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provided by PubMed Central PERSPECTIVE ARTICLE published: 24 November 2009 EVOLUTIONARY doi: 10.3389/neuro.18.004.2009 : and emotional embodiment

Benjamin C. Campbell1* and Justin R. Garcia 2,3*

1 Department of , University of Wisconsin – Milwaukee, Milwaukee, WI, USA 2 Laboratory of Evolutionary Anthropology and Health, Departments of Anthropology and Biological Sciences, Binghamton University, Binghamton, NY, USA 3 Institute for Evolutionary Studies, Binghamton University, Binghamton, NY, USA

Edited by: The Decade of the Mind is a proposal for a research initiative focused on four areas of Steven M. Platek, neuroscience, including mental health, high-level cognitive function, , and computational Georgia Gwinnett College, USA applications. Organizing efforts to date have primarily included cognitive , computer Reviewed by: Robin Dunbar, Oxford University, UK scientists, and engineers, as well as physicians. At the same time have started Ralph L. Holloway, to explore the implications of neuroscience for understanding . Here we suggest that Columbia University, USA evolutionary neuroscience can be used to bridge knowledge obtained by social scientists with *Correspondence: that obtained in the for a more complete appreciation of the mind. We consider Benjamin C. Campbell, Department of such a perspective as neuroanthropology. We use embodiment, an anthropological concept that Anthropology, University of Wisconsin has been substantiated by recent fi ndings in neuroscience, to illustrate an integrative biocultural – Milwaukee, PO Box 413, Milwaukee, Wisconsin 53201, USA. approach within neuroanthropology and suggest future possible directions for research. e-mail: [email protected]; Keywords: embodiment, insula, evolution, , Justin R. Garcia, Laboratory of Evolutionary Anthropology and Health, Departments of Anthropology, Binghamton University, PO Box 6000, Binghamton, New York 13902, USA. e-mail: [email protected]

INTRODUCTION be complemented by evolutionary neuroscience. As shown below, The past few years have seen a call for interdisciplinary research on far from reducing embodiment to neural processes, a neurological the brain, including Decade of the Mind (DOM), an international and evolutionary perspective on embodiment open up new vistas initiative for basic neuroscience research on the mind including for neuroanthropologists to explore in studying mental health, high-level cognitive function, education, and intel- in experience. ligent machines (Albus et al., 2007). Despite DOM’s interest in moving brain research beyond the clinic, to date anthropological EMBODIMENT research has not been well represented in such interdisciplinary As defi ned by anthropologists, embodiment is the subjective experi- discussions. At the same time, however, there has been growing ence of the body, but not the physiological body (Csordas, 1990). As interest in incorporating neuroscience perspectives into anthropol- such, embodiment is generally considered to represent a culturally ogy, as exemplifi ed by the Encultured Brain Conference, Oct 8th generated experience of the body and has been approached ethno- 2009 at Notre Dame University. graphically (Csordas, 1990, 1994), including its expression in ritual Biological anthropology, with its concern for (Strathen and Stewart, 2008). However, because relies evolution (Falk, 2004; Holloway, 2008), has embraced the insights largely on verbal description, the term embodiment has traditionally of neuroscience into the origins of human cultural capacities been limited to philosophical and/or ethnographic discourse, and (Deacon, 1998; Rilling, 2008). , on the other carries post-modern connotations for many . hand, with its focus on cultural variation in human experience, has From the perspective of the neurosciences, the subjective been a philosophical holdout against “reductionist” neuroscience. experience of the body must logically be instantiated in the brain. However, recent research has made it clear that these three fi elds The neural questions underlying embodiment are clear: where is the have much to offer one another in creating a holistic conception subjective representation of body located and functionally processed of the role of the evolved brain in human culture – welcome the in the brain? And is such a representation highly integrative? A heading of neuroanthropology. highly integrative representation of subjective somatic experience Here we suggest that evolutionary neuroscience can be used to would make the neurological contribution to embodiment more bridge knowledge obtained by social scientists with that obtained compelling, yet still require environmentally-specifi c explanation in the neurosciences for a more complete appreciation of the in terms of variable expression. mind. More specifi cally, neuroscience can bring information about Understanding embodiment in terms of its neurological neurological mechanisms, evolutionary processes and correlates allows for more holistic investigation into both inter- context to enrich more traditional anthropological perspectives nal psychological and external socio-cultural factors. Thus, on human experience. To demonstrate this point, we provide an neuroanthropology becomes a truly consilient perspective by example of how our understanding of embodiment, a term used by which to tackle the cultural context of our evolved human anthropologists to denote the subjective experience of the body, can brain. The infusion of evolutionary principles into areas of

Frontiers in Evolutionary Neuroscience www.frontiersin.org November 2009 | Volume 1 | Article 4 | 1 Campbell and Garcia Neuroanthropology

neuroscientifi c investigation have spurred intellectually reward- The anterior cingulate and insula have been implicated in other ing theoretical and predictive study, as demonstrated by Platek, ritual healing practices as well. Ayahausca, a South American psy- et al. (2007) work on evolutionary as choactive plant tea, is known to have dramatic effects on bodily a new and emerging fi eld of inquiry. Similarly, neuroanthro- and emotional perceptions (Riba et al., 2001). Riba et al. (2006) pology combines input from evolutionary , behavioral report that the ingestion of ayahausca is associated with increased neuroscience, and , to attempt a deeper brain activity in the right anterior insula and the anterior cingulate appreciation of how the cultural context of the evolved brain cortex, consistent with previous fi ndings on the neural correlates can infl uence individual experience. of emotional embodiment, and empathy. Thus the ingestion of To begin to appreciate the of embodiment, Craig ayahausca by traditional shaman may be important in generating refers to embodiment in terms of recent fi ndings demonstrating an empathetic state that allows them to experience the feelings of the integration of somatosensory, homeostatic, and emotional affl icted individuals during their spirit journey and facilitate healing information within the insula – suggesting a specifi c location for (Dobkin de Rios, 1984). a global somatic representation (Craig, 2002, 2009). The insula Interestingly, the involvement of the anterior cingulate cor- cortex is part of the cerebral cortex and lies deep within the lat- tex and insula in meditation, yoga, and shamanic practices eral sulcus, overlain by the opercula. The insula is at the base of appears to be mirrored by the activation of both structures in the parietal lobe with important inputs from other sub-cortical long-term romantic relationships. This investigation is consist- structures including the thalamus, anterior cingulate cortex, and ent with Jankowiak and Fischer’s landmark study showing that amygdala (Craig, 2002). romantic love, although culturally and idiosyncratically variable, Such bodily representation is not to be confused with Penfi eld’s is a cross-cultural and human universal (Jankowiak and Fischer, famous homunculus map of the body represented in the cortex. 1992). Among individuals who reported being romantically in Rather, embodiment may be best thought of as somatic mood, love, the anterior cingulate cortex and insula cortex were not very a feeling that is not closely tied to language, perhaps helping to active during the fi rst 8 months (Aron et al., 2005), but become account for the subjective and elusive nature of its linguistic descrip- more active from 8 to 17 months (Aron et al., 2005; Fisher et al., tion. In its positive form, it may be thought of as well-being. We 2005). Further, Bartels and Zeki (2000) found that activation of will use the term emotional embodiment to distinguish the insular the anterior cingulate and insula cortex were clearly involved in representation from the use of embodiment in conjunction with feelings of romantic love among individuals who reported being in language and cognition (see for instance Clark, 2006). love for an average of over 2 years. Alcorte and Sosis (2005) argue that one defi ning experience of ritual is a feeling of intense joy EMBODIMENT AND RITUAL PRACTICES (ritual can also invoke powerful negative feelings as well), a fea- The insula and anterior cingulate cortex have been implicated in ture they associate with dopaminergic neurotransmission. Given recent studies of ritual spiritual practices, including meditation activation of insula and anterior cingulate cortex in meditation, (Lazar et al., 2005; Lutz et al., 2009), yoga (Kakigi et al., 2005), and yoga, ingestion of ayahausca, as well as romantic love, spiritual (Riba et al., 2006). Thus the neural correlates of emo- healing practices may, in fact, as many of them claim, draw on the tional embodiment not only refl ect our evolutionary heritage, but positive neurological experience of love. have become an object of cultural practice. In fact, fi ndings showing that individuals who are more aware of their own heart exhibit EVOLUTION, SOCIALITY, AND THE PRIMATE BRAIN greater activation in the insula and experience stronger emotions Rilling (2008) has suggested that anthropologists might make (Critchley et al., 2004), suggest that some individuals may be more their best contribution to a deeper understanding of the human intrinsically skilled at such practices than others. brain by concentrating on the neural basis of behaviors uniquely Recent fi ndings indicate that the relationship between emotion, developed in and critical to the evolution of the human the insula, anterior cingulate cortex, and autonomic nervous system brain, including language (Deacon, 1998), tool making (Stout and function is central to meditation. For instance, experienced com- Chaminade, 2007; Stout et al., 2008), mental perspective-taking passion meditators showed greater activation of the insula to nega- (Amodio and Frith, 2006), and altruism (Moll et al., 2006). We sug- tive sounds (Lutz et al., 2008) and such activation was more strongly gest that emotional embodiment, that is the global representation tied to heartbeat relative to novices (Lutz et al., 2009). Lazar et al. of bodily status as somatic mood, is also critical to the evolution of (2005) report increased thickness of the insula among meditators the human brain and deserves special focus from neuroscientists who focused on internal awareness, suggesting long-term inter- and anthropologists alike. nal awareness can lead to increased development of the neural Bodily awareness has been argued by numerous philosophers structures of embodiment. and neuroscientists, including William James and Antonio In a more exotic example, Kakigi et al. (2005) investigated brain Damasio, as the basis of human consciousness (see Prinz, 2004 activity in a Japanese yoga master who claimed to be impervious for a more recent example). The insula and anterior cortex is to while meditating. They report decreased activity in the not only central to elements of somatic awareness, such as pain insula and anterior cingulate cortex during meditation relative to (Singer et al., 2004; Jackson et al., 2006) but also to empathy a non-meditative state, regions already mentioned to be central to (Lamm et al., 2009), racial group identity (Xu et al., 2009), social the emotional aspects of pain (Singer et al., 2004; Jackson et al., norm violation (King-Casas et al., 2008), and moral intuitions 2006). More such studies are needed to see if such fi ndings are (Woodward and Allman, 2007), thus linking somatic awareness common among yogis who claim similar powers. to social emotions.

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Based on anatomical evidence, Craig (2002) argues that the fairness may seem a long step from bodily awareness, it represents incorporation of C and Aδ nerve fi bers into the spinothalamic a logical extension of threats to bodily awareness into the social lamina I tract provides with an integrated representation sphere, or “social embodiment” (Singer, 2007). To the extent that of physiological status not found in other mammals. Such fi bers others’ actions threaten bodily survival they are unlikely to be arise from nearly every cell of the body, including some that respond experienced as “fair”. Activation of the ACC under laboratory to lactic acid in muscle and provide information about peripheral conditions of social exclusion (Eisenberger et al., 2003) suggests metabolism processes. Furthermore, among primates, the termi- that fairness may be linked to survival because group exclusion nation of the tract in the posterior ventromedial nucleus with the is perceived as potentially threatening to survival. thalamus (VMpo) means that all such information is integrated The salience of the neural correlates of emotional embodiment in a single location providing a global emotional representation of extends to vocalization, language, and music, all important ele- the body (Craig, 2002). ments in ritual. Recent studies indicate that the insula is active Compared to anthropoid primates however, the representation in the response to the prosody or emotional content of language of somatic status appears to be elaborated in humans. Humans (Dietrich et al., 2008; Quadfl ieg et al., 2008; Ethofer et al., 2009), exhibit a relatively larger VMPo. While in non-human primates laughing and crying (Sander and Scheich, 2005), and music listen- some of the spinothalamic lamina I neurons go directly to the ing (Brown et al., 2004). In fact, music and speech perception over- orbitofrontal cortex, in humans, they all pass through the insula, lap in the insula (Brown et al. 2006), and the dorsal anterior insula in particular the right anterior insula (Craig, 2002). This allows may be specifi c for processing language and auditory information for a fuller representation of somatic status, which is then passed (Mutschler et al., 2009). While language may facilitate social com- on to the orbital frontal cortex where it serves as an hedonic input munication among larger human groups, its role in social cohesion for decision-making (Wallis, 2007). is linked to emotional elements of vocalization clearly expressed in The social brain hypothesis holds that it is the demands of com- laughing, crying, and music. plex social interactions in groups that have spurred the adaptive increase in brain size across the biological order Primates (Dunbar, EMBODIMENT AND BRAIN DEVELOPMENT 1998, 2009), a relationship not found in other mammalian orders Biological anthropologists are particularly attuned to substantial (Shultz and Dunbar, 2007). The importance of bonding among population variation in somatic growth based on energy balance primates would explain why affi liation through physical touch (the difference between consumption and output) related to sub- initiates a neurochemical cascade, involving oxytocin and opiates, sistence patterns and cultural consumption practices (Stinson, that is positively reinforcing and fundamental to effective social 2000). However, much less attention has been given to the poten- cohesion (Dunbar, 2010). While such neuroendocrine mechanisms tial impact of energetics for population variation specifi cally in remain important in human social interaction, they do not appear terms of brain development. This refl ects an assumption that suffi cient to explain group cohesion among humans for whom the brain is prioritized for energy (Fehm et al., 2006) and hence language and technology form the foundation for greatly expanded should suffer little from variation in energy supply (Campbell, spheres of social interaction. in press). Humans and the great apes (), but not other primates, However, given that the development of the prefrontal cortex exhibit Von Economo neurons (VENs) linking both the fronto- during the fi rst 15 years of life is directly related to glucose utiliza- insular and anterior cingulate cortex (ACC) to other areas of the tion (Chugani, 1998), and that cortical development is a sequential prefrontal cortex (Nimchinsky et al., 1999). The density of VENs hierarchical process (Gogtay et al., 2004; Shaw et al., 2008), brain is related to the degree of sociality exhibited across the four genera development may be more sensitive to fl uctuations in energy avail- of great apes – (Pongo), gorillas (Gorilla), ability than currently considered (Vaynman and Gomez-Pinilla, (Pan), and humans (Homo). These fi ndings suggest a potentially 2006). More specifi cally, given that the insula and ACC exhibit similar role for emotional embodiment in complex social behavior, elevated glucose utilization relative to the prefrontal cortex from together with similarities in the prefrontal cortex, between humans the age of 6 years into the 20’s (Van Bogaert et al., 1998), food and the other great apes (Semendeferi et al., 2002). availability may have important implications for the development In humans, the neural correlates of emotional embodiment of emotional embodiment and hence empathy, notions of fairness, appear to be particularly well developed. Along with a large and and artistic development. well developed insula (Craig, 2009), humans demonstrate both There is relatively little evidence linking chronic undernutri- greater density of VEN linking the ACC and insula relative to the tion to specifi c aspects of brain development in humans. However, apes (Nimchinsky et al., 1999) as well as the presence of VEN in recent fi ndings demonstrate altered insula activity in anorexia the dorsolateral prefrontal cortex (Fajardo et al., 2008). Allman nervosa (Nunn et al., 2008; Kaye et al., 2009). Altered insula activity and colleagues (Allman et al., 2001; Woodward and Allman, 2007) is related not only to changes in the taste of food, but also distorted suggest that limbic/cortical connections through VENs provide a self-body perception (Sachdev et al., 2008). In addition, the size neural pathway for rapid processing of complex social information of the ACC is reduced in AN (Mühlau et al., 2007; McCormick which they argue underlies so-called moral intuition (Woodward et al., 2008), an effect that appears to refl ect the degree of weight and Allman, 2007). loss (Mühlau et al., 2007) and is reversible with weight gain Importantly, both the insula and ACC are active in response to (McCormick et al., 2008) Importantly, both the ability to indentify the perception of fairness in social interactions (Hsu et al., 2008; emotions (Miyake et al., 2009), and impaired cognitive set shifting Tabibnia et al., 2008; Chiao et al., 2009). While the notion of (Zastrow et al., 2009) among individuals with AN have been related

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to alteration in the ACC, among other structures. Together these much more diffi cult, because of a lack of brain imaging techniques fi ndings implicate the ACC and insula in body perception, emotion, that can be used in the fi eld. Thus much of the investigation of and intellectual performance, a combination of traits suggestive of emotional embodiment in traditional will have to rely emotional embodiment. on indirect methods, including questionnaires, neuropsychological AN is a chronic pathological condition and hence represents tests, genetic and hormonal markers, and inferences from labora- an extreme case for the potential malleability of the insula and tory based brain imaging studies. ACC in brain development. However, Kar et al. (2008) recently For instance, among male Arrial pastoralists from northern reported that a small sample of chronically unnourished children Kenya, self-reported quality of life, which may be thought of as a aged 5 to 10 years from India show reduced cognitive function. measure of well-being, is predicted by the number of male sup- Defi cits included attention, working memory, learning and mem- porters as well as amount of body fat (Campbell unpublished ory, and visuospatial ability but not motor speed and coordination. data). Other fi ndings demonstrate that DRD4 7R+ is positively Furthermore, while attention scores increased with age among the related to BMI among nomadic Ariaal males (Eisenberg et al. 2008) malnourished children, those of design fl uency, working memory, while salivary T is positively related to measures of body fat in visual construction, learning and memory did not. The authors the same men (Campbell et al., 2007). Whether such biomarkers conclude that chronic malnutrition specifi cally underlies defi cits are also related to quality of life through their association with in higher cognitive functions. somatic status deserves more a detailed investigation of health, These results are especially important because the ages of 5 to well-being and subjective mood among Ariaal men based on 10 years coincide with middle childhood, a time of elevated glu- genetic variation in and salivary steroids, as cose utilization and overall brain plasticity (Chugani, 1998), as well well as cultural ideals. as important changes in social, emotional, and intellectual skills (Piaget, 1963), including the development of reason and respon- SUMMARY sibility (White, 1996). Thus given the hierarchical and sequential There is growing excitement among neuroscientists and social sci- nature of cortical maturation (Gogtay et al., 2004; Shaw et al., entists alike about the possibility of investigating the brain proc- 2008), alterations in brain development during this stage may have esses underlying those capacities for culture that seem uniquely important consequences for the long-term maturation of emotion, human. We suggest here that an evolutionary framework for such social emotion, and morality. a neurological perspective on the human brain highlights a pre- Surprisingly, the role of physical activity in brain development existing primate neural system of emotional embodiment as a key may be particularly relevant in our own . Recent work point- element in human sociality. The phylogenetic elaboration of bodily ing to the importance of motor activity in the early development of awareness helps to suggest the elaboration of human romantic love the brain (Diamond, 2001) as well as the impact of physical exercise into a wider set of positive social emotions and moral sentiments on learning in both school age children and adults (Ploughman, that act to maintain the cohesion of larger groups. In addition, it 2008) are consistent with the continued importance of elevated suggests that practices such as meditation, yoga, and shamanism levels of physical exercise thought to characterize our hunting and are based on activating the neurological mechanisms associated gathering ancestors (Vaynman and Gomez-Pinilla, 2006). Thus the with such positive social emotions. simple recognition of the importance of physical activity for learn- The investigation of cultural variation’s infl uence on neu- ing and the detrimental effects of a sedentary lifestyle as associated roplasticity is in its infancy. An evolutionary approach sug- with video games and heavy use of the internet may do more for gests that the role of culture in human is not reviving our education and health care systems than any other a recent event, but extends throughout human brain evolution single brain based pedagogical programs. (Deacon, 1998). Hence the role of metabolic constraints (Fehm FUTURE RESEARCH DIRECTIONS et al., 2006) is crucial to an evolutionary understanding of the way in which empathy and other social emotions are linked to Cultural neuroscience is already revealing important dichoto- somatic states. Thus the investigation of traditional with mies in the activation of brain regions for such basic behaviors as deeply engrained cultural practices, high levels of habitual physi- response to fear faces (Chaio et al., 2008) as well the valuation of cal activity, and low caloric intake, has a critical role to play in dominant and subordinate behaviors (Freeman et al., 2009) based neuroanthropology. However, the lack of suitable brain imaging on differences between Western and Eastern cultures. Such results methods for the fi eld means that such investigations, for now, demonstrate that cultural conditions can lead to discernable differ- will have to rely on indirect methods and courageous attempts ences in the specifi c cues that activate fundamental brain structures at interdisciplinarity. such as the amygdala and mesolimbic reward pathways. We expect that similar comparisons of Western and Eastern cultures directed toward understanding the role of the ACC and insula in such top- ACKNOWLEDGMENTS ics, as ritual, group identity, and romantic love will reveal similar The authors thank Leslie Heywood for supportive discussion and differences based on habitual experience. comments, along with Paul Brodwin and two anonymous review- Extending such studies directly to traditional societies in which ers for helpful comments on an earlier draft of this article. We also undernutrition, habitual levels of physical exercise, and even para- thank our Neuroanthropology colleagues for valuable discussion sitic infections may represent important inputs in somatic mood, is (see http://neuroanthropology.net/).

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The child’s entry into the use, distribution, and reproduction in any alimbic activation following aya- biological and cultural factors. In: age of reason. In The fi ve to seven year medium, provided the original authors and huasca, the pan-Amazonian inebriant. : An Evolutionary shift: the age of reason and responsibil- source are credited.

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