maintain a good understanding of intentions and emotions of others (mentalizing abilities). When the attachment system is not chronically aroused the capacity for collaboration emerges, as evidenced by the ability of children to reengage in intersubjective sharing through reciprocal imitation and pretend play, abilities that go hand in hand with higher degrees of mentalization (Hill et al., 2008). As intersubjective abilities become increasingly integrated with the attachment system during the course of normal development, they become a necessary condition for the smooth exercise of all other interpersonal motivational systems, such as the ability to cooperate and compete successfully with peers and siblings (Sroufe et al., 2005). Autism is an example of the second situationadverse inuences or disruptions of higher order intersubjective functions will not necessarily disrupt lower-order functions. Many autistic individuals with severe intersubjective decits can maintain an attachment to important people in their lives, albeit a very atypical attachment (Stern, 2004). The fact remains that the attachment system is still operational in autistic individuals, even though its quality is signicantly disturbed. A high functioning autistic person, Temple Grandin, reports memories suggesting normal wishes for attachment interactions when she was a child (Grandin, 1992). In a conversation with Oliver Sacks she discussed her memories of longing to be soothed by a caregivers hug, and her feelings of comfort while she was in the caregivers arms (Sacks, 1995). The problem with satisfying her normal wishes for attachment was her inability to cope with overwhelming feelings of unpredictability and uncontrollability generated during interpersonal exchanges. The decit in intersubjectivity inuenced attachment (and all types of interpersonal behaviors) in later phases of the development of the disorder. These decits are not the consequence of parental insensitivity or frightened and/or frightening caregivers responses to her attachment needs, as would have been true of a child disorganized in her attachment (Hesse, Main, Abrams, & Rifkin, 2003). Rather, they are the result of her difculty in the intersubjective sharing and understanding of motives, emotions, and intentions. A recent article experimentally tested this hypothesis comparing autistic children with matched control groups of mentally retarded, language-delayed, and normally developing children (van IJzendoorn et al., 2007). The results show unequivocally, as predicted, that parental sensitivity affected the quality of the attachment relation with mentally retarded and typical developing children, but had no discernable effect on autistic children. While there were more atypical and insecure attachment patterns with autistic children, these patterns were unrelated to parental sensitivity. The clear inference is that the insecure and atypical attachment patterns of autistic children are not caused by parent child attachment difculties, but are caused by the intersubjec-

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tive decits of autistic childrentheir inability to correctly read and interpret the emotions and communications of their parents. In the absence of more empirical research on the reciprocal inuences (positive and negative) between attachment and intersubjectivity, these examples may provide illustrations of the principle of hierarchical organization of motivational systems and intersubjective abilities.

Intersubjectivity Is Activated Tonically, Attachment Is Activated in Phases


A metaphor from the physiology of muscle activity captures another important difference between intersubjectivity and attachment. Like the tone in a living muscle, intersubjective sharing and cooperation are tonically activeit may change in its motivational intensity, but never disappears totally from the mental activity that is the basis of human higher-order consciousness (Edelman, 1989). As long as there is higher-order consciousness there are advanced forms of intersubjectivity that involve sharing of experience from multiple perspectives through gestures or language (Cortina & Liotti, in press). Even when we are alone, every single perception that emerges in higher-order consciousness becomes conscious from the perspective of being potentially communicable to another human being (Barlow, 1980). When we become conscious of anything, we are (even if only latently) prone to communicate it to somebody else. In contrast, domain-specic interpersonal motivations are phasically active. They work in phases, in a manner that is similar to the specic sequences of muscle contractions and relaxation that are coordinated to attain specic goals. Any conscious activity that takes place in phases has a beginning and an end, a rule of activation and a rule of termination, and will fade in and out of conscious awareness, while a tonic activity is, so to speak, always tonically present. Furthermore, it is possible to specify the rule of activity and the rule of termination of every interpersonal motivation system, but despite what Stern (2004) asserts, this is not so clear with intersubjective motives that are better seen as general-purpose default systems that remain tonically active. Sharing experience with others and being able to examine experience from multiple perspectives is the normal default system in humans. This intersubjective motive and ability for mutual perspective taking might collapse temporarily under strain, but will assert itself vigorously as soon as the emergency is over. The cooperative motive to help others and engage in human communication through gestures and language is also a pervasive state of being. The sharing and cooperative motives in humans remain tonically active in most circumstances, even when the domain specic motivation such as sexuality, attachment and competition are normally active. Even in highly competitive activities like games, sports and scientic endeavors, a cooperative infrastructure undergirds many competitive activities. Indeed, as Piaget (1965) showed in his classic book on the origins of morality in children, a set of rules have to be consensually agreed upon and reciprocally enforced before school-age children can participate in games with peers such as playing marbles. It is only in pathological conditions such as autism, or where there is a history of attachment trauma, that intersubjective abilities and motives to share and cooperate with others are seriously compromised or limited. In domain-specic adaptations such as the interpersonal motives of attachment, caregiving, or ranking systems, the rules of activation and deactivation are clearly dened and specic. Activation of the attachment system coincides with perceived distress, fear, vulnerability or loneliness, while termination coincides with attaining protective proximity

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of an attachment gure and/or with perceived safety. The caregiving system is activated by signals of vulnerability, danger or distress in juvenile members of the social group with whom an attachment relationship has been established. The caregiving systems stopping rule coincides with the successful soothing of the others distress. The sexual system activated by proper secretion of sexual hormones and pheromones in interplay with sexually arousing stimuli of potential matesis usually terminated by orgasm. Among primates, the ranking system is activated by threats of losing rank (and hence losing control of environmental resources and/or preferential access to mating partners) and is terminated by signals of yielding or submission (Gilbert, 1989). Needless to say, the triggers that activate competitive struggles and desire for dominance over others in humans are much more complex and less ritualistic. Humans have created competitive games and contests that are governed by rules of fair play and reciprocity. Contests can range from being very playful to being ercely contested, as is the case in many individual and team sports, but there are explicit rules and sanctions that prevent competition from becoming violent. These are some of the important differences, but we can still see the clear evidence of this ancient motivational system in the case of bullies, in sadomasochistic phenomena and in political struggles over power. One only has to read Franz de Waals description of power politics among the apes (de Waal, 1982) along with Machiavellis The Prince to realize how little has changed in the quest for rank and power among human and nonhuman apes.

Some Clinical Implications Attachment, Intersubjectivity, and the Therapeutic Alliance


Perhaps the single most important clinical application of being able to distinguish the different prosocial functions and motives associated with attachment and intersubjectivity is that it provides a good theoretical model that helps us think about establishing a therapeutic alliance during the course of psychotherapy. Numerous studies have pointed out that the single most important factor predicting the effectiveness of psychotherapy, regardless of the type of psychotherapy that is practiced, is the quality of the patient therapist relation (Hovarth, 2001; Martin, Garske, & Davis, 2000). The more a patient feels understood, feels that the therapist is able to read his or her signals and communications, and feels safe with the therapist, the better the outcome. These qualities are all dependant on intersubjective and attachment functions. Feeling understood and being able to take a different perspective on emotional problems are mentalizing/ intersubjective functions. Feeling that ones therapist is a reasonably protective and trustworthy gure is an attachment related function. Ever since Freud wrote his papers on technique almost 100 years ago, it has been widely accepted by psychodynamic therapists of all stripes that development of an unobjectionable positive transference is one of the most important leverages that help push the therapeutic tasks forward (Freud, 1912). Of course, outcomes are dependent on many other variables, but a positive transference, like smooth sailing, makes getting to any destination a much easier task. Freud was also the rst to recognize that establishing a positive transference based on parental imagoes stemming from childhood, what we now describe as positive attachment experienceswas one of the keys for a successful analysis. Even to the end of his career, in one of the most sober assessments of the limits of psychoanalysis (Analysis Terminable or Interminable) he continued to believe in the

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power of a positive transference (Freud, 1937). But what happens when these positive attachment experiences from childhood are not present or when these attachment experiences have been traumatic? Many changes in technique in psychoanalysis came about in order to be able to work with patients who have unstable relations, are very impulsive, have intense, extremely ambivalent relations to others and toward the therapist and have a history of traumatic or disrupted attachments. When the attachment relation is activated in the transference with this population, it cues these traumatic memories and the result may be disorganized or dissociated responses. There is a consensus among attachment-informed therapists that this early activation of attachment in therapy should be avoided or side stepped to the extent possible until a base of cooperation and trust has been established that will allow for the gradual working through of these traumatic experiences (Bateman & Fonagy, 2004; Holmes, 2001; Liotti et al., 2008; Slade, 1999). A high degree of cooperation, mutuality and reciprocity is built into human intersubjectivity based on these representational abilities, but this mutuality is fragile. Clinical experience and a growing body of research (Bateman & Fonagy, 2004) is showing these representational abilities can temporarily collapse under severe psychological strainas when attachment trauma is activated (see below). Liotti et al. (2008) have described the same phenomena as the collapse of intersubjective abilities. If we are not in a position to establish a haven of safety and a secure base from which to explore because of a history of attachment trauma what can be done? We have other prosocial motivations to draw from that are not disorganizing, namely a desire to collaborate with the therapist in order to reduce suffering (the cooperative motive) and a desire to share experience with others who are seen as being like me (Kohuts mirroring and twinship selfobject needs). We can build on collaborative sharing motives by establishing joint therapeutic tasks that are not threatening, such as helping patients regulate intense affects by developing a better understanding of situations that might trigger disruptive emotions, establishing clear, consistent and exible boundaries, working toward reducing self-injurious and destructive behaviors by developing alternative selfsoothing techniques or any other therapeutic goals that can be agreed upon. These measures build a sense of trust and hope and create a reservoir of good will that we can draw from when the inevitable disruptions occur. Another approach we have been experimenting with is having two therapists collaborate closely in different settings in order to decrease the likelihood that disruptions with one therapist will terminate the treatment by having a secondary therapist provide additional support. The second therapist can be a psychiatrist who medicates the patient and is versed in dealing with this type of patient, a group therapist, a marital therapist or even another individual psychotherapist. The key to success is that both therapists share a common theory and approach to treating these challenging patients, that they respect each others work, and are in constant communication and consultation (Liotti et al., 2008).

Lessons Learned From Children Placed in Foster Care After Early Attachment Traumas
It is now well known that early relational traumas such as those caused by frightened and/or frightening caregiving behavior (Hesse et al., 2003), can lead to disorganization of early attachments. Attachment disorganization is characterized by interactions with care-

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givers in which the child is likely to experience fright without solution. This causes children (and also adults coming from histories of severe attachment disorganization) to tend to respond with anticipatory fear and/or dissociation whenever their attachment system becomes active (Hesse et al., 2003; Liotti, 1999, 2000, 2004). Particularly severe early traumas and institutional deprivation of stable caregiving can yield not only disorganization of attachment, but also indiscriminately friendly behavior toward strangers (OConnor, 2002). Controlling strategiesthat inhibit the attachment system through the defensive, vicarious activation of the caregiving system (inverted attachment) or of the ranking system with its punitive-dominant behavior (Liotti, 2004, pp. 480 481)seem the only solution these children can nd to avoid the repetition of fright and dissociation whenever the attachment system tends to become active. Descriptions of the controlling-caregiving and controlling-punitive strategies employed by children who had been disorganized in their infant attachments, have been provided by Hesse et al. (2003) and by Lyons-Ruth (2003). When the conditions for the activation of the attachment system are sufciently intense or prolonged, the relative inhibition by the defensive activation of the caregiving or the ranking system may be overcome. The disorganized representation of the attachment relation may then be activated, with its cohort of sometimes dramatic, frightening dissociative experiences (Hesse, 2003; Liotti, 1999; Liotti, 2000; Liotti, 2004; LyonsRuth, 2003). Clinicians treating children placed in foster care after repeated attachment injuries and severe abuse have noted extremely abnormal responses of these children when their attachment needs become active. These children also show decits in their capacity for joyful intersubjective exchanges. In these traumatized children, the dynamic relation between (a) poor intersubjective responses to opportunities for joyful intersubjective sharing, and (b) abnormal expression of attachment needs, is of an altogether different kind than observed in autistic children. Two clinical vignettes may illustrate the difference.8 A preadolescent girl was interviewed together with her foster parents after a night when she trashed her room in an uncontrollable storm of fear and rage. A few hours before, the child and her foster parents had enjoyed particularly happy exchanges, laughing together at the foster fathers funny stories of his years in college. They were able to relax afterward in front of the TV screen before going to their bedrooms for the night. This foster child was able to explain her behavior during the interview: I went into a panic last night because I thought we had been having fun. Fun is dangerous. The therapist thought that the little girl had felt particularly close to her foster parents during and after the positive intersubjective exchange. This closeness primed the activation of her attachment wishesa likely event when a child feels alone at night-time. In turn, this activation elicited, at an implicit level of mental functioning, her disorganized mental representations or internal working models (IWM) portraying memories of fright without solution. She intuited that there was a relationship between having had fun with her foster parents (positive intersubjective sharing) and expecting undened but catastrophically

These vignettes are the courtesy of Alec Clark, a London family therapist involved in the treatment of foster parents and children placed in their care after having been exposed to severe attachment traumas (Alec Clark, personal communication with Giovanni Liotti, May 7, 2007).

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negative events (activation of the IWM of a traumatic attachment), and drew the conclusion that fun is dangerous. Here is the second vignette. In the course of regularly scheduled consultations, a foster parent sends the therapist weekly reports on signicant exchanges between her and the six year old girl who has been placed in her care about one year before. The little girl, B., had been removed from a chaotic abusive household 3 years before. The following is an abstract from one of the foster-parents reports: B. loves to do my hair and pretend to paint my nails, and in return she loves me to do the same to her . . . Suddenly she said, I love you, I really do. I didnt want to spoil the moment so I said nothing but gently cradled her like a baby. A week later the foster-parent reported: B. started screaming as soon as I left the room, I f* hell hate you. Im going to f* punch you . . . owwwww . . . Im hurt now and its your fault. Its your fault I have hurt myself. According to the therapist, this little girl switches unpredictably, but almost on a daily basis, from joyful, playful exchanges with her foster parent to bouts of aggression, fear, and despair such as the one reported. The therapists formulation is that her foster parents offering of playful intersubjective exchanges accompanied by empathic attitudes (I gently cradled her like a baby) is weakening Bs controlling defenses, so that her attachment system becomes active and B is overwhelmed with memories expectations of pain and danger.

Concluding Remarks
We have shown that while attachment and intersubjectivity are intimately related through development, they can be distinguished on several evolutionary and developmental grounds. We argue that the most important evolutionary strategy driving human evolution was the emergence of cooperative groups that were able to share resources on an equal basis and therefore compete favorably with other groups (group selection). This evolutionary strategy most likely coevolved with cooperative breeding and life history strategies as Hrdy has persuasively argued. The emergence of a hypercooperative form of sociability required more effective communication between group members. A better understanding of the intentions and motives of other members assisted in joint cooperative planning of hunting and gathering activities among nomadic groups during the course of human evolution. Understanding intentions, motives and mental states of others takes place at an intersubjective level. This rich interpersonal and experiential matrix provides a fertile common ground upon which symbolic activities and language emerge. We use this evolutionary and developmental framework to further understand and rene the differences between attachment and intersubjectivity based on three conceptual arguments: (1) the distinction between domain-specic and domain-general adaptations, (2) the difference between tonic and phasic forms of activation and rules of activation and deactivation and, (3) the different hierarchical levels involving intersubjective motives (sharing and cooperating) and attachment motives. These differences lead us to expect different types of consequences resulting from the dynamic interplay between the two systems. Domain-specic motivational systems (attachment, caregiving, ranking, and sexual pairing systems) can generate powerful and intense emotions that can hinder positive intersubjective exchanges. Decits in positive intersubjective exchanges, such as observed in autism, involve less intense emotions, but can interfere with all the interpersonal motives. Exploring the clinical implications of these views is new

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territory. We hope the reections in this article will stimulate others to explore this fascinating terrain.

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