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AMERICAN JOURNAL OF HUMAN BIOLOGY 24:123–129 (2012) Original Research Article ‘‘Theory of Food’’ as a Neurocognitive Adaptation JOHN S. ALLEN* Dornsife Cognitive Neuroscience Imaging Center, Brain and Creativity Institute, University of Southern California, Los Angeles, California 90089-1061 ABSTRACT Human adult cognition emerges over the course of development via the interaction of multiple critical neurocognitive networks. These networks evolved in response to various selection pressures, m
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  Original Research Article  ‘‘Theory of Food’’ as a Neurocognitive Adaptation JOHN S. ALLEN*  Dornsife Cognitive Neuroscience Imaging Center, Brain and Creativity Institute, University of Southern California, Los Angeles,California 90089-1061  ABSTRACT  Human adult cognition emerges over the course of development via the interaction of multiple criticalneurocognitive networks. These networks evolved in response to various selection pressures, many of which were modi-fied or intensified by the intellectual, technological, and sociocultural environments that arose in connection with theevolution of genus Homo . Networks related to language and theory of mind clearly play an important role in adult cog-nition. Given the critical importance of food to both basic survival and cultural interaction, a ‘‘theory of food’’ (analogousto theory of mind) may represent another complex network essential for normal cognition. I propose that theory of foodevolved as an internal, cognitive representation of our diets in our minds. Like other complex cognitive abilities, it relieson complex and overlapping dedicated neural networks that develop in childhood under familial and cultural influen-ces. Normative diets are analogous to first languages in that they are acquired without overt teaching; they are also dif-ficult to change or modify once a critical period in development is passed. Theory of food suggests that cognitive activ-ities related to food may be cognitive enhancers, which could have implications for maintaining healthy brain functionin aging. Am. J. Hum. Biol. 24:123–129, 2012. ' 2012 Wiley Periodicals, Inc. Normal human behavior depends on mastering a num-ber of complex cognitive abilities that integrate multiplesensory, motor, perceptual, attentional, and experientialdomains (Gazzaniga, 2000). Although these abilities arein many ways neurologically hard-wired, they typicallyemerge over a normative course of development in child-hood. This development must occur in an environmentthat is at least minimally supportive of neurocognitivegrowth and maturation. The neural networks underlyingthese abilities that develop in childhood become the foun-dations for adult cognition. Although these cognitive abil-ities are remarkably complex, they become ‘‘second na-ture’’ once mastered. For example, compare the apparentease with which people acquire their first language withthe gear-grinding difficulty of second language learningthat occurs after the critical developmental period duringchildhood.Language development highlights a salient fact aboutthese complex cognitive abilities in humans: they can bestrongly influenced by the cultural environment. The neu-rocognitive biology of language, with its brain regions andnetworks dedicated to the production and perception of language, suggests that this ability is hard-wired andlikely evolutionarily adaptive (Pinker, 1994). However,the specific languages that people speak are of coursedetermined by the cultural environment. Furthermore,there is increasing evidence that language structure mayhave a deep-seated influence on cognition in myriad ways(Boroditsky, 2011). Although other complex cognitiveactivities are less obviously culturally or environmentallyinfluenced, that does not mean that they are not shapedby the developmental context. Consider something as fun-damental as walking. Although much of the neurologicalcontrol of gait occurs at the subcortical level, the planningand organization of walking behavior is initiated in thefrontal cortex (Sheridan and Hausdorff, 2007). The neuro-cognitive networks involved with walking are both hard-wired and shaped by the environment in which they areformed. The cultural component of that environmentmust make some contribution to the neurological develop-ment of gait control, even if it is relatively minor com-pared with other factors.This article is not about walking and talking but aboutfood and eating. I will argue that how humans ‘‘think’’food—the neurocognitive underpinnings of how we goabout deciding what is food and eating it—is similar infundamental ways to these other complex cognitive activ-ities. Like language, how people think about the food theyacquire, process, and eat develops in a biologically norma-tive way, but its final expression is significantly shaped bythe cultural environment. In the same way that languageis apparently effortless and naturally produced by humanspeakers, people typically have a ‘‘normal’’ diet that seemsas natural as breathing. Only when a diet is changed bycircumstance or choice does its deep-seated cognitive foun-dation become apparent.In general, food is as important to human survival asreproduction, social behavior, or technological prowess.Since the hominin lineage split from the great apes, diethas clearly been a significant factor in the evolution of various hominin types. For example, one of the majorbranches of the hominin family tree, the robust australo-pithecines, was distinguished by a dental and cranialanatomy that likely represented an adaptation to a dietthat was increasingly reliant on grasses and sedges, com-pared with a more typical ape-ish diet (Cerling et al.,2011; Sponheimer et al., 2006).One of the early hominins that apparently did not godown this grassy path was ancestral to Homo , a genus Contract grant sponsor: National Institute of Neurological Disordersand Stroke; Contract grant number: NS 19632.*Correspondence to: John S. Allen, Dornsife Cognitive NeuroscienceImaging Center, Brain and Creativity Institute, University of SouthernCalifornia, Los Angeles, CA 90089-1061, United States.E-mail: jsallen@usc.eduReceived 19 September 2011; Revision received 15 November 2011; Accepted 16 November 2011DOI 10.1002/ajhb.22209Published online 19 January 2012 in Wiley Online Library (wileyonlinelibrary.com).  AMERICAN JOURNAL OF HUMAN BIOLOGY 24:123–129 (2012) V V C 2012 Wiley Periodicals, Inc.  characterized by dental reduction and increased brainsize, among other traits. Changes in diet have long beenhypothesized to have been of critical importance in theevolution of  Homo , especially in terms of providingadequate nutrition to grow and support a large brain(Aiello and Wheeler, 1995; Allen, 2009). Increases in meator marine resources or tubers have all been hypothesizedto be critical factors in increasing the quality of the homi-nin diet (Crawford et al., 1999; Langdon, 2006; Milton,2003). The development of technological skills importantfor procuring or preparing food has long been thought tohave an important role in a positive feedback loopbetween technology and increased cognitive ability. Forexample, Wrangham (2009) has argued that cooking withfire was instrumental in increasing the quality of the hom-inin diet by making meat and certain plant foods morenutritionally accessible. Overall, the cognitive flexibilityand adaptability that emerged concomitant withincreased brain size contributed to an expansion or diver-sification of the diet of  Homo , which in turn allowed forthe migration to and settlement of a range of environ-ments in the Old World (Ungar et al., 2006).So whatever the precise nature of their contributions orinfluences, food and diet were obviously both generallyand specifically critical for the evolution of human brainand behavior. The mind that emerged during this evolu-tion was unique in its creative scope and intelligence(however defined); it constructed a sociocultural environ-ment that was just as critical to shaping human adapta-tions as the ecological environment. Some of these adapta-tions, such as language, are essentially cognitive in na-ture, and thus the mind is both the shaper of and shapedby the biocultural, selective environment.For humans, the dietary environment is also fundamen-tally shaped by the cultural and cognitive environments.Human diets, in all their variety, do not consist simply of the accessible, edible, and familiar but are the product of nutritional, cultural, and cognitive imperatives (see forexample, Jones, 2007). The complexity of the human dietas a mental phenomenon suggests that like language andother complex cognitive abilities, mastering it requires acombination of implicit and explicit learning over thecourse of childhood development. I suggest that whatemerges during this process is a cognitively unified per-spective on diet—a ‘‘theory of food’’ (ToF)—that synthe-sizes a variety of mental processes, including those relatedto homeostatic monitoring, the senses, memory, emotion,and categorization (Allen, 2012). THEORY OF FOOD IS ANALOGOUS TO THEORY OF MIND Language provides one model of the kind of complexcognitive ability that may be represented by ToF. How-ever, a better model may be found in the influential hy-pothesis known as ‘‘theory of mind’’ (ToM). Comparativepsychologists David Premack and Guy Woodruff intro-duced the ToM concept in 1978 (Premack and Woodruff,1978a,b). They were interested in comparing the cognitionof chimpanzees and humans in terms of their ability topredict or estimate or impute the mental states of others.ToM provided them with a means of comparing cognitionacross these two species.Premack and Woodruff argued that to be able to func-tion in an interactive social group, especially one com-posed of such socially complex creatures as human beings,an individual needs to have an implicit theory about themental states of others. Social actors need to be able tomake judgments about the motives or veracity of thesocial actions of others. A more formal way of saying thisis that people are ‘‘endowed with a representational sys-tem that captures the cognitive properties underlyingbehavior’’ (Leslie, 2000, p 1235). Premack and Woodruff said that the ‘‘theory’’ part of ToM is in recognition of thatfact that it reflects both a state of mind that is not observ-able by outsiders and it is used by individuals to predictthe behavior of others. ToM is a complex cognitive abilitythat has been shaped by natural selection in response tothe evolution of, and in, interactive social environments.Like language, ToM appears to undergo a fairly predict-able process of development in children, with increasingsophistication with increasing age. Numerous tests havebeen developed to examine different types and levels of ToM ability in children (Leslie, 2000). Children as youngof 4 years of age have no problem discerning a false belief (in another social actor) in experimental settings. Even bythe age of 2 years, children are quite expert at determin-ing if another individual is pretending. For example, a 2-year-old child seeing her mother speak into a banana asthough it is a telephone knows that the mother is pretend-ing. This knowledge reflects the child’s (accurate in thiscase) ToM about the mother’s mental state.ToM has become an important focus for research inmany fields. In psychiatry, it has been widely used toassess social function in conditions such as schizophreniaand, especially, autism (Baron-Cohen, 2000; Pickup,2008). ToM deficits emerge in autistic children at 18months or even earlier, leading to what Baron-Cohen(2009) calls a kind of ‘‘mind-blindness.’’ People with au-tism or Asperger syndrome are unable to mind-read: theyhave difficulty imagining the thoughts and feelings of others. Thus ‘‘they find other people’s behavior confusingand unpredictable, even frightening’’ (Baron-Cohen, 2009,p 69).The presence of ToM deficits in autism suggests that aneurobiology of ToM exists, and that it is not working cor-rectly. Unfortunately, research on autistic individuals hasnot led to the identification of a specific affected region orregions. In fact, neuroimaging research on ToM has shownthat many brain regions and networks are potentiallyactive during ToM activities, varying according to experi-mental tasks (Carrington and Bailey, 2008). Parts of thefrontal lobe (the medial prefrontal cortex/orbitofrontalregions) and the superior temporal lobe are activatedmost consistently in these studies, suggesting that theyare more critical than other areas for ToM, but not always.Like other complex cognitive functions, ToM seems to bedependent on a widely distributed, overlapping complex of neural networks. ToM emerges from the combined inter-actions of these various networks. A model proposed by Marcel Adam Just and Sashank Varma (2007) attempts to account for the dynamic proc-esses in the brain that underlie forms of complex cogni-tion, such as ToM or ToF. They start with a basic principle,which is generally agreed upon by all cognition research-ers: ‘‘Thinking is the product of the concurrent activity of multiple brain areas that collaborate in a large-scale corti-cal network’’ (p 154). According to Just and Varma, thesecortical networks change according to the demands of thethinking-related task. Although there is some specializa-tion in the cortex, cortical areas can generally perform 124 J.S. ALLEN  American Journal of Human Biology  multiple functions, and different functions can be per-formed in multiple cortical areas. This flexibility allowsnot only for the reformation of networks following braininjury but also for the dynamic recruitment of regions toattend to tasks on a regular basis. Although the brainmay develop primary neural networks for specific complexcognitive tasks, variations on a theme are possiblebecause of the recruitment of different cortical areas to-ward similar—but not identical—goals.The forms of these flexible and complex large-scale neu-ral networks are ultimately shaped by natural selectionand proximately shaped by the developmental environ-ment. The organization of the neural networks underlyingcomplex cognitive abilities such as language or ToM isclearly not reformulated de novo in each individual basedon the developmental environment; on the other hand,they are not so hard-wired that they cannot accommodatedevelopmental variability. For humans and some otherprimates, such as chimpanzees (Call and Tomasello,2008), the social dimension is one of the most criticalaspects of these environments; hence, it is reasonable tohypothesize that something like ToM has evolved as a cog-nitive adaptation to this environment. Similarly, food isalso a critical aspect of the human biocultural environ-ment. The very complexity of the human diet, in its nutri-tional, physiological, ritual and symbolic, emotional, tech-nological, and social contexts, suggests the adaptivepotential in uniting these various cognitive strands into ahigher level ToF network. THEORY OF FOOD ToF is an internal, cognitive representation of our dietsin our minds. My hypothesized ToF is analogous to ToMand shares with it many of the basic features of complexcognition. ToM evolved because humans (and other prima-tes) live in highly interactive social groups that place apremium on the ability to read the minds of other socialactors. Similarly, our ToF evolved not only because food isimportant for survival and we must learn how and whatto eat as we grow up but because our complex language-based cultural environment embeds food in an extensiveweb of other cognitive associations. All primates to some extent learn how to eat as theygrow up, observing what their mothers and other mem-bers of their social group do with food items (Fragaszy and Visalberghi, 2004). ToF, like ToM, is not necessarilyunique to humans. However, I suggest that like ToM, oursociocultural environment and enhanced cognitive abil-ities take ToF to a level that is not seen in other primates.In the same way that the sexual dichotomies of biologybecome the continuum of gender under culture and sexualreproduction goes from being between a male and a femaleto a social institution, food and eating are much morethan ingestion and digestion. Although physiology is obvi-ously important, the sociocultural context (and ultimatelythe cognitive context) has just as large a role in definingwhat is and is not food and what should or should not beeaten. Humans need a ToF not simply for sustenance butto make use of one of the basic currencies of human socialexistence (Counihan and van Esterik, 2008; Harris andRoss, 1987).Similar to ToM and language, the form of an individu-al’s ToF is likely shaped during a critical period in child-hood. Developmental psychologists have long charted thenormal progression of diet development from infancythrough weaning and the transition to more adult tablefoods. This period of ‘‘early life programming’’ has beenundergoing increased scrutiny with the onset of the obe-sity epidemic in the developed world (Cottrell andOzanne, 2008). The importance of the food environmentduring this developmental stage for establishing lifelongfood habits (both psychological and physiological) is high-lighted by the fact that researchers are targeting this pe-riod for potential obesity interventions (Anzman et al.,2010). Targeting this critical period for dietary interven-tion is tacit recognition of the fact that ‘‘first diets,’’ likefirst languages, have a privileged place in both minds andbodies.Like ToM, an individual’s ToF is necessarily shaped byboth genetic and environmental factors. Individualgenetic variation likely plays a role in shaping someaspects of ToF. For example, individual genetic variationin tasting ability is reasonably common. There are ‘‘super-tasters,’’ individuals who are highly sensitive in labora-tory testing to the chemical propylthiouracil [PROP—which is similar in structure to phenylthiocarbamide(PTC)] (Duffy, 2007). These individuals (most of whom arewomen) do not simply experience PROP as bitter, likemost people do, but intensely bitter. Their sensitivity isprobably the result of the fact that they have increasednumbers of taste structures on the tongue (fungiform pap-illae and taste pores). These supertasters are also moresensitive to the creaminess of fat and oral pain (Duffy,2007). Another possible axis of variation that could influ-ence ToF involves the dopamine reward pathways in thebrain. These pathways have become of increasing interestto diet and obesity researchers as the idea of ‘‘food addic-tion’’ has gained popularity (Corsica and Pelchat, 2010;Pelchat, 2009). Studies on both on both rats and humanssuggest that some dopamine receptor variation is corre-lated with obesity and eating behavior (Johnson andKenny, 2010; Stice et al., 2009; Wang et al., 2001). ToF,like all forms of complex cognition, will therefore varyamong individuals because of both genetic and environ-mental factors.Just as it has been difficult to identify a unitary ToMbrain neural network, it will probably also be impossibleto pinpoint a single network that accounts for ToF. SinceToF can be as much about not eating as eating, we wouldnot even predict that those parts of the brain associateddirectly with ingestion should form a sort of default net-work. The absence of a single dedicated neural networkinvolving regions x , y , and z in a predictable sequence doesnot mean that there cannot be an evolved propensity fordeveloping a ToF. Complex cognitive processes, such aslanguage and ToM, are undoubtedly adaptations, and thecomplex, distributed nature of the networks underlyingthese processes is no barrier to their concerted functionalevolution (for networks associated with language, see BenShalom and Poeppel, 2008; Price, 2000). We are in theearly days of understanding the biological basis of com-plex cognition. Historically, experimental methods havenecessarily favored understanding them via the separatecomponents of individual networks rather than as anintact operating system involving multiple, interactingnetworks. With functional neuroimaging, the componentsof networks and even their interactions (Zielinski et al.,2010) are beginning to be understood. And with toolsavailable to identify these kinds of networks, more of  125 THEORY OF FOOD  American Journal of Human Biology  them will be discovered, beyond the ‘‘obvious’’ ones suchas those involved with language.Like many aspects of human biology, ToF did not evolvein a modern, agricultural, industrial food environment(Lindeberg, 2009). The ‘‘normal’’ developmental environ-ment for ToF may therefore include limitations on theamount and availability of high quality, nutrient-densefoods, marked seasonality of foods contributing to greatervariety, and periods of food shortage. Almost all adult indi-viduals in traditional environments (both hunter-gathererand traditional agricultural) likely had an understandingof the processes of food acquisition and preparation, fromthe hunt or harvest to eating. Meals would often be takenwith members of extended kin groups rather than cen-tered on the nuclear family. Food was more connected toreligion and ritual activities.Michael Pollan (2008) has argued that in the modern di-etary environment, people think more in terms of nutrients than food, which has in turn has led to confusionand ambiguity about what should or should not be eaten.This is to some extent an example of the tyranny of choiceand affluence, although dietary concerns and the obesityepidemic cut across all socioeconomic levels in the devel-oped world (McAllister et al., 2009). Thinking of food asnutrients only removes it from the broader contexts inwhich ToF evolved. Although it is difficult to say howexactly factors such as seasonality, familial connections,ritual, and so on might specifically influence the develop-ment of ToF, it is clear that food and eating have in manyways been removed from multiple traditional and evolu-tionary contexts.Taken as a whole, the modern food environment is insome ways relatively impoverished compared with a moretraditional environment when it comes to people’s rela-tionship with their food. It is not impoverished in thesense of calories or nutrients available, anything but.However, starting in childhood, many people only eat asmall number of foods by choice, which appeal to themlargely for their fat or sugar content (Birch and Fisher,1998); there is no need to have a more expansive palategiven the ready availability of highly palatable, energy-dense foods. In most developed countries, the social andritual contexts of food consumption have been de-empha-sized. While there is no doubt that some foods and mealsmaintain ritual significance in developed societies (e.g.,Siskind, 1992), the cultural significance of food and foodhabits is much more pervasive in traditional societies(e.g., Holtzman, 2009). Another issue is that where food isabundant, and there is reasonable certainty of its continu-ous availability, eating becomes divorced from hunger.Emotional eating, eating only to push the pleasure but-tons in the brain, eating out of boredom, or to put off doingsomething else—these are all options that would havebeen rare in the evolutionary past (Allen, 2012). All of these factors mean that the typical ToF a person mighthave today in the modern, developed world is not only justdifferent from a more ‘‘traditional’’ ToF in content but alsofundamentally different in terms of its underlying cogni-tive associations. THEORY OF FOOD: SOME IMPLICATIONS ToF may have srcinally evolved in hunter-gatherer andtraditional agricultural environments, but most people donot live under those conditions today. For people living inthe current food and eating environment of the developedworld, ToF will have implications that are quite differentfrom what they might have been in the past. As mentionedearlier, it is the prevailing opinion of nutritionists, publichealth officials, clinicians, and others who worry about thehealth of nations, that too many people in the developedworld are too fat, and that the problem is getting worserather than better (Kessler, 2009; Power and Schulkin,2009). Losing weight generally requires dieting, and asmost people are aware, dieting is difficult. Individuals whoare successful weight loss maintainers (SWLs)—who loseat least 13 kg and keep it off for at least a year—are inter-esting enough as a research population that a nationalregistry of them is maintained in the United States. Func-tionalimagingresearchonSWLshasshownthattheyacti-vate the frontal lobes much more when looking at imagesof food items compared with normal weight and obese indi-viduals (McCaffrey et al., 2009). This suggests that SWLsare more able (for whatever reason) to exert conscious, ex-ecutive control over their dietary choices than those whoare less successful for gaining weight. Their implicit ToFhas been to some extent successfully replaced or supple-mented byamore explicit mode ofcontrol.ToF provides one perspective for understanding whydieting is so difficult. It forms as children grow up and im-plicitly acquire knowledge and habits associated with foodand eating. In the same way that children acquire theirfirst language, ToF becomes enmeshed in the cognitivemakeup of an individual. Adopting a new diet, in effectmodifying a ToF, is to some extent like learning a secondlanguage, except more so—it is like replacing a first lan-guage with a new one. ToF is likely not as cognitivelyingrained as language, but changes in it nonetheless couldhave profound effects on overall cognition. At the individ-ual level, ToF enmeshes the things we eat in a larger cog-nitive web. The human species’ basic behavioral plasticityand flexibility means that new foods and dietary patternscan be adopted. However, changes of this kind take timeand effort, especially if the components of the old dietremain readily available. Obviously, contingency is anissue here. People will readily change their diets if the al-ternative is extreme hunger or starvation, although evenin times of extreme food shortage, there are often cultur-ally prescribed responses to such shortages (Farb and Armelagos, 1980). Variation in personality traits and sensory preferencesshould influence variation in the formation of ToF. Linksbetween risk for alcoholism and heightened hedonicresponse to sweet taste and high novelty seeking (Langeet al., 2010; Mennella et al., 2010) indicate a complexinterrelationship among personality factors in terms of the consumption of food and psychoactive substances.Interrelationships of this kind suggest that while ToF isstrongly influenced by the external cultural and familialenvironments, it is also at the individual level a product of genetic predispositions. These predispositions, if theywere understood in the broader ToF context, could influ-ence clinical interventions regarding weight loss and con-trol. Although dieting is synonymous with restraining andrestricting food intake, in a more global cognitive sense, itis an expansion of the baseline repertoire of eating habits. A broader perspective on dietary change and modification,not simply focused on factors related to reducing food con-sumption, may actually help to inform the development of more successful behavioral interventions for weight loss. 126 J.S. ALLEN  American Journal of Human Biology
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