Elsevier

Psychoneuroendocrinology

Volume 23, Issue 8, November 1998, Pages 779-818
Psychoneuroendocrinology

NEUROENDOCRINE PERSPECTIVES ON SOCIAL ATTACHMENT AND LOVE

https://doi.org/10.1016/S0306-4530(98)00055-9Get rights and content

Abstract

The purpose of this paper is to review existing behavioral and neuroendocrine perspectives on social attachment and love. Both love and social attachments function to facilitate reproduction, provide a sense of safety, and reduce anxiety or stress. Because social attachment is an essential component of love, understanding attachment formation is an important step toward identifying the neurobiological substrates of love. Studies of pair bonding in monogamous rodents, such as prairie voles, and maternal attachment in precocial ungulates offer the most accessible animal models for the study of mechanisms underlying selective social attachments and the propensity to develop social bonds. Parental behavior and sexual behavior, even in the absence of selective social behaviors, are associated with the concept of love; the analysis of reproductive behaviors, which is far more extensive than our understanding of social attachment, also suggests neuroendocrine substrates for love. A review of these literatures reveals a recurrent association between high levels of activity in the hypothalamic–pituitary–adrenal (HPA) axis and the subsequent expression of social behaviors and attachments. Positive social behaviors, including social bonds, may reduce HPA axis activity, while in some cases negative social interactions can have the opposite effect. Central neuropeptides, and especially oxytocin and vasopressin have been implicated both in social bonding and in the central control of the HPA axis. In prairie voles, which show clear evidence of pair bonds, oxytocin is capable of increasing positive social behaviors and both oxytocin and social interactions reduce activity in the HPA axis. Social interactions and attachment involve endocrine systems capable of decreasing HPA reactivity and modulating the autonomic nervous system, perhaps accounting for health benefits that are attributed to loving relationships. © 1998 Elsevier Science Ltd. All rights reserved.

Section snippets

WHAT IS LOVE?

Attachment, commitment, intimacy, passion, grief upon separation, and jealousy are but a few of the feelings or emotions sometimes used to describe love (Hatfield and Rapson, 1993, Sternberg and Barnes, 1988). From a scientific perspective, love is a hypothetical construct with many dimensions and interpretations. However, the various emotional states and behaviors associated with love are rarely investigated. In part this is because love has been the domain of poets, novelists, and clinicians,

DEFINITIONS AND MEASUREMENTS OF LOVE AND ATTACHMENT

Love and social attachments function to facilitate reproduction, provide a sense of security and reduce feelings of stress or anxiety. The neurobiology of love is interwoven, phylogenetically and ontogenetically, and in adulthood with reproduction and homeostasis (Uvnas-Moberg, 1997).

Attachment is a component of most, if not all, definitions of human love (Bartholomew and Perlman, 1994, Sternberg and Barnes, 1988). Although attachment may exist in the absence of love, it is unlikely that love

EVOLUTIONARY AND CROSS-SPECIES PERSPECTIVES ON ATTACHMENT

Survival and reproduction can depend on the ability to adapt patterns of social and reproductive behavior to environmental and social demands. Social attachments function to facilitate reproduction, provide a sense of security and reduce feelings of stress or anxiety (Fig. 1). Mammals generally are social creatures, often living and reproducing in pairs or groups. Pairs and larger groups, such as families or troops, are held together by social bonds or selective social behaviors. The expression

Basic Behavioral Systems and Attachment

The tendency to approach or avoid a particular set of social stimuli is fundamental to social behaviors, and attachment behaviors. Some stimuli may be inherently positive or may elicit positive responses; other stimuli, particularly those that are novel, can be innately aversive or fear-inducing. Studies of the physiology of positive social behaviors, including affiliative and reproductive behaviors may be especially relevant to understanding the biology of attachment. Specific physiological

WHEN ARE ATTACHMENTS FORMED?

Evidence for attachment formation comes from behavioral changes associated with mammalian birth, lactation and sexual interactions (Table 1). In addition, novel or stressful experiences may encourage increased social behaviors and attachment. Comparatively high levels of HPA axis activity or other indications of sympathetic arousal, and the subsequent release of oxytocin have been measured under conditions that commonly precede or are associated with the formation of social bonds.

ENDOCRINE THEORIES OF SOCIAL ATTACHMENT: OVERVIEW

Data from a variety of species and different paradigms implicate oxytocin and vasopressin in social attachment and in related prosocial and reproductive behaviors, including parental and sexual behaviors. Some, but not all, of the behavioral effects of oxytocin are similar to those seen after vasopressin treatment. In addition, vasopressin, but not oxytocin, has been associated with agonistic and territorial behaviors, including mate guarding (Winslow et al., 1993). The endogenous opioids also

Oxytocin and Vasopressin: Structure and Synthesis

Oxytocin and vasopressin are small peptides, consisting of nine amino acids, configured as a six amino acid ring with a three amino acid tail. Oxytocin and vasopressin differ from each other in two amino acids and may have evolved from a common ancestral peptide (Acher, 1996, Carter et al., 1995, De Wied et al., 1993, Engelmann et al., 1996, Pedersen et al., 1992). The gene for these two peptides occupies the same chromosome. There is abundant evidence for functional interactions among these

HORMONAL EFFECTS ON PAIR BONDING

Prairie voles, small arvicoline rodents from the midwestern United States, have proven particularly amenable to the experimental analysis of pair bond formation. Prairie voles live in pairs and show well-defined behavioral preferences for their familiar partner (Getz et al., 1981). Pair bonding in this species is assessed by allowing an experimental animal to chose between a stimulus animal made familiar by association or cohabitation, or a comparable stranger (Carter et al., 1995). Both

SEPARATION DISTRESS AND SOCIAL BUFFERING

Separation from an attachment figure is associated with various behavioral and physiological changes (Hennessy, 1997, Reite and Field, 1985, Reite and Boccia, 1994). In young animals vocalizations, in either the audible or ultrasonic range, often increase following separation. Measurements of these vocalizations have been used as indices of distress and may be indicative of attachment (Panksepp et al., 1997).

Physiological changes, including increased secretion of glucocorticoids and/or ACTH,

Overview

The most accepted form of enduring social bond is maternal attachment. The concept of mother love (Harlow, 1986) implies a selective behavioral response by the parent to its offspring. Because of the intimate relationship between parental responses and attachments, and the conservative nature of hormone and behavior relationships, understanding parental behavior, even in cases when the behaviors are not selectively directed to a particular infant, may provide insights into the physiological of

SEXUAL BEHAVIOR

Sexual behavior and attachment are related, but not synonymous concepts. Sexual activity can occur in the absence of social attachment and many forms of attachment do not involve sexual behavior. In humans the most desired sexual partner often is the object of strong feelings of attachment, but exceptions may exist to this pattern.

In monogamous mammals, pair bonds provide a social matrix for sexual behavior. Mating also promotes social preferences (Williams, et al., 1992), possibly because

Ontogenetic Influences on Attachment

Steroid exposures during development have the capacity to produce both structural and behavioral changes (Gorski, 1990), including changes that may alter the propensity for social behavior. For example, in prairie voles prenatal steroid treatments (either testosterone or corticosterone) are associated with an increased preference for familiar versus unfamiliar partners, while postnatal treatments with these same hormones were associated with a preference for strangers (Roberts et al., 1996).

STEROID–PEPTIDE INTERACTIONS

Steroid effects on peptide production. Oxytocin synthesis and release are sensitive to gonadal steroids, including estrogens and androgens (Caldwell, 1992, Rhodes et al., 1981). For example, an estrogen-sensitive promotor has been identified on the oxytocin gene (Zingg et al., 1995). Treatment with a regimen of ovarian steroids that approximates the hormonal profile during late pregnancy and near the time of parturition (chronic estrogen and progesterone followed by progesterone withdrawal)

Oxytocin and Vasopressin

Behavioral studies indicate that some behavioral effects of oxytocin and vasopressin are similar, while in other cases these peptides are functionally antagonistic (Bohus et al., 1978, De Wied et al., 1991, De Wied et al., 1993, Engelmann et al., 1996, Pedersen et al., 1992). For example in rats, passive avoidance (De Wied et al., 1991), and locomotor and autonomic functions (Roozendaal et al., 1993) have indicated that oxytocin and vasopressin can have either similar or apparently opposite

PEPTIDES AND THE AUTONOMIC NERVOUS SYSTEM

Hormones act on the ANS to integrate attention, emotional states and social communication, with other physiological and environmental demands. The ANS is essential for social attachment and love and also contains receptors for oxytocin and vasopressin. The various subcomponents of the ANS suggest sites at which peptides such as oxytocin and vasopressin could act to regulate these behavior.

The polyvagal theory of Porges, 1995, Porges, 1997(this volume) differentiates between a phylogenetically

Behavioral-emotional Models of Attachment

Stressful experiences (such as pregnancy and parturition), anxiety, neophobia and isolation often precede the formation of social attachments (Fig. 1, Fig. 2). These circumstances may increase social drive or motivation and subsequent social interactions. Positive social interactions in turn could be rewarding and in species or individuals that possess the capacity to form attachment, positive social bonds would follow. Both positive social interactions and social bonds could function to

The Nature of Social Attachment

Awareness that social attachment could have physiological substrates is recent, and there are far more questions than answers. For example, is attachment one process or many? Do attachments that form slowly, during long-term associations, including lactation or nonsexual cohabitation, have the same physiology as those that form quickly, for example during an acute experience, such as birth or sexual interactions? Are the mechanisms involved in the formation of a social attachment also

METHODOLOGICAL ISSUES AND THE STUDY OF HORMONAL CORRELATES OF HUMAN ATTACHMENT

Although animal research supports the hypothesis that oxytocin and vasopressin may influence social attachment, very little human research directly addresses this issue. Because neurohypophyseal hormones do not readily pass the blood–brain barrier, it is generally assumed that oxytocin and vasopressin released from the posterior pituitary gland cannot easily return to the brain. Animal research, however, suggests that oxytocin and vasopressin can affect behavior through actions both within the

CLINICAL IMPLICATIONS OF A PEPTIDERGIC THEORY OF SOCIAL ATTACHMENT

The presence or absence of attachments has broad consequences across the lifespan. Like other mammals, humans rely on positive social interactions for both safety and reproduction. It has been argued that the tendency to form pair bonds or social attachments is a universal human characteristic (Fisher, 1992, Hazan and Shaver, 1987). Social support has documented health benefits, and the absence of positive social interactions or social bonds typically is associated with both physical and mental

CONCLUSIONS

The expression of attachments must incorporate genetic potentials and limitations associated with species variations, sex differences and individual experiences. Such changes require both short-term and long-lasting modifications of the nervous system. Steroids, neuropeptides and their interactions provide potential substrates for behavioral processes including those that are necessary for social attachment. Steroid hormones can regulate synthesis, release and receptor binding for oxytocin and

Acknowledgements

I wish to acknowledge the generous advice of Stephen Porges who helped in the development of many of the organizing principles used to structure this review. I am thankful to Courtney DeVries for her help in understanding the role of the HPA axis in pair bonding, and to Bruce Cushing, Diane Witt, Leah Gavish, Luci Roberts, Mary Cho, Katie Bowler, John Stribley, Susan Taymans, Jessie Williams, Zuoxin Wang and Tom Insel for their collaborations and for allowing me in some cases to discuss their

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