Oxytocin enhances the pain‐relieving effects of social support in romantic couples

Kreuder, Ann-Kathrin; Wassermann, Lea; Wollseifer, Michael; Ditzen, Beate; Eckstein, Monika; Stoffel‐Wagner, Birgit; Hennig, Juergen; Hurlemann, René; Scheele, Dirk

doi:10.1002/hbm.24368

Cited by 49 publications

(45 citation statements)

References 65 publications

(113 reference statements)

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“…Importantly, OXT selectively strengthened fear-related functional interplay between the cmA and the dmPFC. The blA is highly connected with the PFC (17), and OXT-induced increased functional connectivity between the amygdala and PFC may reflect an enhanced top-down cognitive control that has previously been observed in the context of social pain modulation (38). Moreover, patients with anxiety disorders exhibit decreased functional connectivity between the CeA and PFC (39), supporting the idea of amygdala hyperactivity (5) and PFC hypoactivity (40) as a neural endophenotype of anxiety disorders.…”

Section: Discussionmentioning

confidence: 62%

“…Consistent with previous imaging studies investigating the effects of OXT on emotional face processing (10)(11)(12)(13)15), our study did not reveal any modulatory effects of intranasal OXT on reaction times during the fMRI task or any change in accuracy ratings (SI Appendix, Results). While ceiling effects in the behavioral data may have hindered the detection of OXT-ergic modulation in the present study, behavioral OXT effects have previously been reported in reaction to more complex social stimuli related to pair-bonding or attachment (38,(48)(49)(50)(51). Importantly, the emotional face-matching task in our study was primarily designed not to produce sensitive behavioral markers for emotional face processing, but rather to evoke robust and reliable amygdala activation.…”

Section: Discussionmentioning

confidence: 82%

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Common and dissociable effects of oxytocin and lorazepam on the neurocircuitry of fear

Kreuder

Scheele

Schultz

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Benzodiazepines (BZDs) represent the gold standard of anxiolytic pharmacotherapy; however, their clinical benefit is limited by side effects and addictive potential. Consequently, there is an urgent need to develop novel and safe anxiolytics. The peptide hormone oxytocin (OXT) exhibits anxiolytic-like properties in animals and humans, but whether OXT and BZDs share similar effects on the neural circuitry of fear is unclear. Therefore, the rationale of this ultra-high-field functional MRI (fMRI) study was to test OXT against the clinical comparator lorazepam (LZP) with regard to their neuromodulatory effects on local and network responses to fear-related stimuli. One hundred twenty-eight healthy male participants volunteered in this randomized double-blind, placebo-controlled, between-group study. Before scanning using an emotional face-matching paradigm, participants were randomly administered a single dose of OXT (24 IU), LZP (1 mg), or placebo. On the behavioral level, LZP, but not OXT, caused mild sedation, as evidenced by a 19% increase in reaction times. On the neural level, both OXT and LZP inhibited responses to fearful faces vs. neutral faces within the centromedial amygdala (cmA). In contrast, they had different effects on intra-amygdalar connectivity; OXT strengthened the coupling between the cmA and basolateral amygdala, whereas LZP increased the interplay between the cmA and superficial amygdala. Furthermore, OXT, but not LZP, enhanced the coupling between the cmA and the precuneus and dorsomedial prefrontal cortex. These data implicate inhibition of the cmA as a common denominator of anxiolytic action, with only OXT inducing large-scale connectivity changes of potential therapeutic relevance.

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Section: Discussionmentioning

confidence: 62%

Section: Discussionmentioning

confidence: 82%

Common and dissociable effects of oxytocin and lorazepam on the neurocircuitry of fear

Kreuder

Scheele

Schultz

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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“…As such, it can be speculated that different intertwined mechanisms modulate our perception of reality: in a given context of close proximity and social touch, the release of OXT may decrease self-centeredness (Zhao et al, 2016) and foster feelings of closeness, eventually facilitating trust (Kosfeld et al, 2005) and bonding (Scheele et al, 2013;Kreuder et al, 2017Kreuder et al, , 2019, thereby promoting a socially biased perception. If a context is ambiguous or even dangerous, an intact amygdala seems to counteract these processes by sustaining a clear self-perception and protecting us against maladaptive loss of reality.…”

Section: Discussionmentioning

confidence: 99%

A Protective Mechanism against Illusory Perceptions Is Amygdala-Dependent

et al. 2019

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Most people have a clear sense of body ownership, preserving them from physical harm. However, perceptual body illusions -famously the rubber hand illusion (RHI) -can be elicited experimentally in healthy individuals. We hypothesize that the amygdala, a core component of neural circuits of threat processing, is involved in protective mechanisms against disturbed body perceptions. To test this hypothesis, we started by investigating two monozygotic human twin sisters with focal bilateral amygdala damage due to Urbach-Wiethe disease. Relative to 20 healthy women, the twins exhibited, on two occasions 1 year apart, augmented RHI responses in form of faster illusion onset and increased vividness ratings. Following up on these findings, we conducted a volumetric brain morphometry study involving an independent, gender-mixed sample of 57 healthy human volunteers (36 female, 21 male). Our results revealed a positive correlation between amygdala volume and RHI onset, i.e., the smaller the amygdala, the less time it took the RHI to emerge. This raised the question of whether a similar phenotype would result from experimental amygdala inhibition. To dampen amygdala reactivity, we intranasally administered the peptide hormone oxytocin to the same 57 individuals in a randomized trial before conducting the RHI. Compared with placebo, oxytocin treatment yielded enhanced RHI responses, again evident in accelerated illusion onset and increased vividness ratings. Together, the present series of experiments provides converging evidence for the amygdala's unprecedented role in reducing susceptibility to the RHI, thus protecting the organism from the potentially fatal threats of a distorted bodily self. Significance StatementCompelling evidence indicates that the amygdala is of vital importance for danger detection and fear processing. However, lethal threats can arise not only from menacing external stimuli but also from distortions in bodily self-perception. Intriguingly, the amygdala's modulatory role in such illusory body perceptions is still elusive. To probe the amygdala's involvement in illusory body experiences, we conducted a multi-methodological series of experiments in a rare human amygdala lesion model, complemented by a morphological and pharmaco-modulatory experiment in healthy volunteers. Our findings convergently suggest that the amygdala's integrity is indispensable for maintaining an unbiased, precise perception of our bodily self. Hence, the amygdala might shield us against distortions in self-perception and the resultant loss of behavioral control of our organism.

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“…15 The latter finding was also confirmed in both a healthy pain-free sample 14 and fibromyalgia patients. 45 Notably, while recent data suggest an interaction effect of intranasal OT and social support on pain perception in a laboratory study in women, 19 most studies on this topic to date have been done in men. Thus, while lower pain levels to OT in men 46 are in concurrence with previous studies, there is limited data available only to help interpret our results in women and no single study on repeated OT administration in this context has been published yet.…”

Section: Discussionmentioning

confidence: 99%

Oxytocin and positive couple interaction affect the perception of wound pain in everyday life

et al. 2020

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A large body of animal and human laboratory research has linked social interaction and support to pain perception, with a possible role for the neuropeptide oxytocin as a neuroendocrine mediator. However so far, it has been unclear whether these effects translate to ecologically valid everyday life behavior and pain perception. In a randomized placebo-controlled study, a standard suction blister skin wound was induced to N = 80 romantic couples (N = 160 individuals). Couples then received intranasal oxytocin or placebo twice daily and were either instructed to perform a positive social interaction (partner appraisal task, PAT) once in the laboratory and two times during the following five days, or not. During these days, all participants reported their subjective pain levels multiple times a day using ecologically momentary assessment. Results from hierarchical linear modeling suggest that pain levels within the couples were inter-related. In men, but not in women, oxytocin reduced pain levels. Women reported lower pain levels in the group of positive social interaction, while this effect did not show in men. These results suggest that intranasal oxytocin might have sex-specific effects with pain reducing effects in men but the opposite effects in women. In contrast, especially women benefit from positive interaction in terms of dampened pain levels after positive interaction. The results add to the evidence for health-beneficial effects of positive couple interaction and point to underlying neuroendocrine mechanisms in everyday life pain specifically. The sex-specific effects, in particular, may have implications for psychopharmacological treatment of pain in men and women.

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Oxytocin enhances the pain‐relieving effects of social support in romantic couples

Cited by 49 publications

References 65 publications

Common and dissociable effects of oxytocin and lorazepam on the neurocircuitry of fear

Common and dissociable effects of oxytocin and lorazepam on the neurocircuitry of fear

A Protective Mechanism against Illusory Perceptions Is Amygdala-Dependent

Oxytocin and positive couple interaction affect the perception of wound pain in everyday life

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