Oxytocin and Serotonin Brain Mechanisms in the Nonhuman Primate

Lefèvre, Arthur; Richard, Nathalie; Jazayeri, Mina; Beuriat, Pierre-Aurélien; Fieux, Sylvain; Zimmer, Luc; Duhamel, Jean‐René; Sirigu, Angela

doi:10.1523/jneurosci.0659-17.2017

Cited by 57 publications

(41 citation statements)

References 55 publications

(8 reference statements)

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“…Mottolese and colleagues also found that administering OT, compared to a placebo, increases serotonin binding potential in regions associated with social processing, attention, and valuation in humans: DRN, amygdala/hippocampal complex, insula, and orbitofrontal cortex (Mottolese, Redouté, Costes, Le Bars, & Sirigu, ). This relationship is also present in the macaque brain (Lefevre et al, ). However, the recruitment of 5‐HT by OT seems to be heavily blunted in individuals with Autism Spectrum Disorders, suggesting that the interaction between OT and 5‐HT is crucial for typical social behaviors, including monitoring others (Lefevre et al, ).…”

Section: Introductionmentioning

confidence: 66%

Differences in how macaques monitor others: Does serotonin play a central role?

Weinberg-Wolf

Chang

2019

WIRES Cognitive Science

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Primates must balance the need to monitor other conspecifics to gain social information while not losing other resource opportunities. We consolidate evidence across the fields of primatology, psychology, and neuroscience to examine individual, population, and species differences in how primates, particularly macaques, monitor conspecifics. We particularly consider the role of serotonin in mediating social competency via social attention, aggression, and dominance behaviors. Finally, we consider how the evolution of variation in social tolerance, aggression, and social monitoring might be explained by differences in serotonergic function in macaques.

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Section: Introductionmentioning

confidence: 66%

Differences in how macaques monitor others: Does serotonin play a central role?

Weinberg-Wolf

Chang

2019

WIRES Cognitive Science

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“…Whereas initial data suggests that ATD may reduce peripheral OXT levels in the absence of behavioral effects [80], the combination of ATD with placebo nasal spray did not produce effects on amygdala reactivity in the present study arguing against an ATD-induced unspecific decrease in OXT signaling. On the other hand, molecular imaging studies have demonstrated that intranasal OXT induces central serotonin release [9,23] and ATD leads to stable and selective reductions in central 5-HT signaling [53], including attenuation of stimulated serotonin release [53,81,82] and availability of serotonin in presynaptic neurons [83]. This suggests that pretreatment with ATD diminished OXTinduced serotonin release via OXT-sensitive receptors on serotonergic raphe neurons in which in turn attenuated anxiolytic effects mediated by serotonergic raphe-amygdala pathways.…”

Section: Discussionmentioning

confidence: 99%

“…Overarching conceptualizations of the role of OXT in human social-emotional behavior have proposed that the complex behavioral effects of OXT are partly mediated by interactions with other neurotransmitter systems [5,6]. Such interactions have been evidenced by initial animal models demonstrating that OXT's effects in the domains of pair bonding are partly mediated by dopamine [7] whereas social reward and anxiolytic effects involve interactions with the serotonin (5-HT) system [8][9][10][11]. Previous research in rodents, non-human primates and humans has demonstrated a pivotal role of attenuated amygdala threat reactivity in mediating the anxiolytic actions of both OXT and 5-HT systems [12][13][14][15][16][17].…”

Section: Introductionmentioning

confidence: 99%

“…The functional relevance of the OXT-sensitive receptors was further demonstrated by additional experiments showing that OXT infusion induced raphe 5-HT release and reduction of anxiety-like behavior, whereas pre-treatment with a 5-HT receptor antagonist abolished such anxiolytic effects [11]. More recently, initial studies combined intranasal or intracerebroventricular OXT administration with concomitant in vivo molecular imaging of 5-HT neurotransmission in non -human primates and humans and reported OXTinduced modulations of serotonergic signaling in regions strongly engaged in salience and threat processing, particularly the amygdala and insula, with further analyses suggesting a central role of the amygdala in the oxytocinergic regulation of 5-HT release [9,23].…”

Section: Introductionmentioning

confidence: 99%

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Oxytocinergic modulation of threat-specific amygdala sensitization in humans is critically mediated by serotonergic mechanisms

Liu

Lan

et al. 2020

Preprint

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Overarching conceptualizations propose that the complex social-emotional effects of oxytocin (OXT) in humans are partly mediated by interactions with other neurotransmitter systems.Recent animal models suggest that the anxiolytic effects of OXT are critically mediated by the serotonin (5-HT) system, yet direct evidence in humans is lacking. To determine the role of 5-HT in OXT-induced attenuation of amygdala threat reactivity and sensitization/ desensitization, 121 healthy subjects underwent a transient decrease in 5-HT signaling via acute tryptophan depletion (ATD) before the administration of intranasal OXT or the corresponding placebo-control protocols, respectively. Mean and repetition-dependent changes in threat-specific amygdala reactivity towards threatening stimuli (angry faces) as assessed by fMRI served as the primary outcome. No treatment main or interaction effects on amygdala threat reactivity were observed, yet OXT switched bilateral superficial amygdala sensitization to desensitization and this effect was significantly attenuated during decreased central 5HT signaling via pretreatment with ATD. The present findings provide the first evidence for a role of OXT in threat-specific amygdala desensitization in humans and suggest that these effects are critically mediated by the 5-HT system.

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“…This contrasts with the comparatively large body of medical and psychological literature on the role of serotonin on human mental health (Olivier, ). Interestingly, some recent studies have revealed the existence of an interplay between 5‐HT and OXT, and its role in social behaviour in primates (Baran, ; Lefevre et al ., ). Furthermore, some authors have shown that the administration of a serotonin receptor (HTR1A) agonist inhibits affiliative behaviour directed at the pair‐mate in social monogamous Callicebus cupreus males (Larke et al ., ) and promotes social rejection in female marmosets ( Callithrix jacchus; Aubert et al ., ).…”

Section: Introductionmentioning

confidence: 97%

Serotonin, behavior, and natural selection in New World monkeys

Reales

Paixão‐Côrtes

Cybis

et al. 2018

J of Evolutionary Biology

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Traits that undergo massive natural selection pressure, with multiple events of positive selection, are hard to find. Social behaviour, in social animals, is crucial for survival, and genetic networks involved in behaviour, such as those of serotonin (5-HT) and other neurotransmitters, must be the target of natural selection. Here, we used molecular analyses to search for signals of positive selection in the 5-HT system and found such signals in the M3-M4 intracellular domain of the 5-HT3A serotonin receptor subunit (HTR3A) in primates. We detected four amino acid sites with signs of putatively positive selection (398, 403, 432 and 416); the first three showed indications of being selected in New World monkeys (NWM, Platyrrhini), specifically in the Callitrichinae branch. Additionally, we searched for associations of these amino acid variants with social behavioural traits (i.e. sex-biased dispersal, dominance and social monogamy) using classical and Bayesian methods, and found statistically significant associations for unbiased sex dispersal (398L and 416S), unbiased sex dominance (416S) and social monogamy (416S), as well as significant positive correlation between female dispersal and 403G. Furthermore, we found putatively functional protein motifs determined by three selected sites, of which we highlight a ligand motif to GSK3 in the 416S variant, appearing only in Platyrrhini. 5-HT, 5-HT3A receptor and GSK3 are part of a network that participates in neurodevelopment and regulates behaviour, among other functions. We suggest that these genetic variations, together with those found in other neurotransmitter systems, must contribute to adaptive behaviours and consequently to fitness in NWMs.

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Oxytocin and Serotonin Brain Mechanisms in the Nonhuman Primate

Cited by 57 publications

References 55 publications

Differences in how macaques monitor others: Does serotonin play a central role?

Differences in how macaques monitor others: Does serotonin play a central role?

Oxytocinergic modulation of threat-specific amygdala sensitization in humans is critically mediated by serotonergic mechanisms

Serotonin, behavior, and natural selection in New World monkeys

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