Author's Personal Copy

Author's personal copy Neuroscience and Biobehavioral Reviews 35 (2011) 1042–1051 Contents lists available at ScienceDirect Neuroscience and Biobehavioral Reviews journal homepage: www.elsevier.com/locate/neubiorev Review Human threat management systems: Self•protection and disease avoidance Steven L. Neuberg a,∗, Douglas T. Kenrick a, Mark Schaller b a Department of Psychology, Arizona State University, Tempe, AZ 85287•1104, United States b Department of Psychology, University of British Columbia, Vancouver, BC, Canada V6T 1Z4 article info abstract Article history: Humans likely evolved precautionary systems designed to minimize the threats to reproductive fitness Received 8 March 2010 posed by highly interdependent ultrasociality. A review of research on the self•protection and disease Received in revised form 18 August 2010 avoidance systems reveals that each system is functionally distinct and domain•specific: each is attuned Accepted 18 August 2010 to different cues; engages different emotions, inferences, and behavioral inclinations; and is rooted in somewhat different neurobiological substrates. These systems share important features, however. Each Keywords: system is functionally coherent, in that perceptual, affective, cognitive, and behavioral processes work Self•protection in concert to reduce fitness costs of potential threats. Each system is biased in a risk•averse manner, Disease avoidance Threat management erring toward precautionary responses even when available cues only heuristically imply threat. And Precautionary psychology each system is functionally flexible, being highly sensitive to specific ecological and dispositional cues Evolutionary psychology that signal greater vulnerability to the relevant threat. These features characterize a general template Domain specificity useful for understanding not only the self•protection and disease avoidance systems, but also a broader Fear set of evolved, domain•specific precautionary systems. Disgust © 2010 Elsevier Ltd. All rights reserved. Prejudice Stigma Social cognition Motivation Error management Contents 1. Introduction and overview . ................................................... 1043 2. The self•protection system . ................................................... 1043 3. The disease avoidance system . ................................................... 1045 4. Features common to the self•protection and disease•avoidance systems . .............................. 1047 5. Final comments . ................................................... ................................. 1049 Acknowledgements. ................................................... ........................... 1049 References . ................................................... .................................... 1049 In the second half of the 20th century, cognitive scientists made result is not only a great number of cognitive and behavioral mech• great progress by thinking of the brain in computational terms. anisms for efficiently and effectively apprehending and interacting Although the brain is indeed an information•processing device, it with the world, but also a set of predictable information process• is not a mere computer. Rather than being designed by engineers ing errors and biases, including many related to the ways humans to process information in a dispassionate manner, the human brain perceive and respond to other people. has been designed by natural selection to be something of a motiva• Evolutionary models of human social cognition explicitly tional device to promote adaptive behavioral responses to critical consider the cognitive and affective implications of different challenges directly related to survival and reproductive fitness. The fitness•relevant threats faced by ancestral populations; in doing so, these models have been able to generate and parsimoniously explain a wide range of empirical discoveries about the links among motivation, cognition, and behavior. ∗ Corresponding author. Tel.: +1 480 965 7845; fax: +1 480 965 8544. Consider, for example, the following findings: prejudices against E•mail address: [email protected] (S.L. Neuberg). African American men are characterized by fear, whereas prej• 0149•7634/$ – see front matter © 2010 Elsevier Ltd. All rights reserved. doi: 10.1016/j.neubiorev.2010.08.011 Author's personal copy S.L. Neuberg et al. / Neuroscience and Biobehavioral Reviews 35 (2011) 1042–1051 1043 udices against gay men are characterized by physical disgust and olfactory cues that distinguish between edible and poisonous (Cottrell and Neuberg, 2005 ). People who feel particularly vulner• fruits), ancestral humans also evolved sensory, affective, cognitive, able to disease have fewer friends with physical disabilities ( Park and behavioral mechanisms that respond functionally to fitness• et al., 2003 ). When Canadians (especially those who believe that relevant features in the social ecology. Some of these mechanisms the world is a dangerous place) find themselves suddenly in the are designed to promote affiliative and/or nurturant behaviors dark, they judge Iraqis to be less trustworthy, but no less intel• toward specific categories of individuals, such as potential mates or ligent ( Schaller et al., 2003a ). Women are especially ethnocentric apparent offspring ( Kenrick et al., 2001; Lieberman et al., 2007; Park and xenophobic during their first trimester of pregnancy, compared et al., 2008 ). But other mechanisms are designed to facilitate avoid• to their second or third trimester ( Navarrete et al., 2007 ). And, ance of or protection against other specific categories of individuals after seeing photographs that make germs and infections salient, (i.e., people who, either intentionally or unintentionally, pose some people view themselves as less extraverted and less open to new threat to one’s reproductive fitness). We focus here on two of these experiences ( Mortensen et al., 2010 ). precautionary systems— self•protection and disease avoidance . At first blush, these findings seem like a list of interesting, but Our review reveals that the self•protection and disease avoid• largely disconnected, curiosities in the realm of social cognition. In ance systems are functionally distinct psychological systems. Each fact, however, the implications of these findings are much broader. system is characterized by a coordinated suite of mechanisms When viewed within an integrative conceptual context spanning adaptively attuned to the perception of specific kinds of threat• the cognitive, social, and biological sciences, they contribute to signaling cues (e.g., angry facial expressions, skin rashes). When a growing scientific literature documenting the existence of two perceived, these cues arouse specific kinds of emotional reactions functionally distinct threat management systems, one devoted to (fear, disgust) and activate specific kinds of cognitive associations self•protection and the other to disease avoidance. We review this into working memory (e.g., inferences about hostile intent, infer• literature to draw inferences about the core features of these two ences about contamination). Consequently, they motivate specific systems. In addition, we suggest that these core features also char• forms of behavioral response (e.g., escape, avoidance of contact). acterize other neurocognitive systems that evolved in response to Moreover, each system is rooted in a somewhat distinct set of additional ancestral threats to survival and reproductive fitness. physiological structures and neurochemical processes. An important conclusion is that human threat detection and threat management is defined not by any singular system, but 1. Introduction and overview instead by a set of functionally distinct domain•specific systems, each of which was designed by evolutionary processes to respond From an evolutionary perspective, an organism’s ultimate goal in particular ways to particular kinds of perceptual cues that con• is reproductive fitness. For Homo sapiens , reproductive fitness has note a particular form of threat. The psychology of threat is most historically been enhanced by success in attaining a recurrent set of aptly characterized as the evolved psycholog ies of threat s (plural). “fundamental” behavioral goals that have clear implications for sur• In addition to the domain•specificity characteristic of evolved vival and reproduction (e.g., resource acquisition, self•protection, precautionary systems (and evolved cognitive systems more gen• disease avoidance, social affiliation, status, mate acquisition, mate erally; Barrett and Kurzban, 2006 ), our review also emphasizes retention, kin•rearing; Kenrick et al., 2010 ). In keeping with this several other features that the self•protection and disease• evolutionary logic, contemporary human psychology is character• avoidance systems have in common. Each system is functionally ized by functionally distinct cognitive and behavioral systems that coherent, in that perceptual, affective, cognitive, and behavioral effectively address these fundamental challenges ( Bugental, 2000; processes work together to reduce fitness costs of potential threats. Kenrick et al., 2003 ). Each system is biased in a risk•averse manner, erring toward pre• Many of these fundamental goals are fundamentally social , in cautionary responses even when available cues only heuristically that the attainment of the goal depends necessarily on the pres• (and often wrongly) imply threat. Each system is highly sensitive ence and actions of other people. Furthermore,

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