Oxytocin Mediates Entrainment of Sensory Stimuli to Social Cues of Opposing Valence

Choe, Han Kyoung; Reed, Michael D.; Benavidez, Nora L.; Montgomery, Daniel P.; Soares, Natalie; Yim, Yeong Shin; Choi, Gloria B.

doi:10.1016/j.neuron.2015.06.022

Cited by 112 publications

(108 citation statements)

References 58 publications

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“…By contrast, positive BUs reflected pessimistic updating. A one-sample test revealed that the mean BU was significantly smaller than 0 [study 1: BU = −1.76, t(1,97) = 2.98, P = 0.004; study 2: BU = −1.37, t(1,94) = 2.80, P = 0.006], indicating reliable optimistic updating across OT and PL groups and replicating previous findings (21,22). More importantly, an independent-samples t test showed that optimistic updating was greater in IN-OT (vs. PL) group [study 1: t (96) = 2.72, P = 0.008; study 2: t(93) = 2.08, P = 0.041; SI Appendix, Table S1], and this result was also replicated in study 3 [t(112) = 2.76, P = 0.007, SI Appendix, Table S1 and Fig.…”

Section: Resultssupporting

confidence: 78%

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Distinct oxytocin effects on belief updating in response to desirable and undesirable feedback

Wang

et al. 2016

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

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Humans update their beliefs upon feedback and, accordingly, modify their behaviors to adapt to the complex, changing social environment. However, people tend to incorporate desirable (better than expected) feedback into their beliefs but to discount undesirable (worse than expected) feedback. Such optimistic updating has evolved as an advantageous mechanism for social adaptation. Here, we examine the role of oxytocin (OT)-an evolutionary ancient neuropeptide pivotal for social adaptation-in belief updating upon desirable and undesirable feedback in three studies (n = 320). Using a double-blind, placebo-controlled between-subjects design, we show that intranasally administered OT (IN-OT) augments optimistic belief updating by facilitating updates of desirable feedback but impairing updates of undesirable feedback. The IN-OT-induced impairment in belief updating upon undesirable feedback is more salient in individuals with high, rather than with low, depression or anxiety traits. IN-OT selectively enhances learning rate (the strength of association between estimation error and subsequent update) of desirable feedback. IN-OT also increases participants' confidence in their estimates after receiving desirable but not undesirable feedback, and the OT effect on confidence updating upon desirable feedback mediates the effect of IN-OT on optimistic belief updating. Our findings reveal distinct functional roles of OT in updating the first-order estimation and second-order confidence judgment in response to desirable and undesirable feedback, suggesting a molecular substrate for optimistic belief updating.oxytocin | social adaptation | confidence | belief updating | optimism

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Section: Resultssupporting

confidence: 78%

“…The oxytocinergic system has been implicated in social learning and optimism. Animal research has shown evidence for a key role of the oxytocinergic system in mediating appetitive and aversive learning in mice (22). Human studies have linked optimism with OT receptor gene function (OXTR; ref.…”

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confidence: 99%

Distinct oxytocin effects on belief updating in response to desirable and undesirable feedback

Wang

et al. 2016

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

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“…Indeed, OT has been shown to increase spike output 89-91 and facilitate synaptic long-term potentiation 92-94 and our data suggest an intrinsic mechanism that may underlie shifts in synaptic efficacy and excitatory/inhibitory balance found in brain regions where OT is critical for myriad social behaviors 67,74,90,95 . Intrinsic properties are shaped by ion channels.…”

Section: Discussionmentioning

confidence: 70%

“…11); this is a measure of the degree to which nodes correlate with multiple modules and has been argued to be an appropriate measure of "hubness" for correlation-based networks 73 . Agranular insular (AI) cortex was among the nodes with the highest participation coefficients along with prelimbic prefrontal cortex (PL), piriform cortex (Pir) and dorsal bed nucleus (BSTd), regions that are associated with emotion contagion 52 , social learning 74 and social decision-making 6 , respectively. Thus, datadriven network analyses revealed functional integration among regions in the social brain, and that the insula is positioned to interact with previously identified nodes important for social and affective behaviors.…”

Section: Insular Cortex and The Social Decision-making Networkmentioning

confidence: 99%

Insular Cortex Mediates Approach and Avoidance Responses to Social Affective Stimuli

Rogers

Varela

Gribbons

et al. 2017

Preprint

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Social animals detect the affective states of others and utilize this information to orchestrate appropriate social interactions. Social affective behaviors include cooperation, reproductive acts and avoiding sick individuals. In a social affective behavioral test in which experimental adult male rats were given the choice to interact with either naive or stressed conspecifics, the experimental rats demonstrated both approach and avoidant behaviors towards the conspecific, depending upon the age of the conspecific; experimental adult rats approached the stressed juvenile but avoided the stressed adult. Optogenetic inhibition of the insular cortex, a region anatomically positioned to contribute to social cognition, disrupted these behaviors. Receptors for the social nonapeptide oxytocin (OT) are found in high density within the insular cortex and here oxytocin increased intrinsic excitability and synaptic efficacy in acute insular cortex slices. Blockade of oxytocin receptors (OTRs) in the insula eliminated the effect of conspecific stress on approach behavior, while insular administration of OT recapitulated the behaviors typically observed in response to stressed conspecifics. Network analysis using Fos immunoreactivity identified functional connectivity between the insular cortex and the network of regions involved in social decision making. These results implicate insular cortex as a novel target of OT and suggest that insula is a key component in the circuit underlying age-dependent social responses to stressed conspecifics.Social animals, including humans, have an enormous repertoire of behavioral expressions that provide for the transmission of one's affective state to other members of the group 1-3 . Sensory and perceptive systems in the "social decision-making network" (SDMN) which consists of the social brain network 4 and the mesolimbic reward system 5 allow one to appraise these social stimuli and integrate them with past experiences, situational, and somatic factors to shape specific behavioral responses 6 . In addition to the SDMN, growing evidence implicates insular cortex in responding to socioemotional stimuli in humans. When tasked to identify the emotion of another from a facial expression, or to observe another suffer a painful stimulation, a reliable neural correlate is relative increase in the blood oxygen level dependent (BOLD) signal in the insular cortex 7,8 . Accordingly, emotion recognition and empathic deficits have been reported among individuals with insular cortex lesions [9][10][11][12] . Empathic processes are also disrupted in autism spectrum 1 Department of Psychology, Boston College, Chestnut Hill, MA 02467, USA 2 These authors made equal contributions to this work. *Corresponding Author: John P. Christianson, Department of Psychology, Boston College, 140 Commonwealth Avenue, Chestnut Hill, MA 02467 USA, Email: j.christianson@bc.edu, Phone: +1-617-552-3970.A note about the preprint. This manuscript was submitted to bioRxiv.org after multiple rounds of peer review. The manuscrip...

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“…Furthermore, the POC and higher areas send information back to the OB as well 26 . Among these many neuron pathways and back projections, POC-derived synaptic output to hypothalamus and medial-orbito-frontal cortices have been known to enhance odor-driven social stimuli in appetitive and aversive behaviors 27 .…”

mentioning

confidence: 99%

The Hitchhiker’s guide to the rhinencephalon

Silveira‐Moriyama

Glass

Rajan

et al. 2016

Arq. Neuro-Psiquiatr.

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Pathology of the rhinencephalon has been a subject of interest in the fields of neurodegenerative diseases, trauma, epilepsy and other neurological conditions. Most of what is known about the human rhinencephalon comes from comparative anatomy studies in other mammals and histological studies in primates. Functional imaging studies can provide new and important insight into the function of the rhinencephalon in humans but have limited spatial resolution, limiting its contribution to the study of the anatomy of the human rhinencephalon. In this study we aim to provide a brief and objective review of the anatomy of this important and often overlooked area of the nervous system.

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Oxytocin Mediates Entrainment of Sensory Stimuli to Social Cues of Opposing Valence

Cited by 112 publications

References 58 publications

Distinct oxytocin effects on belief updating in response to desirable and undesirable feedback

Distinct oxytocin effects on belief updating in response to desirable and undesirable feedback

Insular Cortex Mediates Approach and Avoidance Responses to Social Affective Stimuli

The Hitchhiker’s guide to the rhinencephalon

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