OXYTOCIN MAY MEDIATE THE BENEFITS OF POSITIVE SOCIAL INTERACTION AND EMOTIONS

doi:10.1016/S0306-4530(98)00056-0

Psychoneuroendocrinology

Volume 23, Issue 8, November 1998, Pages 819-835

https://doi.org/10.1016/S0306-4530(98)00056-0 Get rights and content

Abstract

During breastfeeding or suckling, maternal oxytocin levels are raised by somatosensory stimulation. Oxytocin may, however, also be released by nonnoxious stimuli such as touch, warm temperature etc. in plasma and in cerebrospinal fluid. Consequently, oxytocin may be involved in physiological and behavioral effects induced by social interaction in a more general context. In both male and female rats oxytocin exerts potent physiological antistress effects. If daily oxytocin injections are repeated over a 5-day period, blood pressure is decreased by 10–20 mmHg, the withdrawal latency to heat stimuli is prolonged, cortisol levels are decreased and insulin and cholecystokinin levels are increased. These effects last from 1 to several weeks after the last injection. After repeated oxytocin treatment weight gain may be promoted and the healing rate of wounds increased. Most behavioral and physiological effects induced by oxytocin can be blocked by oxytocin antagonists. In contrast, the antistress effects can not, suggesting that unidentified oxytocin receptors may exist. The prolonged latency in the tail-flick test can be temporarily reversed by administration of naloxone, suggesting that endogenous opioid activity has been increased by the oxytocin injections. In contrast, the long-term lowering of blood pressure and of cortisol levels as well as the sedative effects of oxytocin have been found to be related to an increased activity of central α₂-adrenoceptors. Positive social interactions have been related to health-promoting effects. Oxytocin released in response to social stimuli may be part of a neuroendocrine substrate which underlies the benefits of positive social experiences. Such processes may in addition explain the health-promoting effects of certain alternative therapies. Because of the special properties of oxytocin, including the fact that it can become conditioned to psychological state or imagery, oxytocin may also mediate the benefits attributed to therapies such as hypnosis or meditation. © 1998 Elsevier Science Ltd. All rights reserved.

Section snippets

INTRODUCTION

This paper examines the hypothesis that positive social interactions and emotions are associated with an unified pattern of physiological and behavioral events. Social interactions incorporate the exchange of physical and emotional energy. As a consequence these interactions, and the accompanying positive emotional states, lead to physiological adaptations necessary for relaxation, digestion, anabolic metabolism, growth and healing. The corresponding mental states associated with positive

NEUROENDOCRINE MECHANISMS INVOLVED IN DEFENSE AND FIGHT–FLIGHT REACTIONS

When an animal displays active responding to stress by escaping or dealing with environmental challenge, fight–flight prevails and the sympathetic adrenomedullary system is preferentially activated. The fight–flight response is associated with a neurogenic increase of cardiac output facilitated by concomitant blood volume centralization due to widespread vasoconstriction. Here the increased cardiac output favours skeletal muscles, myocardium and brain as their resistance vessels become dilated,

NEUROENDOCRINE MECHANISMS INVOLVED IN POSITIVE SOCIAL INTERACTIONS

Far less is known about the neuroendocrine mechanisms of positive interactive behaviors than those of defense reactions. Suckling or breastfeeding, aspects of maternal behavior, represent examples of positive social interactions which have been explored in depth from a physiological and neuroendocrine point of view. In order to facilitate the description of neuroendocrine mechanisms, this kind of interaction can be divided into different phases of functional activity. Thus, before each suckling

OXYTOCIN

Oxytocin released by the suckling stimulus during lactation causes ejection of milk by contracting the myoepithelial cells in the mammary glands. As will be discussed below, other suckling-induced behavioral, physiological and endocrinological changes occurring during lactation also may be caused by oxytocin.

Oxytocin, which is produced in the supraoptic (SON) and paraventricular (PVN) nuclei of the hypothalamus, is released into the circulation from magnocellular neurons which extend down to

ROLE OF OXYTOCIN IN LACTATION

Oxytocin facilitates the onset of maternal behaviour in sheep and rats and has been shown to promote bonding between ewe and lamb (Kendrick et al., 1987). Considering the physiological effects of oxytocin, the role of this hormone in the ‘giving’ aspect of interactions with offspring is not restricted to milk ejection. Oxytocin also induces vasodilation in the skin overlying the mammary gland, thus promoting transfer of warmth to the pups (Eriksson et al., 1996). Furthermore, oxytocin helps to

MECHANISMS INVOLVED IN EFFECTS CAUSED BY OXYTOCIN

Most behavioural and physiological effects induced by administration of oxytocin can be blocked by an antagonist directed against the uterine receptor. The increased weight gain and the enhanced healing rate of wounds also can be prevented if the oxytocin treatment is combined with administration of the oxytocin antagonist (Petersson et al., in press aUvnäs-Moberg et al., 1996a, Uvnäs-Moberg et al., 1996b). In contrast, the ‘antistress’ effects cannot be blocked by this antagonist, suggesting

ROLE OF OXYTOCIN IN PSYCHOLOGICAL ADAPTATIONS IN BREASTFEEDING WOMEN

As mentioned above, oxytocin promotes maternal behaviour and attachment between mother and offspring in sheep and rats. But does oxytocin induce analogous effects in humans? There is some indirect evidence showing that this may indeed be the case. Mothers having had their newborns skin-to-skin immediately after birth, spend more time with their babies, they interact more with their infants during breastfeeding (Widström et al., 1990), and breastfeed for a longer period (Klaus et al., 1972,

OTHER TYPES OF INTERACTION IN WHICH EFFECTS OF OXYTOCIN MAY BE INVOLVED

In this review, the role of oxytocin in behavioral, physiological and endocrine aspects of lactation has been emphasized. However, oxytocin also may play a similar role in other kinds of social interaction. Oxytocin is known to stimulate sexual behavior in rats and has been shown to be released in response to sexual interactions in both rats and humans. It is, therefore, possible that oxytocin is involved in some of the physiological and behavioral adaptations that occur during sexual behavior (

MECHANISMS THROUGH WHICH SOCIAL BEHAVIOR CAN REDUCE STRESS AND PROMOTE HEALTH

Oxytocin has emerged as a core component of the mechanisms mediating the health benefits and antistress effects of positive social interactions. It has been shown that oxytocin treatments increase social contact in several animal species (Carter et al., 1995, Witt et al., 1992). In addition, in monogamous voles, oxytocin is essential for selective social behaviors and the formation of pair bond (Williams et al., 1994).

Positive social behaviors and social bonding are characterized by repeated

Acknowledgements

This study was supported by grants from the Swedish Medical Council (K98-04X-05207-21C).

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¹: The purpose of this paper is to describe the neuroendocrine mechanisms of positive social interactions.

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OXYTOCIN MAY MEDIATE THE BENEFITS OF POSITIVE SOCIAL INTERACTION AND EMOTIONS1

Abstract

Section snippets

INTRODUCTION

NEUROENDOCRINE MECHANISMS INVOLVED IN DEFENSE AND FIGHT–FLIGHT REACTIONS

NEUROENDOCRINE MECHANISMS INVOLVED IN POSITIVE SOCIAL INTERACTIONS

OXYTOCIN

ROLE OF OXYTOCIN IN LACTATION

MECHANISMS INVOLVED IN EFFECTS CAUSED BY OXYTOCIN

ROLE OF OXYTOCIN IN PSYCHOLOGICAL ADAPTATIONS IN BREASTFEEDING WOMEN

OTHER TYPES OF INTERACTION IN WHICH EFFECTS OF OXYTOCIN MAY BE INVOLVED

MECHANISMS THROUGH WHICH SOCIAL BEHAVIOR CAN REDUCE STRESS AND PROMOTE HEALTH

Acknowledgements

Neuroscience Letters

Neuroscience

Neuroscience and Biobehavior

Regulatory Peptides

Neuroscience and Biobehavior

Psychoneuroendocrinology

Journal of the American Academy of Child Adolescence

Brain Research Bulletin

Brain Research

Neuroscience Letters

Neuroscience Letters

Brain Research

Neuroscience Letters

Physiology and Behavior

Trends in Pharmacological Science

Early Human Development

Physiology and Behavior

Neuroscience

Peptides

Lancet

Trends in Neuroscience

Pharmacology and Biochemical Behavior

Regulatory Peptides

Neuroscience

Trends in Endocrinology and Metabolism

Pharmacology Biochemistry and Behavior

Physiology and Behavior

Early Human Development

Pharmology and Biochemical Behavior

Pharmacology and Biochemical Behavior

Olfactory cues from an oxytocin-injected male rat can induce antinociception in its cage mates

NeuroReport

Suppression of hypothalamic–pituitary–adrenal axis to stress in lactating women

Journal of Clinical Endocrinology and Metabolism

Suckling induced attenuation of plasma cortisol concentrations in postpartum lactating women

Endocrinological Research

Evidence of a peripheral and a central effect of oxytocin on pancreatic hormone release in rats

Neuroendocrinology

The Wisdom of the Body

OXYTOCIN MAY MEDIATE THE BENEFITS OF POSITIVE SOCIAL INTERACTION AND EMOTIONS¹