Fisher.1998.Emotions

Fisher.1998.Emotions - LUST, ATTRACTION, AND ATTACHMENT IN...

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Unformatted text preview: LUST, ATTRACTION, AND ATTACHMENT IN MAMMALIAN REPRODUCTION Helen E. Fisher Rutgers University This paper proposes that mammals exhibit three primary emotion catego- ries for mating and reproduction: (1) the sex drive, or lust, characterized by the craving for sexual gratification; (2) attraction, characterized by in- creased energy and focused attention on one or more potential mates, accompanied in humans by feelings of exhilaration, "intrusive thinking" about a mate, and the craving for emotional union with this mate or potential mate; and (3) attachment, characterized by the maintenance of close social contact in mammals, accompanied in humans by feelings of calm, comfort, and emotional union with a mate. Each emotion category is associated with a discrete constellation of neural correlates, and each evolved to direct a specific aspect of reproduction. The sex drive is associ- ated primarily with the estrogens and androgens; it evolved to motivate individuals to seek sexual union. The attraction system is associated pri- marily with the catecholamines; it evolved to facilitate mate choice, en- abling individuals to focus their mating effort on preferred partners. The attachment system is associated primarily with the peptides, vasopressin, and oxytocin; it evolved to motivate individuals to engage in positive social behaviors and assume species-specific parental duties. During the evolution of the genus Homo, these emotion systems be- came increasingly independent of one another, a phenomenon that con- tributes to human mating flexibility and the wide range of contemporary human mating and reproductive strategies. Received: July 29, 1996; revised May 12, 1997; accepted September 18, 1997. Address all correspondence to Dr. Helen E. Fisher, 4 East 70th Street, New York City, NY 10021. E-mail: hefisher@worldnet.att.nel Copyright © 1998 by Walter de Gruyter, Inc., New York Human Nature, Vol. 9, No. 1, pp. 23—52. 1045-6767/98/51.00+.10 23 34 Human Nature, Vol. 9, N0. 1, 1998 KEY worms: Catecholamines; Emotions; Evolution; Human reproductive strategies; Mate choice; Romantic love. William James implied that emotions are discrete phenomena—that each is associated with a unique pattern of peripheral physiological events. Schachter and Singer (1962) replaced this model with their two—factor emotion theory, the concept that different emotions are the result of the same basic undifferentiated arousal plus specific cognitions. William Iames’s model for the unique psychophysiology of specific emotions has recently come back into favor, however. As psychologist Richard David- son reports, “The notion that different emotional states are associated with unique patterns of central nervous system activity must, in a trivial sense, be true if we subscribe to the belief that no mental modification occurs without a corresponding change in brain activity. . . . The chal- lenge for us is to specify what the natural categories [of emotion] are” (1994240). In 1872, Darwin discussed several natural categories of emotion in The Expression of the Emotions in Man and Animals. Since then many scientists, including Watson (1930), Izard (1977), Plutchik (1980), Panksepp (1986), MacLean (1990), and Ekman (1992), have defined specific categories of emotions (see Ekman and Davidson 1994; Lazarus 1991). This paper reas- sembles current data with the purpose of defining the primary categories of emotion associated specifically with mammalian reproduction.l It places particular emphasis on attraction, the least well-known of these emotion systems. In this paper, it is hypothesized that mammals have evolved three primary, discrete, interrelated emotion systems for mating and reproduc- tion; each is associated with a specific constellation of neural correlates, and each evolved to direct a specific aspect of mammalian reproduction. The sex drive (the libido, or lust) is characterized by the craving for sexual gratification,- it is associated primarily with the estrogens and androgens; and it evolved primarily to motivate individuals to seek sexual union with any conspecific. The attraction system is characterized by increased energy and focused attention in mammals, as well as by exhilaration, ’intrusive thinking,” and the craving for emotional union in humans. l\ttraction is associated primarily with the catecholamines; and it evolved to facilitate mate choice, enabling individuals to focus their mating effort on preferred conspecifics. The attachment system is characterized by terri- Iory defense and/ or nest building, mutual feeding, grooming, mainte- nance of close proximity, separation anxiety, shared parental chores, and other affiliative behaviors in mammals, and with feelings of calm, securi- l y, social comfort, and emotional union in humans. Attachment is associ- Lust, Attraction, and Attachment in Mammalian Reproduction 25 ated primarily with the neuropeptides vasopressin and oxytocin; this emotion system evolved to enable individuals to engage in positive social behaviors and / or sustain affiliative connections long enough to complete species-specific parental duties. As reproductive strategies vary according to the degree of mating effort and parental investment required of each species and each individual (Lancaster and Kaplan 1994; Trivers 1972), the distribution of brain sites for hormone and neurotransmitter receptors associated with each of these emotion categories, as well as the duration, intensity, and types of activ- ities at these neural sites, are expected to vary from one species to the next. Evidence of this variation is discernible among different species of voles; for example, in monogamous prairie voles (Microtus ochrogaster) the distribution of limbic system receptor sites for oxytocin, one of the pep— tides associated with attachment, varies from that of montane voles (Mi- crotus montanus), an asocial relative (lnsel et al. 1993). Moreover, data on binding activities at oxytocin receptor terminals in limbic brain areas of the monogamous prairie vole versus similar data on the asocial montane vole suggest that it is not variations in gene structure but a phylogenetic shift in regulatory sequences that directs varied mammalian parenting strategies. "In other words, the evolution of monogamy might result from relatively minor changes in promoter sequences, directing the expression of the same receptor protein [oxytocin] to very different neural circuits” (Leckman et al. n.d.:26). Further investigation should establish many species-specific variations in the expression and neurophysiology of the sex drive, attraction, and attachment. The neural mechanisms governing these emotion systems also can be expected to vary between individuals within a species. Individual varia- tions in the sex drive are commonly reported among humans and among individuals of other primate species. Tennov (1979) reports individual variations in the frequency and duration of human attraction. Behavioral variations in the expression of attachment are documented among mo- nogamous prairie voles. After initial copulation, almost 90% of males remain with a mate to rear offspring as a team; however, the remaining 10.9% abandon the reproductive unit (Carter et al. 1995; Insel and Carter 1995). Cross—cultural and within-culture divorce rates illustrate individual variations in human attachment behaviors as well (Fisher 1989, 1992, 1994, 1995). Although cultural and ecological forces clearly contribute to these individual human variations in the sex drive, attraction, and attach- ment, these individual variations most likely have neural correlates. The neural mechanisms mediating the sex drive, attraction, and attach- ment also can be expected to vary across the life course. Data on voles confirm it. lnsel reports that at parturition, when the female montane vole 36 Human Nature, Vol. 9, No. 1, 1998 lirst affiliates with her infants, “the expression of OT (oxytocin) receptors :hanges in the direction of the pattern observed in the highly parental prairie vole” (Insel 199224). The neural mechanisms associated with these .-motion systems for mating can be expected to vary according to sex/ gender and in response to environmental opportunities and exigen- sites as well; however, discussion of these variations is beyond the scope of this paper. Extensive data indicate that the hormonal and neurotransmitter sys- tems underlying these three emotion categories interact with one another md with other bodily systems. Recent data on male prairie voles, for Axample, indicate that testosterone, which promotes mounting and intro- mission, can facilitate the production of vasopressin and thus, indirectly, the regulation of male parental care (De Vries 1990; De Vries, Wang et al. 1994; Wang et al. 1994). Several studies report that oxytocin administered ‘entrally to virgin female rats induces maternal behaviors within minutes (Fahrbach et al. 1984a, 1984b, 1985; Pedersen and Prange 1979; Pedersen it al. 1982; Wamboldt and Insel 1987), but the response is dependent on priming with gonadal steroids (Leckman and Mayes, in press). For more _,~xamples, oxytocin affects dopaminergic activity (Samyai and Kovacs I994), and serotonin can alter the synthesis, release, or function of several neuropeptides (Fuller 1996). A host of data also indicate that these three emotion systems not only Inhibit and / or enhance one another, they can inhibit or enhance conjoin- ing systems and independent neurohormonal systems (Crawley and \Ichean 1996; Herbert 1996; Nyborg 1994; Sitsen 1988; see Ziegler and Lake 1984). These interactions are expected. As psychologist Iaak l’anksepp writes, "one of the persistent problems is that there is consider- ,ible overlap in the autonomic and endocrine outputs of the various basic -moti0nal systems, which is to be expected. The main function of the auto- nomic and endocrine changes is to bring various bodily reactions in line with behavioral/psychological demands of each emotional system” (Panksepp 1994:258, emphasis added). Nevertheless, under some circumstances these three emotion systems can act independently. Male gibbons (Hylobates lar) have been docu- mented to express attachment toward a mate by dueting, grooming, and displaying coordinated territorial defense within the same time frame that they express attraction toward a female in a neighboring territory (Palombit 1994). The independence of these emotion systems, however, is most clear in humans. Men and women can express attachment for a spouse or long-term mate, attraction toward a different conspecific, and the sex drive in response to visual, verbal, or mental stimuli that are unrelated to either the spouse or the individual to whom they are roman- tically attracted. Further examination of data on specific species is neces- Lust, Attraction, and Attachment in Mammalian Reproduction 27 sary to illustrate how each emotion system is differentially expressed and how it interacts with the others and with other bodily systems. Psychologists distinguish between the sex drive, attraction (standardly termed "passionate love" or "obsessive love"), and attachment (stan— dardly termed "companionate love”; see Hatfield and Rapson 1996; Hat- field and Sprecher 1986; Hatfield 1988; Shaver et al. 1988). But they have not discussed the neural correlates of these emotion systems, the specific role of attraction in mammalian reproduction, the evolution of these emo- tion systems in Homo sapiens, or the impact of these three distinct emotion systems on contemporary human patterns of mating and reproduction. So the present paper defines and distinguishes these three emotion sys- tems for mating, reports on data suggesting the primary hormones and / or neurotransmitters associated with each emotion system, proposes that the attraction system evolved to facilitate mate choice in mammals, and concludes that during the course of hominid evolution these three emotion systems became increasingly independent from one another, a neurophysiological artifact that contributes to current patterns of human mating flexibility and the wide range of contemporary human reproduc- tive strategies. LUST The sex drive, otherwise known as lust, the libido, or the urge for sexual consummation, is a multidimensional phenomenon; many parts of mam— malian anatomy and physiology are involved. Myriad ecological stimuli including seasonal light, temperature, and olfactory cues influence this emotion system as well. In primates, learning also plays an important role in triggering the sex drive. The present paper does not review the ecologi- cal or social cues that influence the sex drive; instead it examines the primary neural correlates associated with this emotion category in order to establish the sex drive as an emotion system distinct from that of attraction or attachment. For several decades, the sex drive has been regarded as a distinct emoc tion system associated with specific hormones and primary neural struc-A tures (Beach 1948, 1976; see Komisaruk et al. 1986). This neural circuitry varies between species, but it is known to be innate, and common aspects of this neural circuitry are known to be present in all mammals. The sex drive is regulated, in large part, by the preoptic area of the anterior hypothalamus, which is one source of gonadotropin—releasing hormone (GnRH), also known as luteinizing hormone—releasing hormone. GnRH traverses a portal vascular system to the anterior pituitary to stimulate Human Nature, Vol. 9, No. l, 1998 oduction of follicle-stimulating hormone (FSH) and luteinizing hor- one (LH). FSH and LH stimulate the gonads to produce the sex steroids, cluding testosterone, and testosterone can be metabolized to dihy- otestosterone, estradiol, and other estrogens. Other areas of the brain c associated with the sex drive in specific mammalian species, but these gions and the sex steroids are associated with sexual arousal in all .immals (see Komisaruk et al. 1986). When testosterone is administered to castrated male rats, mice, or pigs, cir sex drive returns (see Beach 1948; 1976; Nyborg 1994). In humans, udrogens are associated with increased libido in both sexes (Sherwin '94). Women with higher levels of circulating testosterone have more xual thoughts, greater desire for sex, and higher mean levels of sexual tivity (Morris et al. 1987; Persky et al. 1978). Older men and women ho receive injections of testosterone report that sexual thoughts and xual motivation increase (Sherwin and Gelfand 1987; Sherwin et al. '85). The androgens have long been associated with the male sex drive each 1948). Now there is also "compelling evidence that libido, or sexu- motivation, in women is dependent on androgens” (Sherwin 1994:428). Estrogen also plays a role in the sex drive. Rising levels of estradiol trimarily) triggers estrus and sexual behavior in female mammals; rhe- xs monkeys are an example (Wallen and Tannenbaum 1997). The link tween increasing levels of estradiol and increasing sexual motivation id behavior is significantly reduced in humans; nevertheless, some omen report that they have more sexual desire just before they ovulate, hen ovarian estrogen levels peak (Judd and Yen 1973). Small amounts adrenal androgens convert to estrogen in aging men, contributing to cir sex drive too. in fact, injections of testosterone and other androgens ay initiate sexual behavior in castrated female mammals and injections estrogens may trigger sexual behavior in castrated male mammals. The testosterone / estrogen relationship and its function in relation to her bodily systems is a complex phenomenon (see Nyborg 1994). Nev- 'theless, the brain circuitry for the sex drive is clearly independent of the -ural correlates for attachment in mammals; all mammals engage in 'xual activity, yet individuals in only 3% of mammalian species form a vng-term attachment to a mating partner (Kleiman 1977). The relation- iip between the sex drive and attraction is more problematic. Mammals vgularly express the drive for sexual consummation, yet most prefer rme partners over others—an indication that the sex drive and attraction 'e somewhat distinct phenomena. Evidence that these three emotion stems are distinct is clearest in Homo sapiens. Humans can feel and \press sexual desire toward individuals for whom they feel no romantic traction, as well as for conspecifics to whom they are not emotionally tached. Lust, Attraction, and Attachment in Manmmlian Reproduction 29 The sex drive and attraction are regularly lumped together in ethologi- cal discussions of mammalian mating behavior, a custom that stems from the work of Frank Beach. Beach (1976) defined three distinct stages of sexual behavior in female mammals: attractivity, proceptivity, and recep- tivity. Attractivity refers to masculine appetitive (approach) reactions to females as attractive sexual stimuli, expressed most frequently when a female is secreting maximum levels of estrogens. Proceptivity refers to feminine appetitive sexual reactions toward males, also associated with maximum levels of estrogen (although Beach also implicates the an- drogens in the sex drive of both male and female mammals). Rcceptivity refers to consummatory acts of mating in both sexes. Beach does not distinguish between the neural correlates associated with the sex drive and those associated with attraction. He does acknowledge attraction in mammalian species, referring to it as “favoritism,” "selective proceptivity,” "individual preference,” "distinct preferences for some part- ners and strong aversion to others,” and "sexual choice” (Beach 1976:124). He notes that “the occurrence or nonoccurrence of copulation depends as much upon individual affinities and aversions as upon the presence or absence of sex hormones in the female” (Beach 19762130; see Phoenix 1973). He states that "proceptive and receptive behavior may depend upon different anatomical and neurochemical systems in the brain” (Beach 1976:131; emphasis added). And he reports data that confirm this distinc- tion between the sex drive and attraction: "The mating behavior of female rats treated with monoamine receptor blocking agents indicates that ’lord- otic behavior and soliciting behavior may be mediated by anatomically and possibly neurochemically separate systems’ " (Beach 1976:131; see Ward et al. 1975). But Beach (1976) concludes that mammalian attractivity and receptivity are controlled primarily by estrogen, whereas proceptive be- havior may be stimulated when androgens are added. Beach's conclusion that the androgens and estrogens both play a prima- ry role in the sex drive has been supported. But there is no evidence that the androgens (or estrogens) play a primary role in attraction—the emo- tion system that enables individuals to focus their mating effort on spe- cific preferred sex partners. When menopausal women are injected with androgens, for example, their sex drive is enhanced, but there is no evi- dence that injections of androgens evoke feelings of romantic attraction or attachment to specific individuals. When rats, monkeys, and other mam- mals are injected with estrogens and /or androgens, they exhibit in- creased appetitive sexual behaviors but they do not display increased favoritism, increased partner preference, or increased focused attention on preferred conspecifics. Beach’s (1976) model of attractivity, proceptivity, and receptivity is use- ful for distinguishing between stages of the sex drive. But this model does 0 Human Nature, Vol. 9, No. 1, 1998 .ot adequately distinguish a second emotion system for mating that may .perate in tandem with the sex drive in most mammalian species, ttraction. \TTRACTION 'he close physiological and behavioral association between the sex drive .nd attraction in mammals may account for the scarcity of investigation nto the brain correlates of attraction. Nevertheless, naturalists and scien- rsts have acknowledged attraction as a discrete emotion system for over a entury. When Darwin (1859, 1871) proposed the concept of sexual selec- ron to explain patterns of sexual dimorphism in secondary sexual charac- uristics and mating behaviors in birds and mammals, he proposed two elective agents: competition between individuals of one sex and prefer- uce for certain traits exhibited by the opposite sex. Central to Darwin’s nodel was "female choice,” also known as mate choice or mate prefer- -nce. Since then, many articles have discussed aspects of mate preference attraction) in birds and mammals (see Andersson 1994; Campbell 1972). Implicit in Darwin’s model of sexual selection and subsequent discus— ions of mate choice is the understanding that some type of emotion ystem is activated when individual mammals focus their energy and nating effort on preferred mating partners. So it is proposed in this paper hat mate preference has two fundamental aspects: First, factors that trig- rr mate preference, such as symmetry, the display of resources, the dis- rlay of fertility, and/or other biological and behavioral factors that timulate to whom one becomes attracted; second, the emotion system that rcilitates this mate preference, including increased energy and intent fo- us on this conspecific. In humans, for example, timing, state of health, .ccess to resources, childhood experiences, and myriad other cultural and riological forces play crucial roles in triggering to whom one becomes .ttracted. But as this choice emerges, a specific emotion system is activated, nabling the individual to focus his / her mating effort on this preferred ndividual. Since myriad species-specific anatomical, chemical, and behavioral shenomena have evolved in mammalian species expressly to stimulate .ttraction from conspecifics, it is parsimonious to suggest that these sexu- rlly selected stimuli activate a specific emotion system in all mammals. So I is hypothesized that attraction constitutes a discrete emotion system; hat this emotion system is associated with a specific constellation of reural correlates; that the neural circuitry for attraction is interrelated vith the neural circuitry for the sex drive (and most likely with the Last, Attraction, and Attachment in Mammalian Reproduction 31 attachment system); and that the mammalian attraction system evolved to enable individuals to focus their mating effort on preferred conspecifics, generally those displaying genetically superior traits. This excitatory emotion system is hereby labeled attraction; in humans, intense attraction is hereby labeled infatuation, romantic love, "being in love,” passionate love, and / or obsessive love. Descriptions of mammalian mating interactions characteristically in- clude reports of increased energy and focused attention directed toward preferred conspecifics. Yet the behavioral components of the attraction system in nonhuman mammals are undefined, and cross-species compar- ative descriptions of the attraction system have not been compiled. In rats and other mammals, however it is likely that attraction-associated behav- iors are short—lived, whereas in humans these behaviors are longer-term and intensely expressed (Fisher 1992; Jankowiak and Fisher 1992). So the attraction system is best examined in humans. Intense attraction, commonly known as romantic love, is recorded in all human cultures for which data are available. lankowiak and Fischer (1992) surveyed 166 contemporary societies and found evidence of ro- mantic love in 147 of them; they note that the 19 negative cases are due to ethnographic oversight. Historical and literary sources indicate that at- traction was also evident in ancient Sumeria and Egypt, classical Greece and Rome, and in the preindustrial civilizations of India, China, Japan, Europe, Africa, and the Americas (Alarcon 1992; Bullfinch 1993; Cole 1963; Fowler 1994; Hamill 1996; Hurford 1995; Melville 1990; Moore and Beier 1984; Wolkstein 1991). So Iankowiak and Fischer (1992:154) con- clude that attraction constitutes a "human universal" or “near universal." Some psychologists see the development of human passionate love as rooted in childhood experiences. They focus their investigations on the effects of mother-infant bonding in order to explain variations in the form, duration, and/ or frequency of adult passionate relationships (see Hatfield and Rapson 1996; Shaver et al. 1988; Sternberg and Barnes 1988). These data on the development of passionate love from childhood experi- ences are not the focus of this paper: The present paper does not discuss the context in which romantic attraction develops across the human life course, when it develops, toward whom it is directed, why it is directed toward specific individuals rather than others, how often one experiences attraction, or how long an individual maintains attraction for a partner or a spouse. Instead, the present paper is a preliminary investigation of the specific constellation of neural correlates associated with this primary emotion category. First it is necessary to discuss the psychophysiological properties of human attraction, since this suite of traits gives some indication of the 32 Human Nature, Vol. 9, No. 1, 1998 neural substrate involved in this emotion system. Several psychologists have investigated the properties of attraction. Using a series of question- naires and in-depth interviews of approximately 2,000 individuals, Ten- nov (1979, personal communication 1997) isolated a suite of psychological traits associated with "being in love,” a state she calls limerence. Hatfield and Sprecher (1986) have also isolated a suite of traits commonly associ- ated with attraction, a state they call "passionate love.” Reviewing these data, as well as the past 25 years of psychological literature on attraction, Harris (1995) compiled a list of characteristics associated with romantic attraction that has been frequently cited and is well supported. I In a current synthesis of these data, the author and colleagues (Fisher et a]. n.d.a) have compiled a more extensive list of psychophysical proper- ties associated with attraction: 1. the loved person takes on "special meaning.” As one of Tennov's informants phrased it, "My whole world had been transformed. It had a new center, and that center was Marilyn” (Tennov 1979:18). This phenomenon is coupled with the inability to feel romantic passion for more than one person at a time; intrusive thinking about the loved person; 3. crystallization, or the tendency to focus on the loved person’s positive qualities and overlook or falsely appraise his/ her nega- tive traits; 4. labile psychophysiological responses to the loved person, including exhilaration, euphoria, buoyance, spiritual feelings, feel- ings of fusion with the loved person, increased energy, sleepless- ness, loss of appetite, shyness, awkwardness, trembling, pallor, flushing, stammering, aching of the “heart,” inappropriate laugh- ing, gazing, prolonged eye contact, butterflies in the stomach, sweaty palms, weak knees, dilated pupils, dizziness, a pounding heart, accelerated breathing, uncertainty, anxiety, panic, and / or fear in the presence of the loved person; 5. a longing for emotional reciprocity coupled with the desire to achieve emotional union with the loved person; 6. emotional dependency on the relationship with the loved person, including feelings of hope, apprehension, possessiveness, preoc- cupation with the beloved, hypersensitivity to cues given by the beloved, inability to concentrate on matters unrelated to the be— loved, jealousy, emotional vulnerability, fear of rejection by the beloved, fantasies about the loved person, separation anxiety, and swings in mood associated with the fluctuating state of the rela- tionship, as well as feelings of despair, lack of optimism, listless- .N Lust, Attraction, and Attachment in Mammalian Reproduction 33 ness, brooding, and loss of hope during a temporary setback in the relationship or after rejection by the loved person; 7. a powerful sense of empathy toward the loved person, including a feeling of responsibility for the beloved and a willingness to sac- rifice for the loved person; 8. a reordering of daily priorities to be available to the loved person coupled with the impulse to make a certain impression on the loved person, including changing one's clothing, mannerisms, habits, or values; 9. an intensification of passionate feelings caused by adversity in the relationship; 10. a sexual desire for the target of infatuation coupled with the de- sire for sexual exclusivity; 11. the precedence of the craving for emotional union over the de— sire for sexual union with the beloved; 12. the feeling that one’s romantic passion is involuntary and uncontrollable. Some of these psychophysiological properties of attraction suggest spe- cific neural correlates. Psychiatrist Michael Liebowitz (1983) has proposed that the exhilaration of romantic attraction is associated with heightened levels of one or more of the monoamine neurotransmitters, dopamine, norepinephrine, and serotonin, and / or phenylethylamine (PEA) in meso- limbic "reward centers” of the brain. Other properties of attraction listed above, including heightened energy, “intrusive” thinking, and focused attention, also suggest that the monoamine neurotransmitters are in- volved. To test Liebowitz’s hypothesis that one or more of these mono- amine neurotransmitters play a primary role in human romantic attraction, the rest of this section examines current data on the monoamines. Dopamine (DA) is a catecholamine. Increased concentrations of dopa- mine in the brain are associated with euphoria (Wise 1988), loss of appetite (Colle and Wise 1988), hyperactivity (Post et al. 1988), increased mental activity, a delay of the onset of fatigue, and decreased need for sleep (Kruk and Pycock 1991). Hence dopamine is a likely agent for the exhilaration, heightened energy, sleeplessness, and reduced appetite as- sociated with passionate attraction in humans. In rats, blocking the activ- ity of dopamine diminishes proceptive behaviors, such as hopping and darting reactions (Herbert 1996). Data on some drugs of abuse also sup- port the hypothesis that dopamine is a primary agent of attraction: Co- caine and amphetamines increase concentrations of dopamine in the brain (Wise 1989, 1996) and produce the exhilaration, excessive energy, .4 Human Nature, Vol. 9, No. 1, 1998 .leeplessness, and loss of appetite that are characteristic of individuals vho report being passionately in love. increased concentrations of dopamine in the brain have also been asso- iated with heightened attention, motivation, and goal-directed behaviors n humans and other mammals (Kiyatkin 1995; Salamone 1996; Scatton et II. 1988), suggesting that the focus, motivation, and goal-directed behav- ors characteristic of infatuated humans and other mammals are due to leightened concentrations of central dopamine. Dopamine neurons in- nervating the prefrontal cortex are stimulated during exposure to a novel -nvironment (Tassin et al. 1980); this may occur when an individual is 'xposed to the n0velty of a new partner. In addition, increased concentra- ions of central dopamine have been associated with "a hyperreactive, earlike state” (Lee et al. 19882324) and with anxiety and panic (Post et al. 988); both are properties of intense romantic attraction. Norepinephrine (NE) is a catecholamine chemically derived from do— >amine. The effects of norepinephrine (and dopamine) are varied, de- >ending on the receptors that they trigger. Nevertheless, increasing levels vf central norepinephrine are generally associated with exhilaration, ex- essive energy, sleeplessness, loss of appetite, and other excitatory re- ponses commonly associated with attraction. Amphetamine and related lrugs of abuse increase concentrations of norepinephrine (Seiden et al. 988), and amphetamines are regularly associated with euphoria, in- reased energy, loss of appetite, and wakefulness—all properties of ro- nantic attraction. Norepinephrine has been associated with imprinting in in avian species (Davies et al. 1985), and the focused attention characteris- iC of romantic attraction could be considered a form of imprinting on the weloved. Norepinephrine is also associated with increased memory for NEW stimuli (Griffin and Taylor 1995), a trait that could be associated with he phenomenon of “crystallization,” the increased recall of moments pent with the beloved that infatuated informants report (Tennov 1979). After administering monoamine oxidase inhibitors to "lovesick" pa- ients, Liebowitz (1983) concluded that the exhilaration of attraction is, It least in part, associated with phenylethylamine. Phenylethylamine PEA) is chemically and pharmacologically related to the catecholamines Sabelli and Iavaid 1995). Sabelli and Javaid (1995:6) report that PEA may re a neuromodulator at aminergic synapses that modulates both NE and )A synapses; they conclude that PEA works in concert with these cate- ‘holamines to elevate mood. Hence it is likely that PEA plays a secondary ole in the emotion system referred to here as attraction. Observational data on nonhuman mammals include many incidences n which individuals display increased energy, focused attention, and pal-directed behavior while courting. And several studies conclude that he catecholamines play a crucial role in the preparatory phase of sexual Lust, Attraction, and Attachment in Mammalian Reproduction 35 behavior, specifically motivation and sexual arousal (Melis and Argiolas 1995). For example, when female prairie voles are exposed to a drop of male urine on the upper lip, norepinephrine is released in specific areas of the brain olfactory bulb, stimulating the release of estrogen and concomi- tant proceptive behavior (Dluzen et al. 1981). In most mammalian species, attraction may occur as a spontaneous, brief, catecholaminergically in- duced, excitatory reaction to a conspecific that initiates sexual physiology and behavior. Serotonin (5-HT) is an indoleamine derived from tryptophan that has at least fifteen receptor subtypes, some of which may be associated with appetitive reproductive behaviors. In general, however, high levels of central serotonin have been associated with the consummatory and satiat- ing aspects of sexual behavior and a loss of sexual interest; no specific appetitive sexual behaviors have been linked with high concentrations of central serotonin (Herbert 1996; Robbins and Everitt 1996). The data relat- ing serotonin specifically to attraction in humans are conflicting. In- creased concentrations of central serotonin can suppress appetite (Cooper 1996) and produce sensations of well-being, properties associated with infatuation. But increased concentrations of central serotonin generally accelerate and prolong sleep and reduce anxiety and fearfulness (Hard— man et al. 1996; Stein and Stanley 1994); these are not properties of infatuation. Low levels of serotonin may be associated with attraction, however. Insomnia, a common property of passionate attraction, is associated with low concentrations of central serotonin (Hardman et al. 1996). In addition, serotonin-reuptake inhibitors, which increase serotonin at the synapse, are currently the agents of choice in treating most forms of obsessive- compulsive disorder (Flament et al. 1985; Hollander et al. 1988; Thoren et al. 1980), suggesting that low levels of central serotonin may contribute to obsessive "intrusive thinking,” a primary element of passionate love. Dosage effects of the above-mentioned monoamines, interactions be- tween these monoamines, and interactions between these monoamines and other central and peripheral emotion systems make analysis of this emotion system, attraction, highly complex. Yet the similarities between the psychophysiological properties of romantic attraction (listed above) and the psychophysiological properties of these monoamines suggest that dopamine, norepinephrine, and serotonin may play central roles in this emotion category (Table 1). Liebowitz (1983) proposed that the brain architecture associated with romantic attraction involves mesolimbic "pleasure centers.” The brain’s “pleasure centers" were first described in the 19505 (Olds 1956; Olds and Milner 1954; see Wise 1996). But recent advances in the neurophysiology of addiction, as well as other studies, have refined our understanding of 35 Human Nature, Vol. 9, No. 1, 1998 Table 1. The Three Proposed Emotion Categories for Mammalian Mating and Reproduction and Their Associated Hormones and Neurotransmitters in the Brain (Listed are molecules that have an action in the brain and that play a major, but not exclusive, role in lust, attraction, or attachment. Evidence for the role of these molecules in the different emotions comes from rodent and human data.) m Lust Attraction Attachment (Sex Drive) (Obsession/Attention) (Comfort, Parenting) Androgens Catecholamines: Oxytocin I Estrogens Dopamine Vasopressin Norepinephrine Phenylethylamine (PEAV Serotonin 'PEA is associated with catecholaminergic cells and sympthomimetic functional effects. It may be a modulator of aminergic synapses and not a classic neurotransmitter. some of the primary areas of the brain’s "reward circuitry,” and the mesocorticolimbic dopamine system is strongly implicated (Wise 1996). Wise (1989, 1996) proposes that a central component of the brain’s reward circuitry is increased concentrations of dopamine at dopamine receptors localized to specific subpopulations of neurons in the nucleus accumbens and prefrontal cortex. Discussing the neurobiology of motiva- tion and reinforcement, Robbins and Everitt (1996:229) concur, implicat- ing the mesolimbic dopamine system that projects from the ventral tegmental area to the ventral striatum, including the nucleus accumbens (Figure 1). Several neuroscientists report that related structures are most likely also involved, including the basolateral amygdala, the hippocampal formation, and the prefrontal cortex (Gallagher and Chiba 1996; Robbins and Everitt 1996). The amygdala is a phylogenetically old brain structure that is centrally involved in the function of the autonomic nervous system (Kilts et al. 1988). So specific areas within the amygdaloid complex associ- ated with dopamine (Kilts et al. 1988) and the control of arousal (Gal- lagher and Chiba 1996) most likely play central roles in the peripheral excitatory responses associated with attraction.2 The specific neural circuitry of the brain’s system for motivation, rein- forcement, pleasure, and / or reward is complex (see Kalivas and Neme- roff 1988). Other brain areas associated with catecholaminergic activity could be involved (Figure l), and neurotransmitters other than dopamine are currently being investigated (Robbins and Everitt 1996). Nevertheless, this mesocorticolimbic reward system in the brain is associated with heightened energy, motivational processes, and goal-directed behavior in a range of mammalian appetitive categories of emotion, including the Search for preferred foods and preferred drugs (Kiyatkin 1995; Robbins and Last, Attraction, and Attachment in Mammalian Reproduction 37 Amygdala 1 ® Androgen. and unoan @ Oxytocln and vuopnnln ® Amen-m, «hogan. oxytocln, vamp-"In. nonplmptulno Cat-cholamlnn w NdeJocmcoomlwc © NW. ventral twmmn GD bop-mm...“th nlpu.vonlnllogmonht|ru ({{D W.MWW — ) mummmwmmm Figure 1. Brain areas and primary hormones and neurotransmitters associated with lust, attraction, and attachment. The simplified human brain drawing shows the principal sources and targets of the hormones and neurotransmit- ters implicated in the emotions of lust (androgens and estrogens), attraction (catecholamines), and attachment (oxytocin and vasopressin). Sources of the hormones for lust are the gonads; sources of the hormones for attachment are the PVN / SON of the hypothalamus. Sources of the catecholamines are cell groups in lower hindbrain areas including the locus coeruleus, ventral teg- mental area, and substantia nigra. Targets of the hormones tend to be in lower brain areas whereas major targets of the catecholamines are in the forebrain. The mesocorticolimbic dopaminergic projections are known for their role in euphoria and positive reinforcement and may play a primary role in the emotions associated with attraction in humans. PVN / SON refers to the para- ventricular and supraoptic nuclei of the hypothalamus. 38 Human Nature, Vol. 9, No. 1, 1998 Everitt 1996). So it is parsimonious to suggest that this neural system is part of the constellation of neural correlates associated with some of the properties of attraction, including exhilaration; increased energy; auto- nomic reactions such as loss of appetite, sleeplessness, and a pounding heart; motivation; goal-oriented behaviors; and focused attention on a preferred mate. Attraction may be associated with a range of other neural regions as well. As Davidson (1994:241) writes, "emotion-specific patterning at the discrete emotion level may be found in those brain circuits that are not exclusively devoted to emotional processing, but also are involved in higher-order cognitive processes.” Since cultural rules and childhood ex- periences contribute a great deal to human mating behavior, it is logical to suggest that a range of higher-order cognitive processes and correspond- ing cortical structures also are involved in human attraction. Hatfield and Walster (1978) distinguish between reciprocated love, as- sociated with fulfillment and ecstasy, and unrequited love, associated with emptiness, anxiety, and despair. Their data, along with the many descriptions of romantic love in other psychological literature and de— scriptions of attraction in thousands of myths, legends, stories, novels, poems, and works of nonfiction cross-culturally, suggest that passionate romantic attraction takes a variety of graded forms, from elation to de- spair, from calm to anxiety. So it is expected that the constellation of neural correlates associated with these gradations of attraction will vary accordingly. For example, most likely the relationship among the cate- cholamines and serotonin varies in specific ways as a romantic relation- ship becomes more or less reciprocated. Analysis of infatuated subjects, using in-depth questionnaires in conjunction with functional magnetic resonance imaging of the subjects’ brains, may establish more definitively some of the fundamental anatomical and neurochemical components of mammalian attraction (Fisher et al. n.d.a, n.d.b). Data already exist, however, to suggest that attraction is a discrete emotion category distinct from the sex drive: 61% of Tennov’s female infomants and 35% of male informants agreed with the statement, "I have been in love without feeling any need for sex”; 95% of Tennov’s female informants and 91% of her male subjects rejected the statement, “The best thing about love is sex" (Tennov 1979:74). These informants distinguished between the sex drive and feelings of romantic attraction. Moreover, humans can feel the urge for sexual consummation with a partner without feeling romantic attraction toward this partner. The dis- tinction between attraction and lust is also observable in other mammals. Mammals regularly express the drive for sexual consummation, yet most prefer some partners and reject others. Lust, Attraction, and Attachment in Mammalian Reproduction 39 So it is parsimonious to conclude that the constellation of neural corre- lates associated with attraction are distinct from those associated with the sex drive; that these emotion systems operate along conjoining and / or closely linked neural circuits; and that each of these emotion categories evolved to direct a distinct aspect of mammalian reproduction: Lust evolved to motivate individuals to seek sexual gratification with any con- specific, and attraction evolved to enable individuals to focus their mating effort on preferred mating partners. In humans, attraction is mediated by a host of cultural stimuli. When an individual falls in love, where they fall in love, with whom they fall in love, how they court, even whether they choose to act on their bodily sensations of attraction can be expected to be influenced by childhood experiences, by myriad other cultural forces, and by individual volition. But the actual feeling an individual experiences as he / she becomes attracted to a pre- ferred conspecific is a product of the evolution of the mammalian brain designed to enable individuals to choose genetically superior mating partners. ATTACHMENT Many scientists have discussed mother—infant bonding and its role in aspects of adult attachment (Ainsworth 1969, 1989; Ainsworth et al. 1978; Shaver and Hazan 1993; Shaver et al. 1988). But these investigations con- centrate on types of psychological attachment and the development of psy- chological attachment through the life course; instead, the present paper defines this emotion system, specifies some of the neural mechanisms associated with all forms of attachment behavior, and cites data to estab- lish that this emotion system, attachment, is distinct from that of the sex drive and attraction. Neuroscientists currently distinguish appetitive and consummatory be— haviors as distinct behavioral and physiological phenomena; they regard the neural substrates of these categories of emotion as distinct (see Robbins and Everitt 1996); and they regard attachment as an emotion associated with consummatory behavior (see Pedersen et a1. 1992). Psy- chologists have recognized attachment as a specific emotion system since John Bowlby began to investigate and record attachment behaviors in humans and other mammalian species in the 19503 (see Bowlby 1969, 1973, 1980). Bowlby (1969:179) regarded attachment behavior “as a class of social behaviour of an importance equivalent to that of mating behav- iour . . . that had a biological function specific to itself" (emphasis added). He 40 Human Nature, Vol. 9, No. 1, 1998 described attachment behavior as "what occurs when certain behavioural systems are activated” (Bowlby 1969:179). Attachment behaviors in social mammals include recognizing con- specifics to whom one is attached, preferring the company of these con- specifics, maintaining proximity (often close body contact), exhibiting Species-specific patterns of touch, displaying separation anxiety when apart, and attempting to restore close contact after separation (Bowlby 1969; Mendoza and Mason 1997). Attachment behaviors also include mo- nogamous male-female affiliative gestures and monogamousparental behaviors, such as territory defense, nest building, mutual feeding, grooming, and shared parental chores (see Carter et al., eds. 1997; Ped- ersen et al. 1992). In humans, the above-mentioned behavior patterns associated with attachment are accompanied by reported feelings of closeness, security, peace, social comfort, mild euphoria, and reduced anxiety when in contact with a partner, and separation anxiety when apart for a length of time (Liebowitz 1983). Psychologists describe human attachment as "the affection we feel for those with whom our lives are deeply entwined” (Hatfield 1988:205). Several neuropeptides have been implicated in male-female bonding, group bonding, and mother-infant bonding in mammals (see Carter et al. 1997; Insel 1992; Pedersen et al. 1992). But recent data indicate that oxy- tocin and vasopressin released in the central nervous system are the primary hormones that produce monogamous male-female attachment and monogamous parenting behaviors in mammals (Carter 1992; Carter et al. 1995; Insel et al. 1993; see Pedersen et al. 1992; Winslow et al. 1993). Vasopressin is produced primarily in the supraoptic (SON) and para- ventricular (PVN) nuclei of the hypothalamus. Oxytocin, which varies from vasopressin by two amino acids, is also produced primarily in the supraoptic and paraventricular nuclei of the hypothalamus (Carter 1992). Carter and colleagues report that among monogamous prairie voles, "no evidence currently exists that gonadal hormones play a role in the partner preference component of pair bonding” (Carter et al. 19972263); instead oxytocin and vasopressin play a predominant role in maintaining these sustained monogamous attachments (see Carter et al. 1997). And although the neural correlates of attachment are associated with those for the sex drive (Insel 1992), several neuroscientists view the constellation of neural correlates associated with attachment as a specific emotion catego- ry (Carter 1992; Carter et al. 1995; Inselet al. 1993; see Pedersen et al. 1992; Winslow et al. 1993). Observational data on humans support the hypothesis that the neural correlates of attachment are distinct from those of the sex drive and those of attraction. Arranged marriages, for example, are common cross- culturally (Frayser 1985), as are longterm marriages (Fisher 1989, 1992, Last, Attraction, and Attachment in Mammalian Reproduction 41 1994, 1995). Spouses in arranged marriages and long—term marriages reg- ularly maintain attachment to one another, express feelings ofattachment for one another, and display mutual parental duties without displaying or reporting feelings of attraction or sexual desire for one another. HUMAN MATING FLEXIBILITY A primary characteristic of human reproductive strategies is monoga— mous marriage. Monogamous marriage is the predominant mating tactic in all contemporary societies (Fisher 1989, 1992; Lancaster and Kaplan 1994; Murdock 1949; van den Berghe 1979). All cultures have procedures for initiating and sustaining monogamous marriage, traditions for over- coming the trauma of separation anxiety at the termination of monoga- mous marriage, and means for negotiating monogamous remarriage. Sexual jealousy is also universal to human cultures; humans, as a rule, do not share long-term partners to whom they are attached unless the envi- ronmental and cultural perquisites considerably outweigh the defic1ts. Because monogamous attachment is not characteristic of the African apes, it is parsimonious to suggest that the specific constellation of neural corre— lates associated with sustained monogamous attachment evolved at some point in hominid evolution.3 I - . . But sustained monogamous attachment is not an exclusive hominid reproductive strategy; secondary opportunistic reproductive strategies are also prevalent in humans. Opportunistic serial monogamy is univirsal to human societies (Fisher 1992). Opportunistic polygyny occurs in 83 /o of human cultures (van den Berghe 1979).‘I Opportunistic polyandry occurs in 5% of cultures (van den Berghe 1979). Opportunistic extra-pair attach- ments occur in all cultures for which data are available (Fisher 1992),.and humans exhibit other secondary forms of attachment in assoc1ation With a range of environmental variables (Lancaster and Kaplan 1994). Mating flexibility is a hallmark of Homo sapiens. ' ‘ I These data suggest that during the course of hominid evolution the constellations of neural correlates associated with lust, attraction, and attachment became increasingly independent of one another, enabling hominids to exercise mating flexibility and engage (sometimes Simul- taneously) in a range of primary and secondary opportunistic reproduc- tive strategies. CONCLUSION Many scientists have presented lists of primary categories of emotion in mammals. Panksepp and colleagues (1997280) note that for several of 42 Human Nature, Vol. 9, No. 1, 1998 these emotions "existing neurobiological data are affirming that distinct brain circuits exist.” The present paper attempts to isolate the primary categories of emotion associated with mammalian reproduction; to pre- sent these emotion systems as a useful model for categorizing aspects of mating behavior in mammals; to propose the evolutionary relationship between attraction, mate choice, and sexually selected, species—specific traits; and to offer a hypothesis for the flexibility and range of contempo- rary patterns of mating and reproduction in Homo sapiens. It is proposed that mammals exhibit three interrelated, bidirectional yet, in some species, distinct emotion systems for mating that evolved to regulate three primary aspects of mammalian reproduction: the sex drive associated primarily with the androgens and estrogens, motivates indi: viduals to seek sexual gratification with any conspecific; the attraction system, associated primarily with the catecholamines, motivates indi— viduals to focus their mating effort on preferred conspecifics; and the at- tachment system, associated primarily with oxytocin and vasopressin motivates individuals to assume species-specific parental duties. I The precise composition, duration of activation, and activities of the neural mechanisms associated with each of these three emotion systems can be expected to vary according to the primary reproductive strategy of each. species. These emotion systems can also be expected to vary within specres from one individual to the next, across the life course, according to gender, and in response to specific environmental opportunities and exi- gencres. These emotion systems can also be expected to be closely interre- lated and to work in concert with one another and with other bodily systems. Nevertheless, the constellations of neural correlates associated with the sex drive, attraction, and attachment are also proposed to be distinct from one another in some mammals, including humans. Men and women can express attachment for a long-term mate, attraction to a different con- specxfic, and the sex drive in response to stimuli unrelated to either of these individuals. The independence of these emotion systems in humans evolved to take advantage of rare mating opportunities and to pursue a mixture of short-term and long-term reproductive strategies simul— taneously or in succession. Hence the independence of these emotion systems enabled mating flexibility in hominid populations of the past and contributes to contemporary patterns of human serial monogamy extra- pair copulations, and other variations in the wide range of human inatin and reproductive behaviors. 8 At least 25% of homicides in the United States involve spouses sexual partners, or sexual rivals (Daly and Wilson 1988). Any given year ap- proxrmately 1.8 million wives in the United States are beaten by their husbands (Strauss 1978); male jealousy is the most common cause of wife Lust, Attraction, and Attachment in Mammalian Reproduction 43 battering cross-culturally (see Smuts 1992; Daly and Wilson 1988). Fifty- six percent of American college women in one study reported being harassed by a rejected lover (Jason et al. 1984). An untold number of husbands receive physical abuse from wives as well, and many other crimes of passion, as well as incidences of stalking and cases of clinical depression and suicide, are commonly associated with romantic attrac- tion cross-culturally (Hatfield and Rapson 1996; Tennov 1979). So the model presented here for identifying attraction as a specific emotion sys- tem, independent from the sex drive and from attachment, may be useful to understanding some patterns of human criminal, social, and reproduc- tive behavior. The author thanks Lucy L. Brown (Albert Einstein College of Medicine, Neuro- science) for designing the table and figure that accompany this article. The au~ thor also thanks the following individuals for reading versions of the manuscript: Lucy L. Brown (Albert Einstein College of Medicine, Neuroscience); Michelle Cristiani (University of New Mexico, Graduate Student, Anthropology); Steven Glickman (University of California, Berkeley, Psychology); Wade Mackey (South- eastern CC, Psychology); John Munder Ross (Cornell University Medical Center, Psychiatry); James B. Ranck, Jr. (SUNY Health Sciences Center at Brooklyn, Physi- ology); Gregory V. Simpson (Albert Einstein College of Medicine, Neuroscience); Barbara Smuts (University of Michigan, Psychology); Fred Suffet (Center for Com- prehensive Health Practice, Sociologist); and MacGregor Suzuki (MacGregor Su- zuki, Inc, statistician). All errors are those of the author. Helen Fisher, Ph.D./Physical Anthropology, is a research associate in the Department of Anthropology, Rutgers University. She is author of Anatomy of Love (W. W. Norton 1992/ Faucett 1994), The Sex Contract: The Evolution of Human Behavior (William Morrow 1982/ Quill 1983), and several articles on the evolution of serial monogamy among Homo. Her research interests include the evolution of the emotions, human reproductive strategies, and gender differences in behavior and the brain. NOTES 1. Discussion of avian mating systems is beyond the scope of this paper, but it is likely that avian species exhibit related anatomical and neurohormonal emotion systems for mating. 2. Because depletion of dopamine in the brain's reward circuitry has been proposed as a consequence of drug withdrawal (Wise 1996),.a similar drop in dopamine levels in the central reward system may account for the feelings of depression, loss of energy, and lack of motivation associated with rejection by a conspecific to whom one is attracted. 3. 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