Organizational effects of oxytocin on serotonin innervation

Eaton, Jennifer L.; Roache, Laura E.; Nguyen, Khanhbao N.; Cushing, Bruce S.; Troyer, Emily A.; Papademetriou, Eros; Raghanti, Mary Ann

doi:10.1002/dev.20566

Cited by 54 publications

(44 citation statements)

References 41 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…In women, OT increases the VTA activation to salient sexual and infant stimuli (Gregory et al 2015) in nulliparous and postpartum women, respectively. Finally, the raphe magnus shows a specific OT-ir innervation, from which OT can act on serotoninergic neurons (Eaton et al 2012;Mottolese et al 2014) modulating anxiety (Yoshida et al 2009) and aggression (Pagani et al 2015).…”

Section: Distribution Of Ot-immunoreactive Processesmentioning

confidence: 99%

Distribution of oxytocin and co-localization with arginine vasopressin in the brain of mice

et al. 2015

View full text Add to dashboard Cite

Oxytocin (OT) and vasopressin (AVP) play a major role in social behaviours. Mice have become the species of choice for neurobiology of social behaviour due to identification of mouse pheromones and the advantage of genetically modified mice. However, neuroanatomical data on nonapeptidergic systems in mice are fragmentary, especially concerning the central distribution of OT. Therefore, we analyse the immunoreactivity for OT and its neurophysin in the brain of male and female mice (strain CD1). Further, we combine immunofluorescent detection of OT and AVP to locate cells co-expressing both peptides and their putative axonal processes. The results indicate that OT is present in cells of the neurosecretory paraventricular (Pa) and supraoptic hypothalamic nuclei (SON). From the anterior SON, OTergic cells extend into the medial amygdala, where a sparse cell population occupies its ventral anterior and posterior divisions. Co-expression of OT and AVP in these nuclei is rare. Moreover, a remarkable OTergic cell group is found near the ventral bed nucleus of the stria terminalis (BST), distributed between the anterodorsal preoptic nucleus and the nucleus of anterior commissure (ADP/AC). This cell group, the rostral edge of the Pa and the periventricular hypothalamus display frequent OT + AVP double labelling, with a general dominance of OT over AVP immunoreactivity. Fibres with similar immunoreactivity profile innervate the accumbens shell and core, central amygdala and portions of the intervening BST. These data, together with data in the literature on rats, suggest that the projections of ADP/AC nonapeptidergic cells onto these brain centres could promote pup-motivated behaviours and inhibit pup avoidance during motherhood.

show abstract

Section: Distribution Of Ot-immunoreactive Processesmentioning

confidence: 99%

Distribution of oxytocin and co-localization with arginine vasopressin in the brain of mice

et al. 2015

View full text Add to dashboard Cite

show abstract

“…Importantly, in the raphe nuclei, the core area of 5-HT synthesis, serotonergic neurons display OXT receptors and OXT modulates the release of 5-HT (9). Recent results have also shown that administration of OXT during the postnatal period increases the length of serotonergic axons in the hypothalamus and in the amygdala (10). In return, 5-HT is able to modulate OXT release while interacting with different 5-HT receptors in the hypothalamus (11).…”

mentioning

confidence: 89%

Switching brain serotonin with oxytocin

Mottolese

Redouté

Costes

et al. 2014

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

152

View full text Add to dashboard Cite

Serotonin (5-HT) and oxytocin (OXT) are two neuromodulators involved in human affect and sociality and in disorders like depression and autism. We asked whether these chemical messengers interact in the regulation of emotion-based behavior by administering OXT or placebo to 24 healthy subjects and mapping cerebral 5-HT system by using 2′-methoxyphenyl-(N-2′-pyridinyl)-p-[ ]MPPF nondisplaceable binding potential (BP ND ) in the dorsal raphe nucleus (DRN), the core area of 5-HT synthesis, and in the amygdala/hippocampal complex, insula, and orbitofrontal cortex. Importantly, the amygdala appears central in the regulation of 5-HT by OXT: [ 18 F]MPPF BP ND changes in the DRN correlated with changes in right amygdala, which were in turn correlated with changes in hippocampus, insula, subgenual, and orbitofrontal cortex, a circuit implicated in the control of stress, mood, and social behaviors. OXT administration is known to inhibit amygdala activity and results in a decrease of anxiety, whereas high amygdala activity and 5-HT dysregulation have been associated with increased anxiety. The present study reveals a previously unidentified form of interaction between these two systems in the human brain, i.e., the role of OXT in the inhibitory regulation of 5-HT signaling, which could lead to novel therapeutic strategies for mental disorders. B rain chemistry strongly influences our behavior. Among neuromodulators, serotonin (5-HT) and oxytocin (OXT) are important for the regulation and expression of several behaviors such as human affects and socialization. Both systems have been implicated in the control of stress, anxiety, and social cooperation (1, 2). Moreover, their dysfunction is associated with major psychiatric disorders such as depression (3, 4) and autism (5,6). Recent animal studies demonstrated that specific anatomical links exist between these two molecules. Serotonergic fibers originating from the dorsal and medial raphe nuclei of the brainstem project toward magnocellular neurons in the paraventricular and supraoptic nuclei of the hypothalamus, where OXT is released (7). In this region, 5-HT fibers overlap and follow the distribution of OXT cells (8). Importantly, in the raphe nuclei, the core area of 5-HT synthesis, serotonergic neurons display OXT receptors and OXT modulates the release of 5-HT (9). Recent results have also shown that administration of OXT during the postnatal period increases the length of serotonergic axons in the hypothalamus and in the amygdala (10). In return, 5-HT is able to modulate OXT release while interacting with different 5-HT receptors in the hypothalamus (11). Also, the administration of fenfluramine, a serotonergic agonist, to healthy subjects increases plasma OXT level (12). These findings indicate that OXT and 5-HT share anatomical substrates, which may constitute a functional interface in the regulation of emotionbased behaviors. Behaviorally, OXT and 5-HT modulate reactions to social contexts and threatening stimuli in humans and animals (13,14). For instance, oversens...

show abstract

“…The role of dopamine, serotonin, and opioid systems should also be investigated because these neurotransmitters are involved in the rewarding properties of alcohol and other drugs, and play a role in vole social behavior as well, including through interactions with the oxytocin system (59)(60)(61).…”

Section: Discussionmentioning

confidence: 99%

Drinking alcohol has sex-dependent effects on pair bond formation in prairie voles

Anacker

Ahern

Hostetler³

et al. 2014

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

View full text Add to dashboard Cite

Alcohol use and abuse profoundly influences a variety of behaviors, including social interactions. In some cases, it erodes social relationships; in others, it facilitates sociality. Here, we show that voluntary alcohol consumption can inhibit male partner preference (PP) formation (a laboratory proxy for pair bonding) in socially monogamous prairie voles (Microtus ochrogaster). Conversely, female PP is not inhibited, and may be facilitated by alcohol. Behavior and neurochemical analysis suggests that the effects of alcohol on social bonding are mediated by neural mechanisms regulating pair bond formation and not alcohol's effects on mating, locomotor, or aggressive behaviors. Several neuropeptide systems involved in the regulation of social behavior (especially neuropeptide Y and corticotropin-releasing factor) are modulated by alcohol drinking during cohabitation. These findings provide the first evidence to our knowledge that alcohol has a direct impact on the neural systems involved in social bonding in a sexspecific manner, providing an opportunity to explore the mechanisms by which alcohol affects social relationships.anxiety | ethanol | substance use | oxytocin | vasopressin P rairie voles are a valuable animal model of social monogamy. Males and female mates form durable bonds in the wild and in the laboratory (1, 2), and the neural mechanisms of social bonding delineated in this model species have translated with high predictive validity to humans (3, 4). In both species, social reward and drug reward show striking parallels at the behavioral and neurobiological levels (5-9). Prairie voles are now being used to explore the interactions between social relationships and drug abuse (10)(11)(12)(13)(14)(15)(16)(17)(18)(19).We previously demonstrated that prairie voles voluntarily selfadminister substantial amounts of alcohol (ethanol) and can influence the drinking patterns of a social partner (16)(17)(18)(19), similar to social drinking in humans (20). Because alcohol is known to influence social bonds in humans (21-24), we asked here whether alcohol consumption can affect the formation of adult social attachments in prairie voles. Adult male and female prairie voles were paired for 24 h and simultaneously given access to alcohol (10% ethanol by volume in water) and water or only water. They were then tested in the 3-h partner preference (PP) test (PPT), which has proved to be a remarkably sensitive assay for assessing the effects of genetics (25, 26), early social environment (27), and a range of pharmacological agents on social bond formation (28, 29).Results PP was first measured in female prairie voles that drank alcohol during cohabitation without mating. Animals consumed 12.48 ± 1.03 (mean ± SE) grams of alcohol per kilogram of body weight (g/kg) in the 24-h drinking period and showed a 58 ± 5.7% preference for alcohol. Analysis of behavior in the PPT revealed a significant effect of stimulus animal (partner or stranger) on huddling time [F(1,56) = 26.86, P < 0.0001]; no main effect of alcohol on tot...

show abstract

Organizational effects of oxytocin on serotonin innervation

Cited by 54 publications

References 41 publications

Distribution of oxytocin and co-localization with arginine vasopressin in the brain of mice

Distribution of oxytocin and co-localization with arginine vasopressin in the brain of mice

Switching brain serotonin with oxytocin

Drinking alcohol has sex-dependent effects on pair bond formation in prairie voles

Contact Info

Product

Resources

About