Perception of social interaction compresses subjective duration in an oxytocin-dependent manner.
Ontology highlight
ABSTRACT:
SUBMITTER: Liu R
PROVIDER: S-EPMC5963918 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:Social transmission of fear is not restricted to visual or auditory cues, but extends to the phylogenetically more ancient olfactory domain. Anxious individuals exhibit heightened sensitivity towards chemosensory stress signals in sweat; however, it is still unknown whether endogenous neuromodulators such as the peptide hormone oxytocin (OXT) influence the chemosensory communication of stress. Here, we investigated whether OXT selectively diminishes behavioral and neural responses to social chemosensory stress cues utilizing a randomized, double-blind, placebo (PLC)-controlled, within-subject functional MRI study design. Axillary sweat was obtained from 30 healthy male donors undergoing the Trier Social Stress Test (stress) and bicycle ergometer training (sport). Subsequently, 58 healthy participants (30 females) completed a forced-choice emotional face recognition task with stimuli of varying intensities (neutral to fearful) while they were exposed to both sweat stimuli and a non-social control odor following intranasal OXT or PLC administration, respectively. OXT diminished stress-induced recognition accuracy and response time biases towards fear. On the neural level, OXT reduced stress-evoked responses in the amygdala in both sexes, the anterior cingulate cortex (ACC) in females, and the hippocampus in males. Furthermore, OXT reinstated the functional connectivity between the ACC and the fusiform face area that was disrupted by stress odors under PLC. Our findings reveal a new role for OXT signaling in the modulation of chemosensory communication of stress in humans. Mechanistically, this effect appears to be rooted in a downregulation of stress-induced limbic activations and concomitant strengthening of top-down control descending from the ACC to the fusiform face area.
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Project description:Human-human social touch improves mood and alleviates pain. No studies have so far tested the effect of human-robot emotional touch on experimentally induced pain ratings, on mood and on oxytocin levels in healthy young adults. Here, we assessed the effect of touching the robot PARO on pain perception, on mood and on salivary oxytocin levels, in 83 young adults. We measured their perceived pain, happiness state, and salivary oxytocin. For the 63 participants in the PARO group, pain was assessed in three conditions: Baseline, Touch (touching PARO) and No-Touch (PARO present). The control group (20 participants) underwent the same measurements without ever encountering PARO. There was a decrease in pain ratings and in oxytocin levels and an increase in happiness ratings compared to baseline only in the PARO group. The Touch condition yielded a larger decrease in pain ratings compared to No-Touch. These effects correlated with the participants' positive perceptions of the interaction with PARO. Participants with higher perceived ability to communicate with PARO experienced a greater hypoalgesic effect when touching PARO. We show that human-robot social touch is effective in reducing pain ratings, improving mood and - surprisingly - reducing salivary oxytocin levels in adults.
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Project description:BACKGROUND:Oxytocin, classically involved in social and reproductive activities, is increasingly recognized as an antinociceptive and anxiolytic agent, effects which may be mediated via oxytocin's interactions with the dopamine system. Thus, genetic variation within the oxytocin gene (OXT) is likely to explain variability in dopamine-related stress responses. As such, we examined how OXT variation is associated with stress-induced dopaminergic neurotransmission in a healthy human sample. METHODS:Fifty-five young healthy volunteers were scanned using [¹¹C]raclopride positron emission tomography while they underwent a standardized physical and emotional stressor that consisted of moderate levels of experimental sustained deep muscle pain, and a baseline, control state. Four haplotype tagging single nucleotide polymorphisms located in regions near OXT were genotyped. Measures of pain, affect, anxiety, well-being and interpersonal attachment were also assessed. RESULTS:Female rs4813625 C allele carriers demonstrated greater stress-induced dopamine release, measured as reductions in receptor availability from baseline to the pain-stress condition relative to female GG homozygotes. No significant differences were detected among males. We also observed that female rs4813625 C allele carriers exhibited higher attachment anxiety, higher trait anxiety and lower emotional well-being scores. In addition, greater stress-induced dopamine release was associated with lower emotional well-being scores in female rs4813625 C allele carriers. CONCLUSIONS:Our results suggest that variability within the oxytocin gene appear to explain interindividual differences in dopaminergic responses to stress, which are shown to be associated with anxiety traits, including those linked to attachment style, as well as emotional well-being in women.
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Project description:There has been accumulating evidence of human social chemo-signaling, but the underlying mechanisms remain poorly understood. Considering the evolutionarily conserved roles of oxytocin and vasopressin in reproductive and social behaviors, we examined whether the two neuropeptides are involved in the subconscious processing of androsta-4,16,-dien-3-one and estra-1,3,5 (10),16-tetraen-3-ol, two human chemosignals that convey masculinity and femininity to the targeted recipients, respectively. Psychophysical data collected from 216 heterosexual and homosexual men across five experiments totaling 1056 testing sessions consistently showed that such chemosensory communications of masculinity and femininity were blocked by a competitive antagonist of both oxytocin and vasopressin receptors called atosiban, administered nasally. On the other hand, intranasal oxytocin, but not vasopressin, modulated the decoding of androstadienone and estratetraenol in manners that were dose-dependent, nonmonotonic, and contingent upon the recipients' social proficiency. Taken together, these findings establish a causal link between neuroendocrine factors and subconscious chemosensory communications of sex-specific information in humans.
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Project description:Oxytocin (OT) modulates social behavior in primates and many other vertebrate species. Studies in non-primate animals have demonstrated that, in addition to influencing activity within individual brain areas, OT influences functional connectivity across networks of areas involved in social behavior. Previously, we used fMRI to image brain function in human subjects during a dyadic social interaction task following administration of either intranasal oxytocin (INOT) or placebo, and analyzed the data with a standard general linear model. Here, we conduct an extensive re-analysis of these data to explore how OT modulates functional connectivity across a neural network that animal studies implicate in social behavior. OT induced widespread increases in functional connectivity in response to positive social interactions among men and widespread decreases in functional connectivity in response to negative social interactions among women. Nucleus basalis of Meynert, an important regulator of selective attention and motivation with a particularly high density of OT receptors, had the largest number of OT-modulated connections. Regions known to receive mesolimbic dopamine projections such as the nucleus accumbens and lateral septum were also hubs for OT effects on functional connectivity. Our results suggest that the neural mechanism by which OT influences primate social cognition may include changes in patterns of activity across neural networks that regulate social behavior in other animals.
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Project description:Oxytocin (OT) has become a focus in investigations of autism spectrum disorder (ASD). The social deficits that characterize ASD may relate to reduced connectivity between brain sites on the mesolimbic reward pathway (nucleus accumbens; amygdala) that receive OT projections and contribute to social motivation, and cortical sites involved in social perception. Using functional magnetic resonance imaging and a randomized, double blind, placebo-controlled crossover design, we show that OT administration in ASD increases activity in brain regions important for perceiving social-emotional information. Further, OT enhances connectivity between nodes of the brain's reward and socioemotional processing systems, and does so preferentially for social (versus nonsocial) stimuli. This effect is observed both while viewing coherent versus scrambled biological motion, and while listening to happy versus angry voices. Our findings suggest a mechanism by which intranasal OT may bolster social motivation-one that could, in future, be harnessed to augment behavioral treatments for ASD.
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Project description:People are eager to know the self in other's eyes even with personal costs. However, what drives people costly to know evaluations remains unknown. Here we tested the hypothesis of placing subjective value on knowing social evaluations. To quantify the subjective value, we developed a pay-to-know choice task where individuals trade off profits against knowing social evaluations. Individuals computed independent unknown aversion towards positive and negative social evaluations and placed higher values on knowing social evaluation on positive than negative aspects. Such a valence-dependent valuation of social evaluation was facilitated by oxytocin, a neuropeptide linked to feedback learning and valuation processes, by decreasing values of negative social evaluation. Moreover, individuals scoring high in depression undervalued positive social evaluation, which was normalized by oxytocin. We reveal the psychological and computational processes underlying self-image formation/update and suggest a role of oxytocin in normalizing hypo-valuation of positive social evaluation in depression.
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Project description:Parental care and sensory stimulation are critical environmental factors that influence oxytocin (OXT) and its receptor (OXTR). Because developmental Oxt mRNA expression is enhanced by sensory-rich early life experience and reduced by sensory deprivation, we predicted that compared to wild-type (WT) littermates, mice with congenital loss of OXTR (OXTR KO), as a genetically induced deprivation, would show impaired Oxt mRNA expression in the offspring hypothalamus during development. Oxt mRNA levels of male and female OXTR KO mice were not different from WT littermates from postnatal day (P)0 to P6, although, by P8, OXTR KO showed significantly decreased Oxt mRNA expression in the hypothalamus compared to WT littermates. At P14, male and female OXTR KO mice had significantly decreased Oxt mRNA expression specifically in the paraventricular nucleus (PVN), but not the supraoptic nucleus (SON), compared to WT littermates. We investigated whether this effect persisted in adulthood (P90) and found a significant genotype by sex interaction where male OXTR KO mice displayed a reduction in Oxt expression specific to the PVN compared to male WT littermates. By contrast, male and female OXTR KO adults had increased Oxt mRNA levels in the SON. These findings suggest that OXTR plays a role in developmental Oxt mRNA expression with sex by genotype interactions apparent at adulthood. We then measured OXT and neural activation in the PVN and SON at P14. We observed more OXT-immunoreactive cells in the PVN of OXTR KO mice but significantly fewer c-Fos immunoreactive cells. There were no genotype differences in immunoreactivity for OXT and no c-Fos activity in the SON at P14. Combined, these data suggest that OXTR WT P14 mice have more PVN activity and are more likely to release OXT than OXTR KO mice. Future experiments are warranted to understand which OXTR-expressing neural circuits modulate the development of the PVN oxytocin system.
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Project description:Alzheimer's disease (AD)-the most common cause of dementia in the elderly-is characterized by progressive memory loss and β-amyloid protein (Aβ) accumulation in the brain. Recently, loneliness was found to be a high risk factor for AD, and social isolation has become a major cause of AD. AD. Oxytocin (OXT), the main hormone involved in social bonding, has been implicated in social interactions, notably in building trust and relationships. Moreover, social isolation or social enrichment modulates the activation of neurons related to OXT. Recently, we reported that OXT reverses learning and memory impairment in AD animal models. Based on the limited number of studies currently available, OXT might be a therapeutic target for AD. Further studies are necessary in order to better understand the role of oxytocin in AD. In this review, we described the relationships between OXT, AD, and social interaction.
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