Oxytocin Enhances the Encoding of Positive Social Memories in Humans

doi:10.1016/j.biopsych.2008.02.008

Biological Psychiatry

Volume 64, Issue 3, 1 August 2008, Pages 256-258

https://doi.org/10.1016/j.biopsych.2008.02.008 Get rights and content

Background

In nonhuman mammals, oxytocin has a critical role in social recognition and the development of long-term bonds. There has been limited research evaluating effects of oxytocin on the encoding and recognition of faces in humans.

Methods

In a double-blind, randomized, placebo-controlled, between-subject design, we administered oxytocin (24 IU) or a placebo to 69 healthy human male volunteers and then presented 36 happy, angry, or neutral human faces. Participants returned the following day to make “remember,” “know,” or “new” judgments for a mix of 72 new and previously seen faces.

Results

Oxytocin-administered participants were more likely to make remember and know judgments for previously seen happy faces compared with angry and neutral human faces. In contrast, oxytocin did not influence judgments for faces that had not been presented previously.

Conclusions

This study shows that the administration of oxytocin to male humans enhances the encoding of positive social information to make it more memorable. Results suggest that oxytocin could enhance social approach, intimacy, and bonding in male humans by strengthening encoding to make the recall of positive social information more likely.

Section snippets

Methods and Materials

Sixty-nine healthy young adult male students¹ from the University of New South Wales (UNSW; aged 18–30 years, M = 19.98, SD = 2.27) were randomly assigned in a double-blind manner to receive either 24 international units (IU) of OT (n = 35; Novartis, Basel, Switzerland) or a placebo (n = 34). Nasal sprays were developed by a compounding chemist (four puffs per nostril, each with 3 IU), with an identical placebo containing all ingredients except the active OT. Exclusion criteria included

Results

Eight participants were excluded due to equipment malfunction or failure to attend sessions, leaving 31 OT and 30 placebo participants with no age difference [t(59) = .99, p = .33]. t tests and chi-square analysis evaluating differences between drug groups showed there were no differences in positive or negative affect ratings at any session [largest t(59) = –1.58, p = .12], no differences across critical and trustworthiness ratings of faces,² and no differences in the number or type of side

Discussion

This is the first study in humans to show that OT strengthens the encoding of positive social stimuli to make this information more memorable. Participants administered OT at study displayed improved “remember” responding for happy faces and a bias in “know” responding for happy over angry and neutral faces. In support of previous research (12, 13), there was no clear influence of OT on subjective self-reports, such as mood, drug-identification, and face-appraisal ratings. Findings support

References (32)

K. Uvnas-Moberg
Oxytocin may mediate the benefits of positive social interaction and emotions
Psychoneuroendocrinology
(1998)
L.J. Young
The neurobiology of social recognition, approach, and avoidance
Biol Psychiatry
(2002)
M.M. Lim et al.
Neuropeptidergic regulation of affiliative behavior and social bonding in animals
Horm Behav
(2006)
L.F. de Oliveira et al.
Glucocorticoid-mediated effects of systemic oxytocin upon memory retrieval
Neurobiol Learn Mem
(2007)
R.K. Pitman et al.
Effects of intranasal vasopressin and oxytocin on physiologic responding during personal combat imagery in Vietnam veterans with posttraumatic stress disorder
Psychiatry Res
(1993)
J. Bruins et al.
Effect of a single dose of des-glycinamide-[Arg8]vasopressin or oxytocin on cognitive processes in young healthy subjects
Peptides
(1992)
M. Heinrichs et al.
Selective amnesic effects of oxytocin on human memory
Physiol Behav
(2004)
A.J. Guastella et al.
Oxytocin increases gaze to the eye-region of human faces
Biol Psychiatry
(2008)
G. Domes et al.
Oxytocin improves “mind-reading” in humans
Biol Psychiatry
(2007)
A.P. Yonelinas et al.
The relation between remembering and knowing as bases for recognition: Effect of size congruency
J Mem Lang
(1995)

C. Senior

Beauty in the brain of the beholder

Neuron

(2003)

A. Campbell

Attachment, aggression, and affiliation: The role of oxytocin in female social behaviour

Biol Psychol

(2008)

B. Uchino

Social support and health: A review of physiological processes potentially underlying links to disease outcomes

J Behav Med

(2006)

J.A. Bartz et al.

The neuroscience of affiliation: Forging links between basic and clinical research on neuropeptides and social behavior

Horm Behav

(2006)

J.N. Ferguson et al.

Oxytocin in the medial amygdala is essential for social recognition in the mouse

J Neurosci

(2001)

L.J. Young et al.

The neurobiology of pair bonding

Nat Neurosci

(2004)

Cited by (298)

Oxytocin modulates neural activity during early perceptual salience attribution
2024, Psychoneuroendocrinology
Leading hypotheses of oxytocin’s (OT) role in human cognition posit that it enhances salience attribution. However, whether OT exerts its effects predominantly in social (vs non-social) contexts remains debatable, and the time-course of intranasal OT’s effects’ on salience attribution processing is still unknown. We used the social Salience Attribution Task modified (sSAT) in a double-blind, placebo-controlled intranasal OT (inOT) administration, between-subjects design, with 54 male participants, to test existing theories of OT’s role in cognition. Namely, we aimed to test whether inOT would differently affect salience attribution processing of social stimuli (expressing fearfulness) and non-social stimuli (fruits) made relevant via monetary reinforcement, and its neural processing time-course. During electroencephalography (EEG) recording, participants made speeded responses to emotional social (fearful faces) and non-emotional non-social (fruits) stimuli - which were matched for task-relevant motivational salience through their (color-dependent) probability of monetary reinforcement. InOT affected early (rather than late, P3b and LPP) EEG components, increasing N170 amplitude (p = .041) and P2b latency (p .001; albeit not of P1), regardless of stimuli’s (emotional) socialness or reinforcement probability. Fear-related socialness affected salience attribution processing EEG (p .05) across time (N170, P2b and P3b), being later modulated by reinforcement probability (LPP). Our data suggest that OT’s effects on neural activity during early perception, may exist irrespective of fear-related social- or reward-contexts. This partially supports the tri-phasic model of OT (which posits OT enhances salience attribution in an early perception stage regardless of socialness), and not the social salience nor the general approach-withdrawal hypotheses of OT, for early salience processing event-related potentials.
Oxytocin attenuates racial categorization in 14-month-old infants
2023, Infant Behavior and Development
Intergroup bias – the preferential attitudes one holds towards one's social group – is a ubiquitous socio-cognitive phenomenon. In fact, studies show that already in the first months of life, infants manifest a preference for members of their own social group. This points to the possibility of inborn mechanisms involved in social group cognition. Here we assess the effect of a biological activation of infants’ affiliative motivation on their social categorization capacity. In a first visit to the lab, mothers self-administered either Oxytocin (OT) or placebo (PL) via a nasal spray and then engaged in a face-to-face interaction with their 14-month-old infants, a procedure previously shown to increase OT levels in infants. Infants then performed a racial categorization task presented on an eye-tracker. Mothers and infants returned a week later and repeated the procedure while self-administering the complementary substance (i.e., PL or OT, respectively). In total, 24 infants completed the two visits. We found that whereas infants in the PL condition on the first visit exhibited racial categorization, infants in the OT condition in their first visit did not. Moreover, these patterns remained a week later despite the change in substance. Thus, OT inhibited racial categorization when infants first encountered the to-be-categorized faces. These findings highlight the role of affiliative motivation in social categorization, and suggest that the neurobiology of affiliation may provide insights on mechanisms that may be involved in the downstream prejudicial consequences of intergroup bias.
Exogenous estradiol and oxytocin modulate sex differences in hippocampal reactivity during the encoding of episodic memories
2022, NeuroImage
Considerable evidence supports sex differences in episodic memory. The hormones estradiol and oxytocin both affect episodic memory and may contribute to these sex differences, but possible underlying hormonal interactions have not been tested in a sample involving both sexes. To this end, we conducted a randomized, placebo-controlled, parallel-group functional magnetic resonance imaging (fMRI) study including healthy free-cycling women (n = 111) and men (n = 115). The fMRI session was conducted under four experimental conditions: 1. transdermal estradiol (2 mg) and intranasal oxytocin (24 IU), 2. transdermal placebo and intranasal oxytocin, 3. transdermal estradiol and intranasal placebo, 4. transdermal placebo and intranasal placebo. Participants were scanned during the encoding of positive, neutral, and negative scenes. Recognition memory was tested three days following the scanning sessions without additional treatments. Under placebo, women showed a significantly better recognition memory and increased hippocampal responses to subsequently remembered items independent of the emotional valence compared to men. The separate treatments with either hormone significantly diminished this mnemonic sex difference and reversed the hippocampal activation pattern. However, the combined treatments produced no significant effect. Collectively, the results suggest that both hormones play a crucial role in modulating sex differences in episodic memory. Furthermore, possible antagonistic interactions between estradiol and oxytocin could explain previously observed opposing hormonal effects in women and men.
Linking oxytocin and arginine vasopressin signaling abnormalities to social behavior impairments in Prader-Willi syndrome
2022, Neuroscience and Biobehavioral Reviews
Prader-Willi syndrome (PWS) is a genetic neurodevelopmental disorder. Global hypothalamic dysfunction is a core feature of PWS and has been implicated as a driver of many of PWS’s phenotypic characteristics (e.g., hyperphagia-induced obesity, hypogonadism, short stature). Although the two neuropeptides (i.e., oxytocin [OXT] and arginine vasopressin [AVP]) most implicated in mammalian prosocial functioning are of hypothalamic origin, and social functioning is markedly impaired in PWS, there has been little consideration of how dysregulation of these neuropeptide signaling pathways may contribute to PWS’s social behavior impairments. The present article addresses this gap in knowledge by providing a comprehensive review of the preclinical and clinical PWS literature–spanning endogenous neuropeptide measurement to exogenous neuropeptide administration studies–to better understand the roles of OXT and AVP signaling in this population. The preponderance of evidence indicates that OXT and AVP signaling are indeed dysregulated in PWS, and that these neuropeptide pathways may provide promising targets for therapeutic intervention in a patient population that currently lacks a pharmacological strategy for its debilitating social behavior symptoms.
Finding humor in hormones: Oxytocin promotes laughing and smiling
2022, Biological Psychology
Oxytocin (OT) is known for facilitating interpersonal interactions in favorable conditions. Humor, on the other hand, is an interpersonal phenomenon that reduces social distance. In this study, we investigated whether OT would increase laughing and smiling in a favorable environment. Therefore, participants were asked to view a brief video clip of a comedy television program in the presence of an ingroup member after administration of either OT or a placebo. Results demonstrated that participants in the OT condition exhibited more laughing and smiling behavior over the course of viewing the video compared to participants in the placebo condition. OT, however, neither affected self-reported affect nor perceived funniness of the clip. These findings indicate that OT, a hormone that can bolster attachment, also has the power to facilitate implicit social interactions by promoting visible and audible social signals, but does not affect the socially irrelevant inner cheerfulness.
Social partner cooperativeness influences brain oxytocin transcription in Trinidadian guppies (Poecilia reticulata)
2022, Behavioural Brain Research
For non-kin cooperation to be maintained, individuals need to respond adaptively to the cooperative behaviour of their social partners. Currently, however, little is known about the biological responses of individuals to experiencing cooperation. Here, we quantify the neuroregulatory response of Trinidadian guppies (Poecilia reticulata) experiencing cooperation or defection by examining the transcriptional response of the oxytocin gene (oxt; also known as isotocin), which has been implicated in cooperative decision-making. We exposed wild-caught females to social environments where partners either cooperated or defected during predator inspection, or to a control (non-predator inspection) context, and quantified the relative transcription of the oxt gene. We tested an experimental group, originating from a site where individuals are under high predation threat and have previous experience of large aquatic predators (HP), and a control group, where individuals are under low predation threat and naïve to large aquatic predators (LP). LP, but not HP, fish showed different behavioural responses to the behaviour of their social environment, cooperating with cooperative partners and defecting when paired with defecting ones. In HP, but not LP, fish brain mid-section oxt relative transcription varied depending on social partner behaviour. HP fish experiencing cooperation during predator inspection had lower oxt transcription than those experiencing defection. This effect was not present in the control population or in the control context, where the behaviour of social partners did not affect oxt transcription. Our findings provide insight into the neuromodulation underpinning behavioural responses to social experiences, and ultimately to the proximate mechanisms underlying social decision-making.

View all citing articles on Scopus

View full text

Brief ReportOxytocin Enhances the Encoding of Positive Social Memories in Humans

Background

Methods

Results

Conclusions

Section snippets

Methods and Materials

Results

Discussion

Psychoneuroendocrinology

Biol Psychiatry

Horm Behav

Neurobiol Learn Mem

Psychiatry Res

Peptides

Physiol Behav

Biol Psychiatry

Biol Psychiatry

J Mem Lang

Neuron

Biol Psychol

Social support and health: A review of physiological processes potentially underlying links to disease outcomes

J Behav Med

The neuroscience of affiliation: Forging links between basic and clinical research on neuropeptides and social behavior

Horm Behav

Oxytocin in the medial amygdala is essential for social recognition in the mouse

J Neurosci

The neurobiology of pair bonding

Nat Neurosci

Brief Report
Oxytocin Enhances the Encoding of Positive Social Memories in Humans