John T. Cacioppo

Although the quantitative logic and formal proofs of economics were appealing, the emphasis on forecasting rather than on delineating underlying mechanisms was less so. A serendipitous meeting with Lee Becker, a social psychologist at the University of Missouri, led Cacioppo to the medical school, where he conducted his ﬁrst study combin- ing physiological and social measures in investigating a psychological question. Cacioppo abandoned his plans to pursue a career in law and instead went to graduate school in social psychology at Ohio State University. Cacioppo’s mentors at Ohio State included Tony Green- wald, Tim Brock, Bob Cialdini, and John Harvey. Ca- cioppo also continued his studies of psychobiology and psychophysiology, working primarily with Curt Sandman with occasional but always memorable visits to John and

broadly. Bea Lacey at the nearby Fels Research Institute in Yellow Springs, Ohio. Perhaps the most influential person he met publishers. at Ohio State, however, was another first-year graduate student, Richard Petty. By the end of their first week in allied disseminated its graduate school, Cacioppo and Petty were arguing in- be of tensely about everything. To save money, they rented a to one John T. Cacioppo dilapidated house and covered an entire wall with black- not or is Award for Distinguished Scientific Contributions board paint to work through their various arguments. These

and experiences drove home two points that have shaped Ca- cioppo’s thinking for the remainder of his career. First, user Citation

Association complex social behaviors have multiple antecedents within “For his pioneering research within social psychology and and across levels of organization; as such, comprehensive within psychophysiology, and especially for bringing these

individual accounts of social cognition, emotion, and behavior require worlds together. John T. Cacioppo’s penetrating insights

the the speciﬁcation of both multiple causal mechanisms and Psychological of into the fundamental relations between psychological and moderator variables that govern the conditions under which

use physiological levels of analysis have provided a conceptual they operate. Second, the identiﬁcation of complex ante- road map for the hybrid disciplines of social psychophysi- cedents and mechanisms across levels of organization re- American ology and social neuroscience. His methodological innova- quires transdisciplinary research. Comprehensive accounts personal the tions in the use of psychophysiological measures to make of social behavior, therefore, are more likely to come from the by inferences about the biological consequences of social pro- collaborative, integrated programs of scientiﬁc research. for cesses have revolutionized thinking about mind–body in- Cacioppo received his doctor of philosophy degree from teractions. He has made outstanding, programmatic, and solely Ohio State University in 1977 and joined the University of copyrighted integrative contributions to the understanding of evaluative Notre Dame’s department of psychology as an assistant is processes, individual differences in cognitive engagement, professor that year. He moved to the University of Iowa in intended loneliness, and the fundamental relation between the sym-

is 1979 and was promoted to associate professor in 1981 and pathetic and the parasympathetic nervous systems. All of

document to professor in 1985. The colleagues and students at Notre

article his endeavors are characterized by conceptual and analytic Dame and Iowa were stimulating and supportive, and both This precision and deep insights into the fundamental nature of departments were sufﬁciently small that Cacioppo was ex- This relations between psychological and biological levels of posed to yet a wider array of approaches, perspectives, and analysis.” levels of analysis. Cacioppo’s collaboration with Petty also expanded during this period: They coauthored books and Biography articles on, among other things, the elaboration likelihood John T. Cacioppo is the third of four children born to model of attitudes and persuasion and individual differ- Cyrus and Mary K. Cacioppo and the ﬁrst in the family to ences in cognitive motivation (“need for cognition”) with attend college. At the insistence of a math teacher, Ca- an emphasis on the role of need for cognition in attitude cioppo participated in a select summer mathematics pro- formation and changes. gram at the University of Missouri while in high school, During this era, social and biological approaches to be- leading him to complete his bachelor of science degree in havior were typically depicted as antagonistic or mutually economics at the University of Missouri in 1973. exclusive. Cacioppo and Petty, therefore, also spent consid-

November 2002 ● American Psychologist 817 Copyright 2002 by the American Psychological Association, Inc. 0003-066X/02/$5.00 Vol. 57, No. 11, 817–831 DOI: 10.1037//0003-066X.57.11.817 erable time in these early years debating the abyss between of analysis. Because this approach built on a long tradition social and biological levels of analysis and how best to of theoretical and empirical work in the neurosciences, bridge it. By the mid-1980s, the impact of Cacioppo’s psy- cognitive sciences, and social sciences, Cacioppo and chophysiological analyses of social processes led Richard Berntson termed the field social neuroscience. Louttit, the director of the Behavior and Neuroscience In the early 1990s, Cacioppo and Berntson also initiated (BNS) Division of the National Science Foundation, to studies on autonomic organization and function, emphasiz- seek his help in fostering this type of research. The result ing the implications of the heterarchical organization of the was a pioneering five-year program developed and imple- brain and central nervous system for understanding the au- mented by Cacioppo that, as Louttit noted when honored tonomic substrates of stress and affect. Among the numer- by the American Psychological Association for distin- ous findings from this work was that metabolic (e.g., ortho- guished contributions to psychology, became one of the stasis) and psychological (e.g., active coping) stress, jewels of the BNS Division’s funding history. More than although appearing comparable in nomethetic analyses, 40 illustrious scholars (a number of whom became editors were organized quite differently. This led Cacioppo and of leading journals in the field) completed the program be- Berntson to begin an innovative collaboration with Jan tween 1986 and 1991. Kiecolt-Glaser, Ron Glaser, and Bill Malarkey to examine

broadly. Preparation for and lectures to these scholars demanded the role of social and autonomic factors in individuals’ en- the development of more sophisticated, comprehensive, and docrine and cellular immune responses to stress and illness publishers. integrative formulations, and these demands resulted in vulnerability. Cacioppo and Berntson also extended their several conceptual advances. Cacioppo and Louis Tassi- work on the heterarchical organization of the central nervous allied disseminated its nary, an exceptional postdoctoral fellow from Dartmouth system to develop a new theoretical perspective on attitudes, be of College working with Cacioppo during this period, pulled affect, and affective processing in their model of evaluative to one together the major components of the program in an edited space. In 1995, Cacioppo joined the John D. and Catherine T. not or is volume; formalized the problem of mapping across social, MacArthur Foundation Research Network on Mind–Body

and cognitive, and biological levels of organization; and, to- Interactions led by Bob Rose. This led to an expansion of his gether with Gary Berntson, developed a handbook whose research examining how personal relationships get under the user

Association coverage ranged from the physics of functional magnetic skin to affect social cognition and emotions, personality pro- resonance imaging to social relationships and processes. cesses, biology, and health. As before, the students and post-

individual With Elaine Hatﬁeld and Richard Rapson, Cacioppo coau- doctoral fellows with whom Cacioppo worked made seminal

the thored a book on emotional contagion; in collaboration contributions to each of these formulations. Psychological of with Richie Davidson, he organized a small focused scien- In 1999, Cacioppo moved to the University of Chicago

use tiﬁc meeting for the James S. McDonnell Foundation on to build a social psychology program in the Department of new approaches to the study of affect and emotion; and Psychology. As the Tiffany and Margaret Blake Distin- American with Michael Coles, Berntson, and Steve Crites, he evolved guished Service Professor at the University of Chicago, personal the an event-related brain potential procedure to investigate Cacioppo cofounded the Institute for Mind and Biology the by component processes underlying evaluative categorizations with Martha McClintock to support multilevel integrative for and affective processes. analyses of social behavior. He has maintained extramural

solely Cacioppo returned to Ohio State University in 1989 to funding for his work throughout his career, and among his copyrighted join the social psychology and psychobiology programs, distinctions are the National Academy of Sciences Troland is the latter of which was directed by Berntson. Prior to Research Award, the Society for Psychophysiological Re- intended

is meeting, Cacioppo and Berntson had each established pro- search’s Distinguished Scientiﬁc Award for an Early Ca-

document grams entailing multiple levels of analysis. Over a series of reer Contribution to Psychophysiology, the Society for Per-

article early morning coffees, Cacioppo and Berntson discovered sonality and Social Psychology’s Donald Campbell Award This they shared a conviction regarding the importance of multi- for distinguished scientific contributions to personality and This ple levels of analysis, and the two began collaborative re- social psychology, and the Society for Psychophysiological search integrating levels of organization from the social to Research’s Award for Distinguished Scientific Contribu- the neural. They quickly developed a deep mutual intellec- tions to Psychophysiology. He is a fellow in five different tual respect and friendship, mirrored in the quality of the divisions in the American Psychological Association and in collaboration, which drove perspectives from different lev- six other scientific societies, and he has served as the presi- els equally with none subservient to the others. Early in dent of the Society for Personality and Social Psychology, their collaboration, Cacioppo and Berntson articulated a the Society for Consumer Research, and the Society for logic and set of principles for a science concerned with the Psychophysiological Research. He and his colleagues con- relationship between neural and social processes, including tinue to forge new bridges across neural and social levels the intervening information-processing components and of organization and to examine the intervening informa- operations at both the neural and the computational levels tion-processing components and operations at both the neu-

818 November 2002 ● American Psychologist ral and the computational levels of analysis. He has Cacioppo, J. T., Tassinary, L. G., & Berntson, G. G. worked with over a hundred students, postdoctoral fellows, (2000). Handbook of psychophysiology (2nd ed.). New and colleagues and still leaves research meetings amazed at York: Cambridge University Press. his good fortune in having such wonderful and brilliant colleagues with whom to interact. Crawford, L. E., & Cacioppo, J. T. (2002). Learning where to look for danger: Integrating affective and spatial Selected Bibliography information. Psychological Science, 13, 449–453. Berntson, G. G., Cacioppo, J. T., & Quigley, K. S. (1991). Crites, S. L., Jr., & Cacioppo, J. T. (1996). Electrocortical Autonomic determinism: The modes of autonomic control, differentiation of evaluative and nonevaluative the doctrine of autonomic space, and the laws of categorizations. Psychological Science, 7, 318–321. autonomic constraint. Psychological Review, 98, 459–487. Hatﬁeld, E., Cacioppo, J. T., & Rapson, R. L. (1994). Cacioppo, J. T. (1994). Social neuroscience: Autonomic, Emotional contagion. New York: Cambridge University Press. neuroendocrine, and immune responses to stress. Psychophysiology, 31, 113–128. Kosslyn, S. M., Cacioppo, J. T., Davidson, R. J., Hugdahl, broadly. K., Lovallo, W. R., Spiegel, D., & Rose, R. (2002). Bridging psychology and biology: The analysis of publishers. Cacioppo, J. T., & Berntson, G. G. (1992). Social psychological contributions to the Decade of the Brain: individuals in groups. American Psychologist, 57, 341–351. allied Doctrine of multilevel analysis. American Psychologist, 47, disseminated its Petty, R. E., & Cacioppo, J. T. (1981). Attitudes and

be 1019–1028. of

to persuasion: Classic and contemporary approaches. one

not Cacioppo, J. T., & Berntson, G. G. (1994). Relationship Dubuque, IA: Brown. or is between attitudes and evaluative space: A critical review,

and with emphasis on the separability of positive and negative Petty, R. E., & Cacioppo, J. T. (1986). Communication and persuasion: Central and peripheral routes to attitude

user substrates. Psychological Bulletin, 115, 401–423.

Association change. New York: Springer-Verlag. Cacioppo, J. T., Berntson, G. G., Adolphs, R., Carter, C. S., Sarter, M., Berntson, G. G., & Cacioppo, J. T. (1996).

individual Davidson, R. J., McClintock, M. K., et al. (2002). Founda- Brain imaging and cognitive neuroscience: Toward strong

the tions in social neuroscience. Cambridge, MA: MIT Press. Psychological of inference in attributing function to structure. American

use Cacioppo, J. T., Berntson, G. G., Sheridan, J. F., & Psychologist, 51, 13–21. McClintock, M. K. (2000). Multilevel integrative analyses American of human behavior: Social neuroscience and the Uchino, B. N., Cacioppo, J. T., & Kiecolt-Glaser, J. K. personal the complementing nature of social and biological approaches. (1996). The relationship between social support and the by Psychological Bulletin, 126, 829–843. physiological processes: A review with emphasis on for underlying mechanisms and implications for health. Cacioppo, J. T., & Dorfman, D. D. (1987). Waveform Psychological Bulletin, 119, 488–531. solely

copyrighted moment analysis in psychophysiological research. is Psychological Bulletin, 102, 421–438. intended is Cacioppo, J. T., & Gardner, W. L. (1999). Emotion. Social Neuroscience: Understanding the Pieces document Annual Review of Psychology, 50, 191–214. Fosters Understanding the Whole article

This and Vice Versa

This Cacioppo, J. T., & Petty, R. E. (1981). Electromyograms as measures of extent and affectivity of information John T. Cacioppo processing. American Psychologist, 36, 441–456. University of Chicago Cacioppo, J. T., Petty, R. E., Feinstein, J., & Jarvis, W. B. G. (1996). Dispositional differences in cognitive motivation: The life and times of individuals varying in need for cognition. Psychological Bulletin, 119, 197–253. Social science and neuroscience perspectives represent two ends of a continuum of levels of organization studied in Cacioppo, J. T., & Tassinary, L. G. (1990). Inferring psychology. Human behavior as a whole unfolds at social psychological signiﬁcance from physiological signals. levels of organization, whereas much of the research in American Psychologist, 45, 16–28. psychology has focused on cognitive and biological pieces

November 2002 ● American Psychologist 819 of this whole. Recent evidence underscores the to sustain scientiﬁc progress (see, e.g., Wilson, 1998). complementary nature of social, cognitive, and biological Needless to say, social and cultural forces and their impact levels of analysis and how research integrating these levels on human cognition, emotion, and behavior were far too can foster more comprehensive theories of the mechanisms important to await the full explication of cellular and mo- underlying complex behavior and the mind. This research lecular mechanisms, so social and biological perspectives underscores the unity of psychology and the importance of each developed, for the most part, insulated from develop- retaining multilevel integrative research that spans molar ments in the other (see Berntson & Cacioppo, 2000). and molecular levels of analysis. The 20th century was a time of remarkable advances within the neurosciences, cognitive sciences, and social sciences (see, e.g., Gilbert, Fiske, & Lindzey, 1998; Kandel Neuroscientists and cognitive scientists have collaborated & Squire, 2000; Wilson, 1998). As science enters the 21st for more than a decade, with the common goal of under- century, scientists are in a position to move beyond simpli- standing how the mind works. These collaborations have fying assumptions, as evidenced by the emergence of per- helped unravel puzzles of the mind including aspects of spectives such as social neuroscience (see, e.g., Cacioppo, perception, imagery, attention, and memory (see, e.g., Kan- 1994; Cacioppo & Berntson, 1992; Cacioppo, Berntson, et del, 2001; Kosslyn & Andersen, 1992; LeDoux, 1995; Pos-

broadly. al., 2002; Klein & Kihlstrom, 1998; Ochsner & Lieberman, ner & Raichle, 1997). Many aspects of the mind, however, 2001; Sternberg, 2000), to develop more comprehensive publishers. require a more comprehensive approach to elucidate the theories of mind and behavior. The purpose of this address mystery of mind–brain connections. Attraction, altruism, is to review the emergence, breadth, and logic of this allied

disseminated speech recognition, afﬁliation, attachment, attitudes, identi- its perspective. be of ﬁcation, kin recognition, cooperation, competition, empa- To be clear from the outset, all human behavior at some to one thy, sexuality, communication, dominance, persuasion, obe- level is biological, but this is not to say that biological re- not or

is dience, morality, contagion, nurturance, violence, and ductionism yields a simple, singular, or satisfactory expla- person memory are just a few. and nation for complex behaviors or that molecular forms of The notion that 100 billion neurons can give rise to the representation provide the only or best level of analysis for user

Association human mind can be daunting, especially when trying to say understanding human behavior. Molar constructs such as anything more speciﬁc about this feat. To simplify the those developed by the social sciences provide a means of study of the mind, many scientists have ignored the social understanding highly complex activity without needing to individual aspects. The architects of development and behavior were

the specify each individual action’s simplest components, Psychological of initially conceived in molecular biology as the forces of thereby providing an efﬁcient means of describing the be-

use evolution operating over millennia; the builders were cast havior of a complex system. Chemists who work with the as encapsulated within each living cell far from the reach periodic table on a daily basis nevertheless use recipes American of personal ties, social inﬂuences, or society; and the brain rather than the periodic table to cook not because food personal the was treated simply as an information-processing machine preparation cannot be reduced to chemical expressions but the by (Crick, 1970). The additional information that might be because it is not cognitively efﬁcient to do so. The scientist for attributable to the social world was conceived as best con- who uses social, cognitive, and biological levels of analysis sidered later, if the need arose (cf. Allport, 1947). Social solely to understand behavior is no more a dualist than a chemist copyrighted factors, it was further reasoned, might have minimal impli- who uses both culinary and chemical levels of analysis to is cations for basic development, structure, or processes of understand cuisine. intended the brain or mind, in which case the consideration of social is factors would be entirely irrelevant (Scott, 1991). Even if The Emergence of Social Neuroscience document

article relevant, the consideration of social factors might render Human survival depends in large part on the formation of This the study of the human mind and behavior too complicated alliances and accurate social judgments. Affiliation and This nurturant social relationships, for instance, are essential for physical and psychological well-being across the life span Editor’s Note (Cacioppo, Berntson, Sheridan, & McClintock, 2000). Dis- John T. Cacioppo received the Award for Distinguished ruptions of social connections, whether through ridicule, Scientific Contributions. Award winners are invited to de- separation, divorce, or bereavement, are among the most liver an award address at the APA’s annual convention. stressful events people endure (Gardner, Gabriel, & Diek- This award address was delivered at the 110th annual man, 2000; Kiecolt-Glaser, Glaser, Cacioppo, & Malarkey, meeting, held August 22Ð25, 2002, in Chicago. Articles 1998), and social isolation is as large a risk factor for based on award addresses are not peer reviewed, as they broad-based morbidity and mortality as high blood pres- are the expression of the winners’ reflections on the occa- sure, obesity, and sedentary lifestyles even after statistically sion of receiving an award. controlling for known biological risk factors, social status,

820 November 2002 ● American Psychologist and baseline measures of health (House, Landis, & Umber- al., 1999), evaluative and attitudinal processing (Cacioppo, son, 1988). Indeed, the effect size for social isolation and Crites, Berntson, & Coles, 1993; O’Doherty, Kringelbach, morbidity is as large as that for high blood pressure or Rolls, Hornak, & Andrews, 2001), social categorization obesity (House et al., 1988). The case of Phineas Gage in (Golby, Gabrieli, Chiao, & Eberhardt, 2001; Ito & Ca- the late 1800s vividly established the importance of the cioppo, 2000), attributional reasoning (Winston et al., frontal cortex for orchestrating normal social discourse 2002), moral reasoning (Greene, Sommerville, Nystrom, (Macmillan, 2000), and although the entire brain contrib- Darley, & Cohen, 2001), and theory of mind (Siegal & utes to the social enterprise, research in this area is yield- Varley, 2002). ing findings of very specific social behaviors related to cir- cumscribed regions (Adolphs, 1999; Winston, Strange, The Breadth of Social Neuroscience O’Doherty, & Dolan, 2002). Therefore, various authors Despite the impressive impact of the imaging technologies have argued that evolutionary forces operating over thou- on the funding and conduct of research over the past de- sands of years have sculpted the human genome to be sen- cade, it should be remembered that functional imaging sitive to and succoring of relationships with others, to be studies have significant limitations (Uttal, 2001) and ac- wary of others, and to recognize the intentions and predis- count for less than five percent of the studies reported at

broadly. positions of others (Cacioppo et al., 2000; Gould, 1980; recent Society for Neuroscience meetings (Lorig, 2000). Kropotkin, 1989) and that elementary cognitive operations The frontiers of cognitive and social neuroscience depend publishers. have evolved or been adapted to perform social functions fundamentally on the rigorous foundation of cellular and (Winston et al., 2002). allied molecular research (“The Public Face of Neuroscience,” disseminated its Within the cognitive and social sciences, it has long 2002). It is important, therefore, that advances within the be of been recognized that self-reports and overt behavior pro-

to neurosciences favoring the emergence of a social neuro- one vide incomplete information on the human mind (Cacioppo science perspective run deeper than brain imaging tech- not or is & Sandman, 1981; Nisbett & Wilson, 1977). Methods and niques (Sarter, Berntson, & Cacioppo, 1996).

and principles from the neurosciences have offered valuable Viewing the nervous, endocrine, and immune systems as additional information from which to draw inferences about operating outside the reach of sociocultural inﬂuences al- user

Association social and psychological processes (Cacioppo & Tassinary, lowed focused study of isolated anatomical systems with a 1990) and have contributed to (a) an appreciation for the resulting speciﬁcation of component structures and pro-

individual complexity of the mechanisms underlying social behaviors cesses. The simple marine mollusc Aplysia (e.g., sea slug),

the (see, e.g., Berntson, Boysen, & Cacioppo, 1993; Cacioppo for instance, has been the focus of innumerable studies of Psychological of & Berntson, 1994; Damasio, 1994; Phelps et al., 2000), (b) learning and memory in the neurosciences. The Aplysia has

use empirical tests of conﬂicting theoretical accounts of social only about 20,000 neurons in its system, less than behavior (see, e.g., Lieberman, Ochsner, Gilbert, & 0.00002% of those found in the human. Furthermore, the American Schacter, 2001; Winkielman & Cacioppo, 2001), (c) more neurons in the Aplysia, an invertebrate, are large and iden- personal the comprehensive accounts of mental and physical disease tiﬁable, and their organization is limited to a few ganglia, the by (Cohen, 1991, 1996; Harris, in press; Seeman, 2000; Tay-

for making systematic manipulation and observation of neural lor & Brown, 1988; Uchino, Cacioppo, & Kiecolt-Glaser, processes possible.

solely 1996), (d) an expanded understanding of physiological pro- The Aplysia californica has an oriﬁce (called a siphon) copyrighted cesses ranging from anabolic and catabolic processes (Ca- used to pump out waste and seawater; the siphon is located is cioppo, Hawkley, Crawford, et al., 2002; Taylor et al., near a gill used for breathing in the middle of its body. intended

is 2000) to immunology and disease (Glaser & Kiecolt-Gla- The siphon and gill are essential for the animal’s survival,

document ser, 1994; Seeman, Singer, Rowe, Horwitz, & McEwen, so an intense or threatening stimulus such as a jab to the

article 1997), and (e) conceptualizations of social phenomena gill or a shock to the tail results in a reflexive withdrawal This ranging from attachment, morality, and social prejudices to of these essential structures. A light touch to the gill does This social cognition and decision making (Adolphs, 1999; Ca- not initially elicit the siphon withdrawal reflex (SWR), but cioppo & Berntson, 2001; de Waal, 1996; Dolan, 1999; if a light touch to the gill is paired with a shock to the Frith & Frith, 2001). body (the conditioned stimulus and unconditioned stimulus, Corresponding developments within the neurosciences respectively), after repeated pairings a light touch is suffi- have also contributed to the emergence of social neuro- cient to elicit the SWR (a conditioned response). The Aply- science. One of the most obvious contemporary develop- sia fasciata has also served as a model for it changes its ments is brain imaging procedures such as positron emis- responsiveness to a food on the basis of whether or not it sion tomography, event-related brain potentials (ERPs), and succeeds in consuming it. Successful attempts to consume functional magnetic resonance imaging, which have been a palatable food lead to increased responsiveness to the used to examine social processes such as face recognition food, whereas failed attempts lead to decreased responsive- (Gauthier, Skudlarski, Gore, & Anderson, 2000; George et ness to the food. This simple and accessible neural cir-

November 2002 ● American Psychologist 821 cuitry, combined with a predictable behavioral repertoire, (Committee on Future Directions for Behavioral and Social has made the Aplysia a model for cellular studies of learn- Sciences Research at the National Institutes of Health, ing and memory (Kandel, 1979, 2001). 2001; Sternberg, 2000). As noted above, humans are not only information-processing machines, they are also social animals with devel- The Logic of Social Neuroscience opmental capacities for attachment (Maestripieri, 2001), These impressive advances in molecular biology and genet- speech and face recognition (Farah, Wilson, Drain, & ics make it easy to fall into thinking about an organism as Tanaka, 1998; Pascalis, de Haan, & Nelson, 2002), and indifferent to the physical and social environment and to representing their own and other people’s mental states conclude that the scientiﬁc study of mind and behavior is (Frith & Frith, 2001), and they require a web of interper- best pursued exclusively at the level of the gene or cell (cf. sonal relationships, alliances, and cultures to thrive Temple, McLeod, Gallinger, & Wright, 2001). The seminal (Baumeister & Leary, 1995; Cacioppo, Hawkley, Berntson, observations of Claude Bernard (1878/1974), Lewontin et al., 2002; Felthous, 1997). My colleagues and I therefore (2000), Gould (1980), de Waal (1996), MacLean (1985), reasoned that knowledge of biological and social domains and Kropotkin (1989) speak eloquently against such a no- may be necessary to develop comprehensive theories in tion, however (cf. Harris, in press). Bernard over a century

broadly. either domain. It is interesting that even the Aplysia fas- ago observed that the extracellular fluid constitutes the im- ciata spends most of its time in contact with conspecifics; mediate environment—the internalized sea—for plants and publishers. when isolated, the Aplysia actively locomotes toward con- animals. He noted the relative constancy of this internal specifics (Lederhendler, Herriges, & Tobach, 1977). In the allied milieu and regarded this constancy and the physiological disseminated its presence of conspecifics, the Aplysia stops responding to a mechanisms that serve to maintain it as providing protec- be of palatable food that is too tough to swallow (Susswein,

to tion against the powerful entropic forces that threaten to one Schwarz, & Feldman, 1986), but when these Aplysia are disrupt the biological order essential for life. Mammals are not or is socially isolated, this learning is blocked (Schwarz & Suss- far from being indifferent to their surroundings, Bernard

and wein, 1992)—an effect that has been found to be attribut- further observed, but must be in close and intimate relation able to the absence of pheromones secreted by conspeciﬁcs to them, continually compensating for and counterbalanc- user

Association (Schwarz, Blumberg, & Susswein, 1998). ing external variations. This interplay between organismic Much of the research in the neurosciences relies on ani- and environmental conditions is orchestrated at multiple

individual mal models, where problems of generalizing to humans are levels to maintain a balance within the organism. In Le-

the always a concern. Research on rats by Meaney and col- wontin’s (2000) terms, “organisms not only determine what Psychological of leagues has, for instance, revealed that transient early-life aspects of the outside world are relevant to them by pecu-

use stress (e.g., brief handling) attenuated the behavioral and liarities of their shape and metabolism, but they actively neuroendocrine responses to stressors encountered in adult- construct, in the literal sense of the word, a world around American hood, whereas early-life exposure to more severe stressors themselves” (p. 54). Additionally in humans, the physical personal the (e.g., protracted separation from the dam) accentuated re- environment has been shaped profoundly by the social the by sponses to stressors in adulthood (Anisman, Zaharia,

for world. Indeed, Dawkins (1990) has argued for a social Meaney, & Merali, 1998). The brief handling of rat pups equivalent of a gene, the meme, which is a unit of cultural

solely led to an increase in distress calls by the rat pups, greater information, such as a cultural practice or idea, that is copyrighted maternal nurturance, a consequent increase in glucocorti- transmitted verbally or by repeated action from one mind is coid receptor binding sites in the hippocampus and frontal to another, altering the course of a culture and those who intended

is cortex, and a subsequent lowering of hypothalamic–pitu- live in it.

document itary–adrenal reactivity in adulthood; severe early life stress Accordingly, increased collaboration among neuroscien-

article had the opposite effects (Anisman et al., 1998; Meaney et tists, cognitive scientists, and social scientists should be to This al., 1996). As adult rats, the offspring of mothers that ex- the benefit of all who are interested in behavior. Consider This hibited more licking and grooming and nurturance of pups the phenotypic expression of strains of mice with specific during the first 10 days of life were not only characterized genes inactivated (i.e., knockout mice), which is known to by reduced adrenocorticotropic hormone and corticosterone depend on the genetic background (see, e.g., Gerlai, responses to acute stress but also, as mothers, tended to 1996)—so much so that the effects of the social context lick and groom their pups more (Liu et al., 1997). In this were thought either to be unimportant or to alter pheno- way, brain anatomy and behavior were transmitted across types in a monotonic fashion (cf. Lewontin, 2000). Crabbe, generations via the influence of social behavior on genetic Wahlsten, and Dudek (1999) reported a remarkable finding expression and neural development rather than through the to the contrary. Six mouse behaviors (locomotor activity in transmission of different genotypes. Whether the develop- the open field, an anxiety test based on the exploration of ment of the human brain and behavior is affected similarly two enclosed and two open arms of an elevated plus maze, by transient early-life stressors is an active area of research walking and balancing on a rotating rod, learning to swim

822 November 2002 ● American Psychologist to a visible platform, locomotor activation after cocaine ponents, a focus on elementary components contributes to injection, and preference for drinking ethanol vs. tap water) an explanation only when considered in conjunction with were tested simultaneously in three laboratories using the events occurring at different levels of the system. Inter- same inbred strains and one null mutant strain. Large ge- ested readers may wish to see related discussions of the netic (strain) effects on all behaviors were found, which principles of multiple determinism, nonadditive determin- was expected because strains that were known to differ ism, and reciprocal determinism (Cacioppo & Berntson, markedly on the behavioral tasks had been chosen. Impor- 1992). tantly, despite the fact that Crabbe et al. “went to extraor- dinary lengths to equate test apparatus, testing protocols, The Elaboration of Basic ApproachÐWithdrawal and all possible features of animal husbandry” (Crabbe et Response Organizations al., 1999, p. 1670), signiﬁcant effects for site were found Evaluations underlying attitudes, affect, and preferences for nearly all behaviors, with the pattern of strain differ- have traditionally been conceptualized as a unitary process ences varying substantially for several behaviors. Crabbe et with simple components and representations accessible al. issued a cautionary note: “Experiments characterizing through self-reports (Osgood, Suci, & Tannenbaum, 1957; mutants may yield results that are idiosyncratic to a partic- Thurstone, 1931; cf. Cacioppo & Berntson, 1994). Reﬁned

broadly. ular laboratory” (Crabbe et al., 1999, p. 1670). From the feelings of approval/disapproval or admiration/condemna- present perspective, these data exemplify the point that un- tion may be foremost in human minds, but these feelings publishers. derstanding the behavioral manifestations of speciﬁc ge- represent the product of a host of resident processes that netic mutants may require a consideration of physical and allied have evolved over millennia. The study of evaluative pro- disseminated its social factors. In sum, understanding the whole should con- cesses, therefore, is an area in which understanding the be of tribute to an understanding of the pieces.

to pieces has contributed to understanding the whole and vice one The effects of the social context on phenotypic expres- versa. not or is sion are not limited to animal models. The full complement Like the Aplysia, humans are equipped with defensive

and of DNA is in each cell of the newborn, but evidence is withdrawal reﬂexes that can be classically conditioned for mounting that signals from the internal and external envi- protection from nociceptive stimulation. Differentiating user

Association ronment play an important role in the constitution and tran- hostile from hospitable others and events is such a critical scription of DNA and in the translation of RNA to proteins capacity that all animals have rudimentary reﬂexes for cat-

individual (see, e.g., Bronfenbrenner & Ceci, 1994; Gottlieb, 1998). egorizing and approaching or withdrawing from certain

the Wu, Devi, and Malarkey (1996) localized growth hormone classes of stimuli and for providing metabolic support for Psychological of messenger RNA (GH mRNA) in human immune organs, these actions (Berntson et al., 1993; Cacioppo & Gardner,

use including the thymus, lymph nodes, spleen, and peripheral 1999). Evaluative discriminations are performed in simple blood, as well in thymomas and lymphomas. The extant organisms by hardwired stimulus–response connections or American literature on growth hormone suggests that it can influence fixed action patterns. Human infants are also endowed with personal the cellular immunity by altering the efficacy of lymphocytes a finite set of hardwired evaluative discriminations—star- the by in responding to antigens. The genetic transcriptions re-

for tle-response to sudden intense noises and retreat from noci- sponsible for the production of lymphocyte growth hor- ceptive stimuli (Berntson et al., 1993). A remarkable fea-

solely mone (L-GH) are in part predetermined, as evidenced by ture of humans is the extent to which the evaluative copyrighted the robust ﬁnding that L-GH secretion decreases with ag- discrimination of stimuli is shaped by learning, cognition, is ing. However, Malarkey et al. (1996; Wu et al., 1999) also modeling, and culture (Petty & Cacioppo, 1981). intended

is found evidence for the modulation of L-GH levels by so- The 19th century neurologist John Hughlings Jackson

document cial stressors: Caregivers of spouses with Alzheimer’s dis- (1884/1958) emphasized the hierarchical structure of the

article ease had markedly lower L-GH concentrations compared brain and the re-representation of functions at multiple lev- This with age- and gender-matched controls. Stress hormones els within this neural hierarchy. Berntson and colleagues This such as adrenocorticotrophic hormone, cortisol, and cat- (Berntson, Cacioppo, & Sarter, in press; Berntson et al., echolamines are thought to play a role via their regulatory 1993) summarized evidence that primitive protective re- effects on lymphocytes (Wu et al., 1999), with recent work sponses to aversive stimuli are organized at the level of the raising the possibility that the kinetics as well as the level spinal cord, as is apparent in ﬂexor (pain) withdrawal re- of hormonal variations may affect lymphocyte function ﬂexes that can be seen even after spinal transaction. These (Cacioppo, Kiecolt-Glaser, et al., 2002). primitive protective reactions are expanded and embel- More generally, it may be unreasonable to assume that lished at higher levels of the nervous system. The evolu- complex systems such as the human organism can be un- tionary development of higher neural systems, such as the derstood as a simple extrapolation from the properties of limbic system, endowed organisms with an expanded be- their elementary components. Unless the properties of the havioral repertoire, including escape reactions, aggressive system are the simple sum of those of its elementary com- responses, and even the ability to anticipate and avoid

November 2002 ● American Psychologist 823 aversive encounters (Berntson et al., 1993). Evolution not tex lesions show preserved abilities to localize and discrim- only endowed human beings with primitive, lower level inate visual stimuli that are not consciously perceived adaptive reactions but also sculpted the remarkable infor- (blindsight). Second, neuroimaging studies have revealed mation-processing capacities of the highest levels of the correlations between amygdala, superior colliculus, and brain. Thus, neurobehavioral mechanisms are not localized pulvinar cerebral blood flow in masked (“unseen”) emo- to a single level of organization within the brain but rather tional conditions (see, e.g., Morris, O¨ hman, & Dolan, are represented at multiple levels of the nervous system. At 1999). Thus, although the striate cortex visual pathway progressively higher (more rostral) levels of organization affords high-resolution visual processing, the superior col- (spinal, brain stem, limbic, cortical regions), there is a gen- liculus and pulvinar pathway affords relatively fast but eral expansion in the range and relational complexity of low-resolution visual processing that can guide (motivate) contextual controls and in the breadth and flexibility of attention without intention or awareness (LeDoux, 1995). discriminative and adaptive responses (Berntson et al., Such an affective asymmetry serves to guide attentional 1993). and cognitive resources to potential threats in the environ- Adaptive flexibility of higher level systems has costs, ment even before they can be recognized (Smith et al., in given the finite information-processing capacity of neural press).

broadly. circuits (Berntson et al., in press). Greater flexibility im- The later ERP component, the LPP, is sensitive to sub- plies a less rigid relationship between inputs and outputs, a tler variations in stimuli ranging from foods (Cacioppo, publishers. greater range of information that must be processed, and a Crites, et al., 1993) and evocative pictures (Ito, Larsen, slower, serial-like mode of processing. Consequently, the Smith, & Cacioppo, 1998) to personality traits (Cacioppo, allied disseminated its evolutionary layering of higher processing levels onto Crites, Gardner, & Berntson, 1994; Crites, Cacioppo, Gard- be of lower substrates has adaptive advantage in that lower and ner, & Berntson, 1995) and racial categories (Ito & Ca- to one more efficient processing levels may continue to be used cioppo, 1999). The evaluative processes marked by LPP not or is and may be sufficient in some circumstances (Berntson, also can occur spontaneously (Ito & Cacioppo, 2000), un-

and Sarter, & Cacioppo, 1998). Higher neurobehavioral pro- coupled from verbal report (Crites et al., 1995), however. cesses, however, can come to suppress or bypass pain In an illustrative study, Ito and Cacioppo (2000) assessed user

Association withdrawal reﬂexes (Boysen, Berntson, Hannan, & Ca- the implicit and explicit categorization of stimuli along cioppo, 1996). If an individual unknowingly touches a hot evaluative (pleasant, unpleasant) and nonevaluative (people,

individual ﬂame, the individual reﬂexively withdraws his or her hand no people) dimensions. Participants were exposed to stim-

the from the painful ﬁre. If, however, the person hears a child uli that simultaneously varied along both dimensions, but Psychological of on the other side of a wall of ﬂames, he or she can over- half the participants were instructed to count the number of

use ride this defensive reflex and push through the flames. This pictures that depicted people or the absence of people is neither the only nor the most likely action that such an (nonevaluative categorization task), and half were in- American individual would take; instead, he or she would likely structed to count the number of pictures that depicted personal the show a more flexible, contextually appropriate response pleasant or unpleasant scenes (evaluative categorization the by such as looking for a doorway or passage to the child that task). As in prior research, the LPP was sensitive to partic- for was not engulfed by flames or donning fire-retardant cover- ipants’ explicit categorization task. For instance, the LPP

solely ing (e.g., wet blanket) before challenging the ﬂames to re- was larger in the evaluative task when a pleasant picture copyrighted trieve the child. was presented within a series of unpleasant pictures than is My colleagues and I have used ERPs in variations of within a series of pleasant pictures and when an unpleasant intended

is the oddball paradigm to study evaluative processes, with a picture was presented within a series of pleasant pictures

document small positive (P1) component emerging within 140 ms than within a series of unpleasant pictures, and the LPP

article over the corresponding sensory cortex (e.g., occipital re- was larger in the evaluative task when an unpleasant pic- This gion for visual stimuli; Smith, Cacioppo, Larsen, & Char- ture was presented within a series of pleasant pictures than This trand, in press) and a functionally and stochastically sepa- when a pleasant picture was presented within a series of rate late positive potential (LPP) emerging several hundred unpleasant pictures (i.e., the negativity bias; cf. Cacioppo, milliseconds later and peaking approximately 600 ms after Gardner, & Berntson, 1999; Peeters & Czapinski, 1990; stimulus onset over associative cortex (centroparietal re- Taylor, 1991). gions; Cacioppo, Crites, et al., 1993). More interestingly, the LPP also revealed implicit cate- The P1 component is sensitive to negative stimuli and gorization along the non-task-relevant dimension—with to affectively congruent stimuli (Smith et al., in press). clear evidence of an implicit negativity bias in which rare Two sources of evidence have led to the hypothesis that a aversive stimuli spontaneously received greater processing neural circuit involving the superior colliculus, posterior than rare appetitive stimuli. The explicit task of categoriz- pulvinar nucleus, and amygdala underlies the P1 negativity ing stimuli along a nonevaluative dimension neither dimin- bias (Smith et al., in press). First, patients with striate cor- ished nor delayed the LPP to variations in the evaluative

824 November 2002 ● American Psychologist dimension. As would be expected at low levels of hedonic them if the stimulus word presented was positive and to activation, the negativity bias and implicit categorization pull the lever toward them if the stimulus word was nega- effects have not been observed when using mildly evocative; other participants received the opposite instructions. tive experimental stimuli such as words (pleasant, unpleas- Results confirmed that participants were faster to respond ant; Cacioppo, Crites, & Gardner, 1996; Crites & Ca- to positive stimuli when pulling the lever rather than push- cioppo, 1996) rather than more evocative emotional ing the lever and faster to respond to negative stimuli when pictures (see, e.g., Ito & Cacioppo, 2000; Ito et al., 1998). pushing rather than pulling the lever. In a second study, These results suggest the operation of adaptively beneficial Chen and Bargh removed the conscious goal to evaluate implicit categorization processes, triggered by significant the stimuli: Half the participants pushed and half pulled the proximal stimuli, serving broad, cross-situational goals. lever as quickly as possible when a word appeared. As in The attitudinal and behavioral implications of the heter- the prior study, participants who were instructed to push archical organization of evaluative processes have also the lever in this simple reaction-time task were faster in been examined (see, e.g., Boysen et al., 1996). An implica- response to negative than to positive stimuli, and those tion of the rapid operation of lower evaluative mechanisms who were instructed to pull the lever were faster for posi- is that their ascending input may mildly predispose an indi- tive than for negative stimuli:

broadly. vidual’s thoughts, feelings, or preferences for a stimulus. For instance, my colleagues and I found that individuals Immediately and unintentionally, then, a perceived object or

publishers. event is classified as either good or as bad, and this results, in became more positive toward initially neutral and unfamil- a matter of milliseconds, in a behavioral predisposition to- iar Chinese ideographs if the individuals were first exposed allied ward that stimulus. When the conscious mind is elsewhere, disseminated its to the stimuli when their arms were in a state associated automatic evaluative processes prepare the individual to make be of with approach reactions (flexing the arm, as if pulling to the appropriate response. (Bargh & Chartrand, 1999, p. 475) one something toward them) than if they were first exposed to not or is the stimuli when their arms were in a state associated with In sum, neither is there a singular rational thought pro-

and avoidance reactions (extending the arm, as if pushing cess underlying all attitudes and behavior nor are all evalu- something away) even though participants were unaware of ative processes automatic. Instead, there are multiple neu- user

Association any link between their arm positions and motivational or robehavioral mechanisms across the neuraxis. Ceteris affective responses (Cacioppo, Priester, & Berntson, 1993). paribus, rostral relative to caudal mechanisms are (a) slower, more serial like; (b) subject to greater contextual

individual The presence of prior knowledge or feelings about the control; (c) characterized by greater response ﬂexibility;

the stimuli should diminish these subtle ascending inﬂuences, a Psychological of prediction supported by Priester, Cacioppo, and Petty and (d) capable of multiple modes of appetitive and aver-

use (1996): The effects of arm ﬂexion and extension on subse- sive activation (e.g., ambivalence; Berntson et al., in press; quent preferences for stimuli were evident for neutral, pro- Cacioppo, Larsen, Smith, & Berntson, in press). American nounceable, and novel nonwords (e.g., balet) but not for personal the Conclusion neutral, familiar words (e.g., table). the by Implicit social prejudices (e.g., racism) represent an

for As neuroscientiﬁc approaches are applied to more complex evaluative response predisposition that is not apparent in questions, what were thought to be basic principles are be-

solely self-reports (Greenwald, McGhee, & Schwartz, 1998). Im- ing revisited. This is the case for principles in the neuro- copyrighted aging studies have suggested that the strength of implicit sciences as well as in the social sciences. Social neuro- is racial prejudices covaries with the activation of the amyg- science is premised on the notion that biological, cognitive, intended

is dala in response to photographs of unfamiliar African and social levels of analysis, as well as a dialogue and in-

document Americans (Phelps et al., 2000), and social psychological tegrative collaborations among scientists working at these

article studies have suggested that implicit racial prejudices may levels of analyses, will contribute to more comprehensive This have subtle but broad discriminatory effects (Ashburn- explanations of the human mind and behavior. This Nardo, Voils, & Monteith, 2001) while also being difficult It seems obvious that understanding the pieces fosters to modify by an act of will (Greenwald et al., 1998). Pre- understanding the whole and that comprehension of the liminary work from our lab indicates that implicit social whole fosters an understanding of the pieces. The social prejudices may be modifiable by the silent ascending influ- and psychological sciences have long been viewed as a ences of somatic expressions. weak sister to the physical and biological sciences (Wilson, Rapid stimulus processing by lower evaluative mecha- 1998), however, and the lure of popular approbation of a nisms may also predispose an individual’s behavior toward retreat to solely biological levels of analysis can be strong. appetitive stimuli and away from aversive stimuli prior to It seems fair to say that the Decade of Behavior has not more detailed processing of the stimuli. A test of this hy- received the same scientific or public acclaim, or the con- pothesis was performed by Chen and Bargh (1999), who gressional support, as the Human Genome Project or the instructed some participants to push a lever away from Decade of the Brain even though more than a half-dozen

November 2002 ● American Psychologist 825 reports have been issued recently by the National Research Anisman, H., Zaharia, M. D., Meaney, M. J., & Merali, Z. Council calling for more integrative research between the (1998). Do early-life events permanently alter behavioral social and biological sciences (Berkman, 2002). In a recent and hormonal responses to stressors? International Journal issue of the popular science magazine Scientific American, of Developmental Neuroscience, 16, 149–164. the editors observed that “whenever we run articles on social topics, some readers protest that we should stick to Ashburn-Nardo, L., Voils, C. I., & Monteith, M. J. (2001). ‘real’ science” (“The Peculiar Institution,” 2002, p. 8). The Implicit associations as the seeds of intergroup bias: How editors went on to say: easily do they take root? Journal of Personality and Social Ironically, we seldom hear these complaints from working Psychology, 81, 789–799. physical or biological scientists. They are the first to point out that the natural universe, for all its complexity, is easier to Bargh, J. A., & Chartrand, T. L. (1999). The unbearable understand than the human being. If social science seems automaticity of being. American Psychologist, 54, mushy, it is largely because the subject matter is so difficult, 462–479. not because humans are somehow unworthy of scientific in- quiry. (“The Peculiar Institution,” 2002, p. 8) Baumeister, R. F., & Leary, M. R. (1995). The need to

broadly. Technical and methodological developments now enable belong: Desire for interpersonal attachment as a biological measures of ongoing human behavior, including fundamental human motivation. Psychological Bulletin, publishers. electrophysiological recording, functional brain imaging, 117, 497–529. allied and neurochemical techniques. Conversely, social methods disseminated its for studying behavior and ambulatory recordings of biolog-

be Berkman, L. F. (Ed.). (2002). Through the kaleidoscope: of

to ical function can now be applied to animals and humans Viewing the contributions of the behavioral and social one

not living in complex environments, providing a more fruitful

or sciences to health—The Barbara and Jerome Grossman is model for the dynamic interaction between biological Symposium. Washington, DC: National Academy Press. and mechanisms and social context. Changes in medical sci-

user ence, worldwide health problems (e.g., AIDS, chronic dis- Bernard, C. (1974). Lectures on the phenomena of life Association ease), and U.S. demographics have further fueled basic common to animals and plants (H. E. Hoff, R. Guillemin, social and biological research on societal problems. With & L. Guillemin, Trans.). Springﬁeld, IL: Thomas. (Original individual both means and motive now available, there is growing work published 1878)

the evidence that a more comprehensive understanding of the Psychological of mind and behavior will be fostered by integrative, theoreti- Berntson, G. G., Boysen, S. T., & Cacioppo, J. T. (1993). use cal analyses that span the biological and social levels of Neurobehavioral organization and the cardinal principle of organization. American evaluative bivalence. Annals of the New York Academy of personal the Sciences, 702, 75–102. the by Author’s Note

for I wish to thank my students and colleagues for their many Berntson, G. G., & Cacioppo, J. T. (2000). Psychobiology contributions to this work and for comments on an earlier and social psychology: Past, present, and future. solely draft of this address. Special thanks are due to Gary copyrighted Personality and Social Psychology Review, 4, 3–15.

is Berntson and Richard Petty. Preparation of this address

intended was supported by National Institute of Aging Grant PO1 Berntson, G. G., Cacioppo, J. T., & Sarter, M. (in press). is AG18911, National Science Foundation Grant Bottom-up: Implications for neurobehavioral models of document BCS-0086314, and National Institute of Mental Health article Grant P50MH52384-01A1. anxiety and autonomic regulation. In R. J. Davidson, K. R. This Scherer, & H. H. Goldsmith (Eds.), Handbook of affective

This Correspondence concerning this address should be sent to John T. Cacioppo, Department of Psychology, Univer- sciences. New York: Oxford University Press. sity of Chicago, 5848 South University Avenue, Chicago, IL 60637. E-mail: [email protected] Berntson, G. G., Sarter, M., & Cacioppo, J. T. (1998). Anxiety and cardiovascular reactivity: The basal forebrain References cholinergic link. Behavioural Brain Research, 94, 225–248.

Adolphs, R. (1999). Social cognition and the human brain. Boysen, S. T., Berntson, G. G., Hannan, M. B., & Trends in Cognitive Sciences, 3, 469–479. Cacioppo, J. T. (1996). Quantity-based choices: Interference and symbolic representations in chimpanzees Allport, G. W. (1947). Scientiﬁc models and human (Pan troglodytes). Journal of Experimental Psychology: morals. Psychological Review, 54, 182–192. Animal Behavior Processes, 22, 76–86.

826 November 2002 ● American Psychologist Bronfenbrenner, U., & Ceci, S. J. (1994). Nature–nurture Cacioppo, J. T., & Gardner, W. L. (1999). Emotion. reconceptualized in developmental perspective: A Annual Review of Psychology, 50, 191–214. bioecological model. Psychological Review, 101, 568–586. Cacioppo, J. T., Gardner, W. L., & Berntson, G. G. (1999). Cacioppo, J. T. (1994). Social neuroscience: Autonomic, The affect system has parallel and integrative processing neuroendocrine, and immune responses to stress. components: Form follows function. Journal of Personality Psychophysiology, 31, 113–128. and Social Psychology, 76, 839–855.

Cacioppo, J. T., & Berntson, G. G. (1992). Social Cacioppo, J. T., Hawkley, L. C., Berntson, G. G., Ernst, psychological contributions to the Decade of the Brain: J. M., Gibbs, A. C., Stickgold, R., & Hobson, J. A. (2002). Doctrine of multilevel analysis. American Psychologist, 47, Lonely days invade the nights: Social modulation of sleep 1019–1028. efﬁciency. Psychological Science, 13, 385–388. Cacioppo, J. T., Hawkley, L. C., Crawford, L. E., Ernst, Cacioppo, J. T., & Berntson, G. G. (1994). Relationship J. M., Burleson, M. H., Kowalewski, R. B., et al. (2002). between attitudes and evaluative space: A critical review,

broadly. Loneliness and health: Potential mechanisms. with emphasis on the separability of positive and negative Psychosomatic Medicine, 64, 407–417. publishers. substrates. Psychological Bulletin, 115, 401–423. Cacioppo, J. T., Kiecolt-Glaser, J. K., Malarkey, W. B., allied disseminated its Cacioppo, J. T., & Berntson, G. G. (2001). The affect Laskowski, B. F., Rozlog, L. A., Poehlmann, K. M., et al. be of system and racial prejudice. In J. Bargh & D. K. Apsley (2002). Autonomic glucocorticoid associations with the to one (Eds.), Unraveling the complexities of social life: A steady state expression of latent Epstein-Barr virus. not or is Festschrift in honor of Robert B. Zajonc (pp. 95–110). Hormones and Behavior, 42, 32–41.

and Washington, DC: American Psychological Association. Cacioppo, J. T., Larsen, J. T., Smith, N. K., & Berntson, user

Association Cacioppo, J. T., Berntson, G. G., Adolphs, R., Carter, G. G. (in press). The affect system: What lurks below the C. S., Davidson, R. J., McClintock, M. K., et al. (2002). surface of feelings? In A. S. R. Manstead, N. H. Frijda, &

individual Foundations in social neuroscience. Cambridge, MA: MIT A. H. Fischer (Eds.), Feelings and emotions: The

the Press. Amsterdam Conference. New York: Cambridge University Psychological of Press.

use Cacioppo, J. T., Berntson, G. G., Sheridan, J. F., & McClintock, M. K. (2000). Multilevel integrative analyses Cacioppo, J. T., Priester, J. R., & Berntson, G. G. (1993). American Rudimentary determinants of attitudes: II. Arm ﬂexion and personal of human behavior: Social neuroscience and the the extension have differential effects on attitudes. Journal of the by complementing nature of social and biological approaches. Personality and Social Psychology, 65, 5–17. for Psychological Bulletin, 126, 829–843.

solely Cacioppo, J. T., & Sandman, C. A. (1981). copyrighted Cacioppo, J. T., Crites, S. L., Jr., Berntson, G. G., & Psychophysiological functioning, cognitive responding, and is Coles, M. G. H. (1993). If attitudes affect how stimuli are attitudes. In R. E. Petty, T. M. Ostrom, & T. C. Brock intended processed, should they not affect the event-related brain

is (Eds.), Cognitive responses in persuasion (pp. 81–104). potential? Psychological Science, 4, 108–112.

document Hillsdale, NJ: Erlbaum. article This Cacioppo, J. T., Crites, S. L., Jr., & Gardner, W. L. (1996). Cacioppo, J. T., & Tassinary, L. G. (1990). Inferring This Attitudes to the right: Evaluative processing is associated psychological signiﬁcance from physiological signals. with lateralized late positive event-related brain potentials. American Psychologist, 45, 16–28. Personality and Social Psychology Bulletin, 22, 1205–1219. Chen, M., & Bargh, J. A. (1999). Nonconscious approach and avoidance behavioral consequences of the automatic Cacioppo, J. T., Crites, S. L., Jr., Gardner, W. L., & evaluation effect. Personality and Social Psychology Berntson, G. G. (1994). Bioelectrical echoes from Bulletin, 25, 215–224. evaluative categorizations: I. A late positive brain potential that varies as a function of trait negativity and extremity. Cohen, S. (1991). Social supports and physical health: Journal of Personality and Social Psychology, 67, Symptoms, health behaviors and infectious disease. In 115–125. A. L. Greene, E. M. Cummings, & K. H. Karraker (Eds.),

November 2002 ● American Psychologist 827 Life-span developmental psychology: Perspectives on stress Gardner, W. L., Gabriel, S., & Diekman, A. B. (2000). and coping (pp. 213–234). Hillsdale, NJ: Erlbaum. Interpersonal processes. In J. T. Cacioppo, L. G. Tassinary, & G. G. Berntson (Eds.), Handbook of psychophysiology Cohen, S. (1996). Psychological stress, immunity, and (2nd ed., pp. 643–664). New York: Cambridge University upper respiratory infections. Current Directions in Press. Psychological Science, 5, 86–90. Gauthier, I., Skudlarski, P., Gore, J. C., & Anderson, Committee on Future Directions for Behavioral and Social A. W. (2000). Expertise for cars and birds recruits brain Sciences Research at the National Institutes of Health. areas involved in face recognition. Nature Neuroscience, 3, (2001). New horizons in health: An integrative approach. 191–197. Washington, DC: National Academy Press. George, N., Dolan, R. J., Fink, G. R., Baylis, G. C., Crabbe, J. C., Wahlsten, D., & Dudek, B. C. (1999, June Russell, C., & Driver, J. (1999). Contrast polarity and face 4). Genetics of mouse behavior: Interactions with recognition in the human fusiform gyrus. Nature laboratory environment. Science, 284, 1670–1672. Neuroscience, 2, 574–580. broadly. Crick, F. (1970, August 8). Central dogma of molecular Gerlai, R. (1996). Gene-targeting studies of mammalian publishers. biology. Nature, 227, 561–563. behavior: Is it the mutation or the background genotype? Trends in Neurosciences, 19, 177–181. allied disseminated its Crites, S. L., Jr., & Cacioppo, J. T. (1996). Electrocortical be of differentiation of evaluative and nonevaluative Gilbert, D. T., Fiske, S. T., & Lindzey, G. (1998). The to one categorizations. Psychological Science, 7, 318–321. handbook of social psychology (4th ed.) Boston, MA: not or is McGraw-Hill.

and Crites, S. L., Jr., Cacioppo, J. T., Gardner, W. L., & Berntson, G. G. (1995). Bioelectrical echoes from Glaser, R., & Kiecolt-Glaser, J. K. (1994). Handbook of user

Association evaluative categorization: II. A late positive brain potential human stress and immunity. San Diego, CA: Academic that varies as a function of attitude registration rather than Press.

individual attitude report. Journal of Personality and Social

the Psychology, 68, 997–1013. Golby, A. J., Gabrieli, J. D. E., Chiao, J. Y., & Eberhardt, Psychological of J. L. (2001). Differential responses in the fusiform region

use Damasio, A. R. (1994). Descartes’ error: Emotion, reason, to same-race and other-race faces. Nature Neuroscience, 4, and the human brain. New York: Grosset/Putnam. 845–850. American personal the Dawkins, R. (1990). The selﬁsh gene (2nd ed.). New York: Gottlieb, G. (1998). Normally occurring environmental and the by Oxford University Press. behavioral inﬂuences on gene activity: From central dogma for to probabilistic epigenesis. Psychological Review, 105,

solely de Waal, F. (1996). Good natured: The origins of right 792–802. copyrighted and wrong in humans and other animals. Cambridge, MA: is Harvard University Press. Gould, S. J. (1980). Ever since Darwin: Reﬂections in intended

is natural history. Harmondsworth, Middlesex, England:

document Dolan, R. J. (1999). On the neurology of morals. Nature Penguin.

article Neuroscience, 2, 927–929. This Greene, J. D., Sommerville, R. B., Nystrom, L. E., Darley, This Farah, M. J., Wilson, K. D., Drain, M., & Tanaka, J. N. J. M., & Cohen, J. D. (2001, September 14). An fMRI (1998). What is “special” about face perception? investigation of emotional engagement in moral judgment. Psychological Review, 105, 482–498. Science, 293, 2105–2108.

Felthous, A. R. (1997). Does “isolation” cause jail Greenwald, A. G., McGhee, D., & Schwartz, J. (1998). suicides? Journal of the American Academy of Psychiatry Measuring individual differences in implicit cognition: The and the Law, 25, 285–294. Implicit Association Test. Journal of Personality and Social Psychology, 74, 1464–1480. Frith, U., & Frith, C. (2001). The biological basis of social interaction. Current Directions in Psychological Science, Harris, J. C. (in press). Empathy, autism, and the 10, 151–155. integration of the triune brain. In R. Gardner, Jr., & G. A.

828 November 2002 ● American Psychologist Corey, Jr. (Eds.), The evolutionary neuroethology of Paul Kropotkin, P. I. (1989). Mutual aid: A factor of evolution. MacLean: Convergences and frontiers. Westport, CT: Montreal, Quebec, Canada: Black Rose. Greenwood-Praeger. Lederhendler, I. I., Herriges, K., & Tobach, E. (1977). House, J. S., Landis, K. R., & Umberson, D. (1988, July Taxis in Aplysia dactylomela (Rang, 1828) to water-borne 29). Social relationships and health. Science, 241, stimuli from environmental factors. Animal Learning and 540–545. Behavior, 5, 355–358.

Ito, T. A., & Cacioppo, J. T. (1999). Measuring racial LeDoux, J. E. (1995). Emotion: Clues from the brain. prejudice with event-related potentials. Psychophysiology, Annual Review of Psychology, 46, 209–235. 36, S62. Lewontin, R. (2000). The triple helix: Gene, organism, and Ito, T. A., & Cacioppo, J. T. (2000). Electrophysiological environment. Cambridge, MA: Harvard University Press. evidence of implicit and explicit categorization processes. Journal of Experimental Social Psychology, 36, 660–676. Lieberman, M. D., Ochsner, K. N., Gilbert, D. T., & broadly. Schacter, D. L. (2001). Attitude change in amnesia and under cognitive load. Psychological Science, 12, 135–140. publishers. Ito, T. A., Larsen, J. T., Smith, N. K., & Cacioppo, J. T. (1998). Negative information weighs more heavily on the allied Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., disseminated brain: The negativity bias in evaluative categorizations. its

be Freedman, A., et al. (1997, September 12). Maternal care, of Journal of Personality and Social Psychology, 75, to hippocampal glucocorticoid receptors, and hypothalamic–

one 887–900. not

or pituitary–adrenal responses to stress. Science, 277, is 1659–1662.

and Jackson, J. H. (1958). Evolution and dissolution of the nervous system (Croonian Lectures). In J. Taylor (Ed.), user Lorig, T. S. (2000, October) Spheres of inﬂuence: Association Selected writings of John Hughlings Jackson (pp. 154– 204). New York: Basic Books. (Original work published Psychophysiology’s place in a universe of neuroscience. 1884) Paper presented at the meeting of the Society for individual Psychophysiological Research, Denver, CO. the Psychological of Kandel, E. R. (1979). Behavioral biology of Aplysia: A MacLean, P. (1985). Brain evolution relating to family, use contribution to the comparative study of opisthobranch molluscs. San Francisco: Freeman. play, and the separation call. Archives of General

American Psychiatry, 42, 404–417. personal the the by Kandel, E. R. (2001, November 2). The molecular biology Macmillan, M. (2000). An odd kind of fame: Stories of

for of memory storage: A dialogue between genes and Phineas Gage. Cambridge, MA: MIT Press. synapses. Science, 294, 1030–1038. solely copyrighted Maestripieri, D. (2001). Biological bases of maternal is Kandel, E. R., & Squire, L. R. (2000, November 10). attachment. Current Directions in Psychological Science, intended Neuroscience: Breaking down scientiﬁc barriers to the 10, 79–83. is study of brain and mind. Science, 290, 1113–1120. document

article Malarkey, W. B., Wu, H., Cacioppo, J. T., Malarkey, This Kiecolt-Glaser, J. K., Glaser, R., Cacioppo, J. T., & K. L., Poehlmann, K. M., Glaser, R., & Kiecolt-Glaser, This Malarkey, W. B. (1998). Marital stress: Immunologic, J. K. (1996). Chronic stress down-regulates growth neuroendocrine, and autonomic correlates. Annals of the hormone gene expression in peripheral blood mononuclear New York Academy of Sciences, 840, 656–663. cells of older adults. Endocrine, 5, 33–39.

Klein, S. B., & Kihlstrom, J. F. (1998). On bridging the Meaney, M. J., Bhatnagar, S., Larocque, S., McCormick, gap between social-personality psychology and C. M., Shanks, N., Sharma, S., et al. (1996). Early neuropsychology. Personality and Social Psychology environment and the development of individual differences Review, 2, 228–242. in the hypothalamic–pituitary–adrenal stress response. In C. R. Pfeffer (Ed.), Severe stress and mental disturbance in Kosslyn, S. M., & Andersen, R. A. (1992). Frontiers in children (pp. 85–127). Washington, DC: American cognitive neuroscience. Cambridge, MA: MIT Press. Psychiatric Press.

November 2002 ● American Psychologist 829 Morris, J. S., O¨ hman, A., & Dolan, R. J. (1998, June 4). The public face of neuroscience. (2002). Nature Conscious and unconscious emotional learning in the Neuroscience, 5, 183. human amygdala. Nature, 393, 467–470. Sarter, M., Berntson, G. G., & Cacioppo, J. T. (1996). Nisbett, R. E., & Wilson, T. D. (1977). Telling more than Brain imaging and cognitive neuroscience: Toward strong we can know: Verbal reports on mental processes. inference in attributing function to structure. American Psychological Review, 84, 231–259. Psychologist, 51, 13–21.

Ochsner, K. N., & Lieberman, M. D. (2001). The Schwarz, M., Blumberg, S., & Susswein, A. J. (1998). emergence of social cognitive neuroscience. American Social isolation blocks the expression of memory after Psychologist, 56, 717–734. training that a food is inedible in Aplysia fasciata. Behavioral Neuroscience, 112, 942–951. O’Doherty, J., Kringelbach, M. L., Rolls, E. T., Hornak, J., Schwarz, M., & Susswein, A. J. (1992). Presence of & Andrews, C. (2001). Abstract reward and punishment conspeciﬁcs facilitates learning that food is inedible in representations in the human orbitofrontal cortex. Nature

broadly. Aplysia fasciata. Behavioral Neuroscience, 106, 250–261. Neuroscience, 4, 95–102. publishers. Scott, T. R. (1991). A personal view of the future of Osgood, C. E., Suci, G. J., & Tannenbaum, P. H. (1957). psychology departments. American Psychologist, 46, allied

disseminated The measurement of meaning. Urbana: University of its 975–976. be of Illinois Press. to one Seeman, T. E. (2000). Health promoting effects of friends not or is Pascalis, O., de Haan, M., & Nelson, C. A. (2002, May and family on health outcomes in older adults. American

and 17). Is face processing species-speciﬁc during the ﬁrst year Journal of Health Promotion, 14, 362–370. of life? Science, 296, 1321–1323. user

Association Seeman, T. E., Singer, B., Rowe, J. W., Horwitz, R., & The peculiar institution. (2002, April). Scientiﬁc American, McEwen, B. (1997). The price of adaptation: Allostatic

individual 286(4), 8. load and its health consequences. Archives of Internal

the Medicine, 157, 2259–2268. Psychological of Peeters, G., & Czapinski, J. (1990). Positive–negative use asymmetry in evaluations: The distinction between Siegal, M., & Varley, R. (2002). Neural systems involved affective and informational negativity effects. In W. in “theory of mind.” Nature Reviews: Neuroscience, 3, American 463–471. personal Stroebe & M. Hewstone (Eds.), European review of the the by social psychology (Vol. 1, pp. 33– 60). New York: Smith, N. K., Cacioppo, J. T., Larsen, J. T., & Chartrand, for Wiley. T. L. (in press). May I have your attention please:

solely Electrocortical responses to positive and negative stimuli. Petty, R. E., & Cacioppo, J. T. (1981). Attitudes and copyrighted Neuropsychologia. is persuasion: Classic and contemporary approaches.

intended Dubuque, IA: Brown.

is Sternberg, E. (2000). The balance within: The science

document connecting health and emotions. New York: Freeman. Phelps, E. A., O’Connor, K. J., Cunningham, W. A., article This Funayama, E. S., Gatenby, J. C., Gore, J. C., & Banaji, Susswein, A. J., Schwarz, M., & Feldman, E. (1986). This M. R. (2000). Performance on indirect measures of race Learned changes of feeding behavior in Aplysia in response evaluation predicts amygdala activation. Journal of to edible and inedible foods. Journal of Neuroscience, 6, Cognitive Neuroscience, 12, 729–738. 1513–1527.

Posner, M. I., & Raichle, M. E. (1997). Images of mind. Taylor, S. E. (1991). Asymmetrical effects of positive and New York: Scientiﬁc American Library. negative events: The mobilization-minimization hypothesis. Psychological Bulletin, 110, 67–85. Priester, J. R., Cacioppo, J. T., & Petty, R. E. (1996). The inﬂuence of motor processes on attitudes toward novel Taylor, S. E., & Brown, J. D. (1988). Illusion and well- versus familiar semantic stimuli. Personality and Social being: A social psychological perspective on mental health. Psychology Bulletin, 22, 442–447. Psychological Bulletin, 103, 193–210.

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