Evolution of oxytocin pathways in the brain of vertebrates

Knobloch, Hilda; Grinevich, Valery

doi:10.3389/fnbeh.2014.00031

Cited by 214 publications

(194 citation statements)

References 154 publications

(209 reference statements)

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“…Our results parallel neuropharmacological research showing elevated OT levels in the extracellular fluid within the septum and dorsal hippocampus of rodents after intranasal administration, which was accompanied by a sharp rise in plasma OT (37). Activation of OT neurons, which project simultaneously to the posterior pituitary and forebrain regions (38,39), can induce peripheral and central OT release and exert direct effects both at the cellular and behavioral level (40). Taken all together, the results of the present study suggest that OT can penetrate into the central nervous system in dogs when administered intranasally.…”

Section: Discussionsupporting

confidence: 87%

Oxytocin promotes social bonding in dogs

Romero

Nagasawa

Mogi

et al. 2014

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

199

172

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Recent evidence suggests that enduring social bonds have fitness benefits. However, very little is known about the neural circuitry and neurochemistry underlying the formation and maintenance of stable social bonds outside reproductive contexts. Oxytocin (OT), a neuropeptide synthetized by the hypothalamus in mammals, regulates many complex forms of social behavior and cognition in both human and nonhuman animals. Animal research, however, has concentrated on monogamous mammals, and it remains unknown whether OT also modulates social bonds in nonreproductive contexts. In this study we provide behavioral evidence that exogenous OT promotes positive social behaviors in the domestic dog toward not only conspecifics but also human partners. Specifically, when sprayed with OT, dogs showed higher social orientation and affiliation toward their owners and higher affiliation and approach behaviors toward dog partners than when sprayed with placebo. Additionally, the exchange of sociopositive behaviors with dog partners triggered the release of endogenous OT, highlighting the involvement of OT in the development of social relationships in the domestic dog. These data provide new insight into the mechanisms that facilitate the maintenance of close social bonds beyond immediate reproductive interest or genetic ties and complement a growing body of evidence that identifies OT as one of the neurochemical foundations of sociality in mammalian species.cooperative bonds | cooperative mechanisms A ccording to behavioral ecology theory, sociability evolved either to reduce individuals' risk from predation or to increase individuals' ability to find and defend food (1). New evidence from a range of mammalian species, however, shows that competitive success and reproductive performance of social individuals are affected by the nature and quality of the social bonds they form, suggesting that sociability is adaptive in its own right (2, 3). The impact of social bonds on individuals' fitness extends beyond the benefits derived from associations directly related to mating and parental care (4). For example, in baboons (Papio hamadryas ursinus) (2, 3), house mice (Mus musculus) (5), rats (Rattus norvegicus) (6), horses (Equus equus) (7), and bottlenose dolphins (Tursiops truncatus) (8), individuals that maintain strong, enduring same-sex bonds experience a higher longevity or offspring survival than individuals with weaker bonds. These data parallel evidence from human studies that show that the quality and quantity of individuals' social relationships is associated not only with better mental health but also with reduced mortality (9).Beside the above-mentioned fitness benefits of social integration, very little is known about the neural circuitry and neurochemistry underlying the formation and maintenance of social bonds outside reproductive contexts. Although it is likely that brain systems that motivate animals to establish individualized relationships with other group members first evolved to mobilize the maternal care necessary f...

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Section: Discussionsupporting

confidence: 87%

Oxytocin promotes social bonding in dogs

Romero

Nagasawa

Mogi

et al. 2014

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

199

172

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“…However, oxytocin is synthesized and released into the peripheral circulation not only in females but also in males. Furthermore, oxytocin is an evolutionarily conserved peptide, and oxytocin or its homologs are expressed not only in mammals but also in non-mammal vertebrates including agnathans, fishes and amphibians [18,37]. Some kinds of insects, snails and nematodes also express oxytocin homologs.…”

Section: Introductionmentioning

confidence: 99%

“…Oxytocin is also synthesized in neurons located in the parvocellular region of the paraventricular nucleus of the hypothalamus or in the bed nucleus of stria terminals. These oxytocin neurons project to other brain regions [36,37,49].…”

Section: Introductionmentioning

confidence: 99%

Noxious or Non-noxious Inputs to Oxytocin Neurons: Possible Roles in the Control of Behaviors

Onaka

Okabe

Takayanagi

et al. 2015

IIS

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Oxytocin plays an essential role in milk ejection and parturition in mammals. Oxytocin has also been shown to be involved in the control of various behaviors, including anxiety-related behaviors, food intake and affiliative behaviors.We previously showed that noxious stimuli or stimuli previously paired with noxious stimuli (conditioned fear stimuli) activate hypothalamic oxytocin neurons via activation of brainstem catecholaminergic/prolactin-releasing peptide (PrRP)-positive neurons. Oxytocin neurons are activated not only by noxious stimuli but also by nonnoxious touch stimuli. Social contact has been suggested to activate oxytocin neurons. Non-noxious tactile stimuli induce 50-kHz ultrasonic vocalization, an index of positive states in rats, and activate hypothalamic oxytocin neurons, suggesting that pleasant tactile stimuli activate oxytocin neurons.Physiological roles of oxytocin released during noxious or non-noxious tactile stimuli remain to be clarified. Noxious stimuli increase anxiety-related behavior, while pleasant sensory stimuli have pro-social actions. We have shown that endogenous oxytocin reduces anxiety-related behaviors, induces a decrease in amounts of food intake per meal, and facilitates social recognition via distinct neural pathways. Roles of oxytocin released during sensory stimuli may be dependent upon the sensory stimuli used, and oxytocin may contribute to the prevention of overreactions to noxious stimuli or mediate pro-social or anxiolytic actions of pleasant tactile stimuli.

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“…Evolutionary theory suggests that secretion of these peptides in the cerebrospinal fluid has been replaced by a vascular secretion. In advanced vertebrates, the axonal projections of these neurons are toward the PP and also to forebrain, telencephalon and diencephalon regions, probably explaining the behavioral effects of oxytocin [3] and vasopressin (VP) [2] .Tonicity is perceived specifically by neuronal groups on the anterior wall of the third cerebral ventricle ( fig. 1 ).…”

mentioning

confidence: 99%

“…Large neurosecretory magnocellular cells of 20-40 μm and smaller parvocellular cells of 10-15 μm are neuroendocrine, autonomic and circadian controllers and regulators. Oxytocin and arginine vasopressin (AVP) are synthesized in different populations of magnocellular neurons from the supraoptic, paraventricular and accessory nuclei [2] . Evolutionary theory suggests that secretion of these peptides in the cerebrospinal fluid has been replaced by a vascular secretion.…”

mentioning

confidence: 99%

Vasopressin at Central Levels and Consequences of Dehydration

Bichet

2016

Ann Nutr Metab

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Disorders of water balance are a common feature of clinical practice. An understanding of the physiology and pathophysiology of central vasopressin release and perception of thirst is the key to diagnosis and management of these disorders. Mammals are osmoregulators; they have evolved mechanisms that maintain extracellular fluid osmolality near a stable value, and, in animal studies, osmoregulatory neurons express a truncated delta-N variant of the transient receptor potential vannilloid (TRPV1) channel involved in hypertonicity and thermal perception while systemic hypotonicity might be perceived by TRPV4 channels. Recent cellular and optogenetic animal experiments demonstrate that, in addition to the multifactorial process of excretion, circumventricular organ sensors reacting to osmotic pressure and angiotensin II, subserve genesis of thirst, volume regulation and behavioral effects of thirst avoidance.

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Evolution of oxytocin pathways in the brain of vertebrates

Cited by 214 publications

References 154 publications

Oxytocin promotes social bonding in dogs

Oxytocin promotes social bonding in dogs

Noxious or Non-noxious Inputs to Oxytocin Neurons: Possible Roles in the Control of Behaviors

Vasopressin at Central Levels and Consequences of Dehydration

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