Oxytocin in the dorsal raphe nucleus antagonizes the inhibition of maternal care induced by food deprivation

Fujisaki, Motoyuki; Nakamura, Ayane; Muroi, Yoshikage; Ishii, Toshiaki

doi:10.1016/j.yhbeh.2020.104773

Cited by 3 publications

(6 citation statements)

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“…OT may also be involved, as plasma levels are increased during chronic social isolation in rodents (Hylin et al, 2022), and in humans OT modulates attention to both positively and negatively valenced social cues (Domes et al, 2007;Gamer et al, 2010). OT neurons also project to dopaminergic neurons in both the VTA (Hung et al, 2017) and, although to a lesser extent, the DR (Otero-García et al, 2016;Fujisaki et al, 2020). Silencing PVN OT neurons in juvenile rats that have been socially isolated for 1 week restores social novelty preference, indicating that overactivation of these neurons during isolation may drive input to DA neurons to increase their activity and alter social behavior (Musardo et al, 2021).…”

Section: Areas Of Mutual Interest For Human and Animal Researchers St...mentioning

confidence: 99%

Neurobiology of Loneliness, Isolation, and Loss: Integrating Human and Animal Perspectives

Vitale

Smith

2022

Front. Behav. Neurosci.

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In social species such as humans, non-human primates, and even many rodent species, social interaction and the maintenance of social bonds are necessary for mental and physical health and wellbeing. In humans, perceived isolation, or loneliness, is not only characterized by physical isolation from peers or loved ones, but also involves negative perceptions about social interactions and connectedness that reinforce the feelings of isolation and anxiety. As a complex behavioral state, it is no surprise that loneliness and isolation are associated with dysfunction within the ventral striatum and the limbic system – brain regions that regulate motivation and stress responsiveness, respectively. Accompanying these neural changes are physiological symptoms such as increased plasma and urinary cortisol levels and an increase in stress responsivity. Although studies using animal models are not perfectly analogous to the uniquely human state of loneliness, studies on the effects of social isolation in animals have observed similar physiological symptoms such as increased corticosterone, the rodent analog to human cortisol, and also display altered motivation, increased stress responsiveness, and dysregulation of the mesocortical dopamine and limbic systems. This review will discuss behavioral and neuropsychological components of loneliness in humans, social isolation in rodent models, and the neurochemical regulators of these behavioral phenotypes with a neuroanatomical focus on the corticostriatal and limbic systems. We will also discuss social loss as a unique form of social isolation, and the consequences of bond disruption on stress-related behavior and neurophysiology.

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Section: Areas Of Mutual Interest For Human and Animal Researchers St...mentioning

confidence: 99%

Neurobiology of Loneliness, Isolation, and Loss: Integrating Human and Animal Perspectives

Vitale

Smith

2022

Front. Behav. Neurosci.

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“…Such a hunger-induced restriction of maternal motivation may be conveyed via neuropeptide-Y + Arc neurons projecting to the dorsal raphe and the MPOA, as suggested. 128,222,223 In this sense, lactation may benefit females by minimizing the energy drain associated with initial vitellogenesis thus offering the female an extended period to terminate her reproductive investment upon deteriorating environmental conditions with minimal energy loss. 195 This may also explain why the parenting-responsible neurons are marked by two G q -coupled receptors that signal satiety, CALCR and BRS3 (Figure 3).…”

Section: Balancing Homeostatic Needs and Maternal Care: Possible Cont...mentioning

confidence: 99%

“…Thus, when food resources are scarce, mothers must reduce the amount of care for more foraging or give up caring for offspring (desertion). Such a hunger‐induced restriction of maternal motivation may be conveyed via neuropeptide‐Y + Arc neurons projecting to the dorsal raphe and the MPOA, as suggested 128,222,223 . In this sense, lactation may benefit females by minimizing the energy drain associated with initial vitellogenesis thus offering the female an extended period to terminate her reproductive investment upon deteriorating environmental conditions with minimal energy loss 195 .…”

Section: Evolutionary Origin Of Mammalian Parental Carementioning

confidence: 99%

“…Morphological evidence suggests that MPOA amylin neurons are innervated by CALCR + neurons, and the local application of amylin activates CALCR + neurons 140 . Thus, MPOA amylin levels can up/downregulate CALCR + neurons to facilitate/suppress parental care depending on the food resource condition (Figure 3C), together with or as a part of the proposed mechanisms involving AGRP/NPY neurons in the Arc 128,222,223 . To prove this possibility, however, future studies should determine if the amylin level in the MPOA reflects hunger/satiety as well as regulates CALCR + neuronal activity in vivo.…”

Section: Evolutionary Origin Of Mammalian Parental Carementioning

confidence: 99%

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Parental brain through time: The origin and development of the neural circuit of mammalian parenting

Kuroda,

Fukumitsu,

Kurachi

et al. 2024

Annals of the New York Academy of Sciences

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This review consolidates current knowledge on mammalian parental care, focusing on its neural mechanisms, evolutionary origins, and derivatives. Neurobiological studies have identified specific neurons in the medial preoptic area as crucial for parental care. Unexpectedly, these neurons are characterized by the expression of molecules signaling satiety, such as calcitonin receptor and BRS3, and overlap with neurons involved in the reproductive behaviors of males but not females. A synthesis of comparative ecology and paleontology suggests an evolutionary scenario for mammalian parental care, possibly stemming from male‐biased guarding of offspring in basal vertebrates. The terrestrial transition of tetrapods led to prolonged egg retention in females and the emergence of amniotes, skewing care toward females. The nocturnal adaptation of Mesozoic mammalian ancestors reinforced maternal care for lactation and thermal regulation via endothermy, potentially introducing metabolic gate control in parenting neurons. The established maternal care may have served as the precursor for paternal and cooperative care in mammals and also fostered the development of group living, which may have further contributed to the emergence of empathy and altruism. These evolution‐informed working hypotheses require empirical validation, yet they offer promising avenues to investigate the neural underpinnings of mammalian social behaviors.

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“…Endothermy facilitates offspring growth but increases maternal and offspring's caloric demand and subsequent foraging demand for the mother. Thus, when food resources are scarce, mothers must reduce the amount of care for the sake of foraging or give up caring for offspring (desertion), possibly via neuropeptide-Y+ Arc neurons projecting to the dorsal raphe and the MPOA 113,215,216 . In this sense, the benefit of lactation for females is minimizing the energy drain associated with initial vitellogenesis and offering the female an extended period to terminate her reproductive investment upon deteriorating environmental conditions with minimal energy loss 178 .…”

Section: -2 Balancing Homostatic Needs and Maternal Care: Possible Co...mentioning

confidence: 99%

Parental Brain Through Time: function, anatomy, and molecular mechanisms in contexts

Kuroda,

Fukumitsu,

Kurachi

et al. 2023

Preprint

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Mammalian parental care is highly mother-biased, prompting researchers to presume its connection to female reproductive behavior and physiology, not male. However, recent findings in neurobiological studies suggest the opposite. Considering the evolutionary path of mammalian parental care, the ancestral form of vertebrate parental care appears to be male-biased as in living teleosts (bony fish), and originated from egg guarding as an extension of territorial behavior. Phylogenetic analyses suggest that in basal tetrapods, the harsh reproductive environments have facilitated terrestrial adaptation and extensive parental investment in females, and salamander-like basal amniotes exhibited extended egg retention in female bodies. Molecular and fossil evidence indicates that synapsids that have later evolved into mammals have already performed extensive maternal care including egg/offspring hydration in the Carboniferous period. Then the nocturnal adaptation in Jurassic mammaliaforms promoted endothermy and prolonged maternal care for thermal control and lactation. This situation may have added nutritional gate control to the offspring care circuit to balance parental provisioning with maternal homeostatic needs. Combining these paleontological, comparative ecological, and neuromolecular findings, we propose that the mammalian parenting circuit may be derived from MPOA neurons controlling reproductive behaviors during the terrestrial adaptation in anamniotes, either by divergent or parallel evolution. Next, we discuss another long-postulated hypothesis that complex affiliative sociality among adults, including group living, cooperative infant care, empathy, and altruism, may have emerged primarily for extended support of the offspring growth, utilizing the established maternal care circuit in mammals. These evolution-informed working hypotheses may also help dissect the neural basis of the complex cognitive functions in mammals.

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Oxytocin in the dorsal raphe nucleus antagonizes the inhibition of maternal care induced by food deprivation

Cited by 3 publications

References 45 publications

Neurobiology of Loneliness, Isolation, and Loss: Integrating Human and Animal Perspectives

Neurobiology of Loneliness, Isolation, and Loss: Integrating Human and Animal Perspectives

Parental brain through time: The origin and development of the neural circuit of mammalian parenting

Parental Brain Through Time: function, anatomy, and molecular mechanisms in contexts

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