Single transcript level atlas of oxytocin and the oxytocin receptor in the mouse brain

Oxytocin (OXT), a neuropeptide synthesized primarily by magnocellular neurons within the paraventricular (PVH) and supraoptic nuclei (SON) of the hypothalamus (Sofroniew, 1983; Swanson and Sawchenko, 1983; Landgraf and Neumann, 2004), has been broadly implicated in the control of parturition, lactation, appetite, emotions, stress responses, and social behavior. The distribution of OXT receptors (OXTRs) across the brain in different species provides a proxy for the distribution of OXT binding, thus providing evidence for OXT nodes in the brain of physiologic relevance. It has been reported that OXTRs are expressed in many brain sites, including the central nucleus of the amygdala and the ventromedial hypothalamic nucleus (VMH) (Bale and Dorsa, 1995b; Bale and Dorsa, 1995a). Furthermore, Oxtr mRNA has been detected in the hypothalamus, olfactory bulb, ventral pallidum, and the dorsal vagal nucleus (Yoshimura et al., 1993; Adan et al., 1995).

OXT mediates a variety of peripheral and central functions. While the peripheral actions comprise milk ejections, uterine contractions, and prolactin production, the central actions of OXT are mostly related to female reproduction, including sexual receptivity (Caldwell et al., 1986), pair bonding (Insel, 1992), and maternal behavior (Fahrbach et al., 1984; Pedersen et al., 1982; Insel, 1990). Central functions of OXT also include modulation of cardiac vagal input (Bohus et al., 1996), memory consolidation (Dyball and Paterson, 1983), and social/affiliative behavior (Insel, 1992; van Wimersma Greidanus and Maigret, 1996). Axons and dendrites of OXT neurons are localized in close proximity to the third ventricle and even in between tanycytes and ependymal cells facing the cerebrospinal fluid (Landgraf and Neumann, 2004). Notably, magnocellular OXT neurons send extended dendritic trees, forming the basis for the somato-dendritic release of OXT within the PVH and SON (Ludwig and Leng, 2006; Neumann et al., 1993; Neumann, 2007; Pow and Morris, 1989). Such release is likely to facilitate autocrine and/or paracrine regulation of OXT neurons towards physiologic demands, such as lactation (Moos and Richard, 1989; Neumann et al., 1994) and child birth (Neumann et al., 1996). To exert neuronal effects, locally released OXT binds to local OXTRs, which are expressed within or are juxtaposed to the target region, for example, on synapses, as well as on axons and glial processes (Mitre et al., 2016). Alternatively, OXT could putatively diffuse over longer distances to bind to adjacent OXTRs (Landgraf and Neumann, 2004; Ludwig and Leng, 2006; Mitre et al., 2016). Given that OXT exerts its multiple behavioral effects through its action on several regions of the forebrain and mesolimbic brain, the question of whether other extrahypothalamic projections of OXT neurons may also have a role garners significant importance.

It is also becoming increasingly clear that both anterior and posterior pituitary hormones, traditionally thought of as regulators of single physiological processes, affect multiple bodily systems, either directly or via actions on brain receptors (Zaidi et al., 2018; Abe et al., 2003). Nontraditional actions of OXT include its ability to affect the skeleton, wherein it stimulates bone formation by osteoblasts and modulates the function of bone-resorbing osteoclasts (Sun et al., 2019).

Despite a corpus of evidence for the expression of OXT and OXTRs in various brain regions, and their function in regulating central and peripheral actions, such as social behavior and satiety (Sun et al., 2019; Bale et al., 2001), there remains the need for a detailed, sex-specific mapping of the anatomical geography of the OXT and OXTR systems in the brain. Here, we use RNAscope—a cutting-edge technology that detects single RNA transcripts—to create a comprehensive sex-specific atlas of the OXT and OXTR in the mouse brain. We believe that this compendium of OXT and its receptor in concrete brain sites should provide a resource for investigators to study both peripheral and central effects of interrogating OXTRs site—specifically in health and disease. Our identification of brain nuclei with the highest OXT and OXTR transcript density will thus deepen our future understanding of the functional engagement of the central OXT-containing neuronal nodes within a large-scale functional network.

Mapping autoradiographic studies suggest that the distribution of OXTRs in the brain varies greatly among different rodent species (Dubois-Dauphin et al., 1992; Elands et al., 1988; Insel et al., 1997; Tribollet et al., 1992). Besides mapping the full anatomical distribution of Oxt and Oxtr by RNAscope, the present study also assessed sex differences in Oxt and Oxtr distribution. Allowing the detection of single transcripts, RNAscope uses ~20 pairs of transcript-specific double Z-probes to hybridize 10-µm-thick whole-brain sections. Preamplifiers first hybridize to the ~28-bp binding site formed by each double Z-probe; amplifiers then bind to the multiple binding sites on each preamplifier; and finally, labeled probes containing a fluorescent molecule bind to multiple sites of each amplifier.

RNAscope data were quantified on sections from coded three female and three male mice. Each section was viewed and analyzed using CaseViewer 2.4 (3DHISTECH, Budapest, Hungary) and QuPath v.0.2.3 (University of Edinburgh, UK). The Atlas for the Mouse Brain in Stereotaxic Coordinates (Paxinos and Franklin, 2007) was used to identify every nucleus, sub-nucleus, or region, which was followed by manual counting of Oxt and Oxtr transcripts by two independent observers (VR and AG) in every tenth section using a tag feature. Receptor density was calculated by dividing the transcript number by the area (µm², ImageJ) in every nucleus, sub-nucleus, or region. Photomicrographs were prepared using Photoshop CS5 (Adobe Systems) only to adjust brightness, contrast, and sharpness, and to remove artifacts (i.e., obscuring bubbles).

In males, we report the expression of the Oxtr in 359 mouse brain nuclei, sub-nuclei, and regions. Probe specificity was established by a positive signal in the epididymis with an absent signal in the liver (negative control) (Figure 1A). Notably, Oxtr transcripts were detected bilaterally, with no apparent ipsilateral domination. Transcript density was highest in ventricular regions, followed, in descending order, by the hypothalamus, olfactory bulb, hippocampus, cerebral cortex, medulla, midbrain and pons, forebrain, thalamus, and cerebellum (Figure 1B). Using the RNAscope dataset, we further calculated Oxtr density in various brain nuclei, sub-nuclei, and regions. High Oxtr transcript densities and counts, respectively, were also noted in several nuclei, sub-nuclei, and regions as follows (Figure 1C): ventricular regions—ependyma of the OV and 3V; hypothalamus—AHiPM for both; olfactory bulb—vn and GrO; hippocampus—Py for both; cerebral cortex—Cl and Pir; medulla—10N and Sp5I; midbrain and pons—IPF and DpMe; forebrain—aci and CPu; thalamus—PV and PVA and cerebellum—Sim for both (see Appendix 1 for nomenclature and Figure 1—figure supplement 1 for transcript count and representative photomicrographs).

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Oxtr densities in brain nuclei, subnuclei and regions.

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In females, we report the expression of the Oxtr in 301 mouse brain nuclei, sub-nuclei, and regions. Probe specificity was again established by a positive signal in the ovary with no signal in the liver (Figure 2A). Transcript density was highest in the hippocampus, followed, in descending order, by the olfactory bulb, hypothalamus, cerebral cortex, ventricular regions, forebrain, medulla, thalamus, midbrain and pons, and cerebellum (Figure 2B). High Oxtr transcript densities and counts, respectively, were also noted in several nuclei, sub-nuclei, and regions as follows (Figure 2B): hippocampus—Py for both; olfactory bulb—AOD and GrO; hypothalamus—SO and PMCo; cerebral cortex—AIP and Pir; ventricular regions—ependyma of the OV and SVZ; forebrain—SFO and aci; medulla—10N for both; thalamus—PV for both; midbrain and pons—EW and PAG and cerebellum—6Cb for both (see Appendix 1 for nomenclature and Figure 2—figure supplement 1 for transcript count and representative photomicrographs).

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Oxtr densities in brain nuclei, subnuclei and regions.

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RNAscope also revealed Oxt expression in the hypothalamus and forebrain of both male and female mice (Figure 3A and B). High Oxt counts were detected in several nuclei, sub-nuclei, and regions of females and males, respectively, as follows (Figure 3C): hypothalamus—PaMP and PaMM and forebrain—MPA and LPO. Overall, the numbers of Oxt-expressing cells were markedly greater in female compared to the male mice. That is, we found 22 hypothalamic and forebrain regions with 486 Oxt-positive cells in the female mouse. In contrast, there were 15 hypothalamic and forebrain regions containing 308 Oxt-positive cells in the male brain. Breaking this down, in the hypothalamus, the number of Oxt-positive cells was 372 in the female compared with 228 Oxt-positive cells in the male. The number of Oxt-positive cells was 114 in the female forebrain compared with 80 Oxt-positive cells in the male forebrain.

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Numbers of OXT-positive cells in the hypothalamus and forebrain.

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Oxtr expression was also mapped in regions and sub-regions within the hypothalamus (Figure 1 and Figure 1—figure supplement 1). Certain of these hypothalamic sub-regions, such as the lateral hypothalamus (LH) and dorsomedial hypothalamus (DM), send sympathetic nervous system (SNS) outflow to both bone and fat tissue (Ryu et al., 2015; Ryu et al., 2017). Additionally, RNAscope also showed Oxtr expression in both anterior and posterior pituitary lobes (Figure 4A), with Oxtr transcript density that was markedly higher in the female compared with male mice (Figure 4B).

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Sex-specific Oxtr densities in the pituitary gland.

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We also found that six hypothalamic nuclei, sub-nuclei, and regions in male mice displayed overlapping Oxt and Oxtr transcripts. Oxtr/Oxt ratios within the same brain site were as follows: 0.70 in the medial parvicellular part of the paraventricular hypothalamic nucleus (PaMP); 1.51 in the medial magnocellular part of the paraventricular hypothalamic nucleus (PaMM); 6.39 in the lateral magnocellular part of the paraventricular hypothalamic nucleus (PaLM); 26.8 in the arcuate nucleus (Arc); 109.50 in the medial amygdaloid nucleus (MeA); 151.13 in the tuber cinereum area (TC), and 222.00 in the lateroanterior hypothalamic nucleus (LA). In contrast, we found three forebrain nuclei, sub-nuclei, and regions in female mice with overlapping Oxt and Oxtr transcripts. Oxtr/Oxt ratios within the same brain site were as follows: 1.35 in the anterior commissural nucleus (AC); 3.50 in the medial preoptic nucleus, medial part (MPOM), and 13.0 in the bed nucleus of the stria terminalis, medial division, and posterolateral part (BSTMPL). As with the hypothalamus, Oxtr/Oxt ratios in ten nuclei, sub-nuclei, and regions were 0.05 in the PaLM; 0.18 in the PaMM; 0.82 in the paraventricular hypothalamic nucleus, anterior parvicellular part (PaAP); 1.74 in the LA; 5.83 in the anterior hypothalamic area, posterior part (AHP); 8.00 in the anterior hypothalamic area, anterior part (AHA); 9.33 in the supraoptic nucleus (SO); 39.0 in the ventromedial hypothalamic nucleus, dorsomedial part (VMHDM); 40.7 in the TC and 75.3 in the lateral hypothalamic area (LH).

Here, we supplement and integrate previous information on OXT and OXTR expression in the murine brain and report, for the first time, abundant OXTR expression in 301 and 359 brain nuclei, sub-nuclei, and regions in females and males, respectively, as well as, importantly, sex-specific Oxt and Oxtr expression. This report is thus the most comprehensive atlas of brain Oxt and Oxtr expression at the single transcript level. Expression of both Oxt and Oxtr, particularly in overlapping hypothalamic sub-nuclei, nuclei, and regions, points to functionally active neuronal nodes within a large-scale OXT-OXTR network in the brain.

It has been reported that cell bodies and dendrites of OXT-producing neurons within the PVH and SON release OXT and AVP within the magnocellular nuclei, where we find the highest Oxtr/Oxt colocalization—this suggests an additional, possibly paracrine action of OXT (Ludwig and Leng, 2006; Neumann et al., 1993; Neumann, 2007; Pow and Morris, 1989). Indeed, locally released OXT is involved in pre- and post-synaptic modulation of the electrical activity (Bourque et al., 1993; Shibuya et al., 2000; Kombian et al., 1997). Similar to magnocellular neurons of the PVH, we find that several Oxt-producing neuronal populations also overlap with Oxtr expression in other hypothalamic sites—hereby termed ‘Oxtr/Oxt nodes’—these include Arc, MeA, TC, and LA.

It is now well known that central OXT decreases ingestive behavior while OXTR antagonism has the opposing effect in rodents (Liu et al., 2021; Arletti et al., 1990; Blevins et al., 2016; Klockars et al., 2018; Liu et al., 2020; Noble et al., 2014; Ong et al., 2015). Of note is that, in addition to the nucleus of the solitary tract (NTS) (Ong et al., 2015), the Oxtr/Oxt node in the Arc (and, possibly, Arc-bordering LA) rapidly induces satiety (Fenselau et al., 2017) and suppresses excessive food intake to control ingestive behavior (Inada et al., 2022). In terms of sex-specific ability of OXT to inhibit ingestive behavior, it has been reported that the capacity of OXT to decrease food intake is attenuated in females compared with males, whereas lower OXT doses are effective at reducing food intake in males, and doses that are effective in both sexes reduce consumption for a longer duration in males (Liu et al., 2020). The Oxtr/Oxt node in the MeA likely explains the paracrine regulation by OXT of male preference for females and their scents (Yao et al., 2017). Thus, the ablation of Oxtr in aromatase-expressing neurons of the MeA fully recapitulates the elimination of female preference in males, suggesting that this node is both necessary and sufficient for social recognition (Ferguson et al., 2001). Lastly, the TC is a sheet of gray matter that forms a median eminence (ME) around the base of the pituitary stalk or infundibulum; therefore, the Oxtr/Oxt node in the TC (and tanycyte) could be important for mediating bidirectional brain–periphery crosstalk by modulating the blood–hypothalamus brain barrier.

Although we detected clear sex differences and similarities in Oxtr transcript expression in multiple brain areas, here we will focus on those associated with stress, energy homeostasis, emotional, and affective behaviors. Surprisingly, the highest Oxtr transcript density was noted in the ependymal layers of the OV and 3V in both sexes with greater expression density in males and, not surprisingly, in the hypothalamus (Sofroniew, 1983; Swanson and Sawchenko, 1983; Landgraf and Neumann, 2004). In the hypothalamus, the highest density was found in the posteriomedial part of the amygdalohippocampal area (AHiPM) of males compared to that in females. It has been reported that in male mice, ~40% of Oxtr-positive neurons of the amygdalohippocampal area (AHi) project to the medial preoptic area (MPOA) (Sato et al., 2020). Activation of these neurons, comprising excitatory projections to the MPOA, enhances exclusively an aggressive, but not parental behavior, towards pups (Sato et al., 2020). Of interest, females display the highest Oxtr density in the arcuate nucleus (Arc) compared to that of males. Arc^Vglut2 neurons have been reported to express the gene encoding Oxtr (Fenselau et al., 2017). Given that intra-Arc OXT acutely suppresses food intake and OXT exerts a direct stimulatory effect on Arc-OXTR neurons, it is plausible that the Arc-OXTR-satiety circuit, at least, responding to diet-induced hyperphagia (Maric et al., 2022), is pronounced in female rather than male mice. Indeed, it was demonstrated that female rats and mice display a lower than male level of diet-induced overeating (Maric et al., 2022).

The male olfactory bulb and hippocampus also displayed abundant Oxtr transcripts, with the highest density in the vomeronasal nerve (vn) and the pyramidal cell layer of the hippocampus (Py), respectively, in comparison to the female anterior olfactory nucleus, dorsal part (AOD) as well as the same (Py) hippocampal subregion. It has been reported that Oxtrs are expressed in the vomeronasal organ, an olfactory sensory structure involved in the detection of non-volatile chemosignals. OXT injection in mice has been shown to reduce pup-induced vomeronasal activity and aggressive behavior (Nakahara et al., 2020). Given vomeronasal activity declines as males grow up from a pup-aggressive state to a non-aggressive parental state, high Oxtr expression in the vn might indicate a functional switch from pup-aggressive behavior towards strengthening social and sexual behaviors during adolescence and adulthood. The highest Oxtr transcript densities in the AOD, AOM, and AOV of females are consistent with OXT function in the anterior olfactory region, particularly in relation to social cue processing and social recognition (Oettl et al., 2016). As with the hippocampal Py, Oxtrs are found in both excitatory and inhibitory pyramidal neurons within the CA2 and CA3 subregions of the hippocampus, suggesting that OXTRs in the Py may have a role in local circuits relating to stress, emotional, and affective behaviors.

In the cortex, we found that agranular insular cortex, posterior part (AIP) of females and claustrum (Cl) of males displayed the highest Oxtr transcript density. PVH- and SON-OXT neurons project to a wide range of cortical and limbic structures including AIP, Cl, hippocampus, medial amygdala, and the lateral septum, all of which comprise the social recognition memory circuit (Mitre et al., 2016; Ferguson et al., 2001; Son et al., 2022; Tanimizu et al., 2017; Wang and Zhan, 2022). SON neurons, upon activation by the OXTR, release OXT—a putative paracrine loop. Moreover, OXTRs mediate cardiac sympathetic stimulation through direct PVH projections to the intermediolateral column of the spinal cord (Japundžić-Žigon, 2013). Such reciprocal communications are supported by the studies inferring that affiliative social interactions increase OXT activity, which is followed by an anti-stress response, thus promoting bonding, relaxation, and growth, while reducing cardiovascular and neuroendocrine stress (Grippo et al., 2009; Krause et al., 2011; Lee et al., 2005; Windle et al., 1997; Wsol et al., 2008).

Both males and females had the highest Oxtr transcript density in the medullary dorsal motor nucleus of vagus (10N), as has been shown previously in the rat (Raggenbass et al., 1988; Dreifuss et al., 1988; Raggenbass et al., 1987). The OXT-sensitive vagal neurons are mostly preganglionic motor neurons, projecting to the cervical, thoracic, and abdominal visceral areas (Raggenbass et al., 1987). It has also been shown that the microinjection of an OXT antagonist into the 10N blocks the increase in gastric acid secretion and bradycardia induced by electrical stimulation of the PVH—this suggests a role for central OXT in autonomic efferent activity (Rogers and Hermann, 1986).

Finally, we have recently published an atlas of pituitary glycoprotein hormone receptors, namely Tshr, Fshr, and Lhcgr, in more than 400 brain sites (Ryu et al., 2022). Surprisingly, we find a striking overlap in receptor distribution among the four receptors, including the Oxtr—with highest transcript levels in the ependymal layer of the third ventricle and olfactory bulb. While the role of olfactory OXTRs in social recognition is well established (Oettl et al., 2016; Sun et al., 2021; Oettl and Kelsch, 2018), the functional significance of OXTRs in the ependymal layer is yet unknown. However, in light of ubiquitous and newly emerging OXTR expression in the brain and peripheral organs, ependymal OXTRs seem to have an important role in gating the bidirectional brain–periphery crosstalk.

Despite higher plasma OXT levels in women than in men (Marazziti et al., 2019), prior, largely immunohistochemistry-based studies failed to identify a sex difference in Oxt expression in the brain. Similar numbers of OXT-positive immunoreactive (-IR) neurons were found in the PVH, SON, MPOA, and bed nucleus of stria terminalis (BNST) of prairie, pine, meadow, and montane voles (Wang et al., 1996), PVH and SON of naked mole rats (Rosen et al., 2008), and PVH, MPOA, LH, and anterior hypothalamus (AH) of long-tailed hamsters (Xu et al., 2010). Furthermore, no sex differences were detected in OXT-IR neurons in the PVH, SON, BNST, MeA in several species of non-human primates (Caffé et al., 1989; Wang et al., 1997a; Wang et al., 1997b). There were also no sex differences in Oxt mRNA expression in the PVH and SON of the rat (for review, see Dumais and Veenema, 2016). Lastly, there were no sex differences in the number or size of OXT neurons in the PVH and SON in humans (Wierda et al., 1991; Fliers et al., 1985; Ishunina and Swaab, 1999). By contrast, here we establish sex differences in Oxt expression in the mouse brain. Both the hypothalamus and forebrain of the females contained visibly more Oxt-positive cells compared with males. Whereas as expected, hypothalamic PVH of both sexes had high Oxt expression, the medial preoptic area (MPA) of the female forebrain and the lateral preoptic area (LPO) of the male forebrain contained the highest number of Oxt-expressing cells.

The neuroanatomical reality of the brain–bone–fat SNS feedback loops suggests coordinated and/or multiple redundant control of bone and fat remodeling (Ryu et al., 2024). We have noted that regions, such as the LH, DM, tuber cenereum area (TC), basolateral amygdaloid nucleus, and others, known to send SNS outflow to both bone and adipose tissues, express the Oxtr (Ryu et al., 2015; Ryu et al., 2017). Surprisingly, female mice had visibly fewer Oxtr counts in aforementioned sites compared to males, perhaps due to the organizational and activational effects of sex hormones (Kammel and Correa, 2020). This raises the possibility that certain actions of OXT on peripheral tissues, such as on body composition and bone, may also be mediated centrally. Indeed, non-classical actions of OXT include its ability to affect bone remodeling, wherein it stimulates bone formation by osteoblasts and modulates the function of bone-resorbing osteoclasts (Sun et al., 2019). We have also shown that OXT and vasopressin have opposing skeletal actions—effects that may relate to the pathogenesis of bone loss in pregnancy and lactation, and in chronic hyponatremia, respectively (Sun et al., 2019; Sun et al., 2016; Tamma et al., 2009; Tamma et al., 2013). As with fat remodeling, it has been demonstrated that mice deficient in either OXT or OXTRs develop late-onset obesity despite normal ingestive behavior (Takayanagi et al., 2008). Moreover, the increased body weight in OXT knockout mice is accompanied by a 40% increase in abdominal adiposity (Camerino, 2009).

In all, studies on central OXT signaling and its control of reproductive, metabolic, and ingestive functions, and social behaviors occupy the vast majority of the literature. It is our hope that this comprehensive compendium of sex-specific Oxt and Oxtr expression in the brain will stimulate further investigations by others. In more general terms, the direct mapping of receptor expression in the brain and periphery provides the framework for determining new functions of ancient pituitary hormones and helps refocus at least some in the field towards paradigm-shifting discoveries of non-traditional, multifaceted roles of OXT.

All data generated or analyzed during this study are included in the manuscript and supporting files; source data files have been provided for Figures 1—4, Figure 1—figure supplement 1 and Figure 2—figure supplement 1.

1. 1. Abe E
   2. Marians RC
   3. Yu W
   4. Wu XB
   5. Ando T
   6. Li Y
   7. Iqbal J
   8. Eldeiry L
   9. Rajendren G
   10. Blair HC
   11. Davies TF
   12. Zaidi M

   (2003) TSH is a negative regulator of skeletal remodeling

   Cell 115:151–162.

   https://doi.org/10.1016/s0092-8674(03)00771-2

   • PubMed
   • Google Scholar
2. 1. Adan RA
   2. Van Leeuwen FW
   3. Sonnemans MA
   4. Brouns M
   5. Hoffman G
   6. Verbalis JG
   7. Burbach JP

   (1995) Rat oxytocin receptor in brain, pituitary, mammary gland, and uterus: partial sequence and immunocytochemical localization

   Endocrinology 136:4022–4028.

   https://doi.org/10.1210/endo.136.9.7649111

   • PubMed
   • Google Scholar
3. 1. Arletti R
   2. Benelli A
   3. Bertolini A

   (1990) Oxytocin inhibits food and fluid intake in rats

   Physiology & Behavior 48:825–830.

   https://doi.org/10.1016/0031-9384(90)90234-u

   • PubMed
   • Google Scholar
4. 1. Bale TL
   2. Dorsa DM

   (1995a) Regulation of oxytocin receptor messenger ribonucleic acid in the ventromedial hypothalamus by testosterone and its metabolites

   Endocrinology 136:5135–5138.

   https://doi.org/10.1210/endo.136.11.7588251

   • PubMed
   • Google Scholar
5. 1. Bale TL
   2. Dorsa DM

   (1995b) Sex differences in and effects of estrogen on oxytocin receptor messenger ribonucleic acid expression in the ventromedial hypothalamus

   Endocrinology 136:27–32.

   https://doi.org/10.1210/endo.136.1.7828541

   • PubMed
   • Google Scholar
6. 1. Bale TL
   2. Davis AM
   3. Auger AP
   4. Dorsa DM
   5. McCarthy MM

   (2001) CNS region-specific oxytocin receptor expression: importance in regulation of anxiety and sex behavior

   The Journal of Neuroscience 21:2546–2552.

   https://doi.org/10.1523/JNEUROSCI.21-07-02546.2001

   • PubMed
   • Google Scholar
7. 1. Blevins JE
   2. Thompson BW
   3. Anekonda VT
   4. Ho JM
   5. Graham JL
   6. Roberts ZS
   7. Hwang BH
   8. Ogimoto K
   9. Wolden-Hanson T
   10. Nelson J
   11. Kaiyala KJ
   12. Havel PJ
   13. Bales KL
   14. Morton GJ
   15. Schwartz MW
   16. Baskin DG

   (2016) Chronic CNS oxytocin signaling preferentially induces fat loss in high-fat diet-fed rats by enhancing satiety responses and increasing lipid utilization

   American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 310:R640–R658.

   https://doi.org/10.1152/ajpregu.00220.2015

   • PubMed
   • Google Scholar
8. 1. Bohus B
   2. Koolhaas JM
   3. Korte SM
   4. Roozendaal B
   5. Wiersma A

   (1996) Forebrain pathways and their behavioural interactions with neuroendocrine and cardiovascular function in the rat

   Clinical and Experimental Pharmacology & Physiology 23:177–182.

   https://doi.org/10.1111/j.1440-1681.1996.tb02593.x

   • PubMed
   • Google Scholar
9. 1. Bourque CW
   2. Oliet SH
   3. Kirkpatrick K
   4. Richard D
   5. Fisher TE

   (1993) Extrinsic and intrinsic modulatory mechanisms involved in regulating the electrical activity of supraoptic neurons

   Annals of the New York Academy of Sciences 689:512–519.

   https://doi.org/10.1111/j.1749-6632.1993.tb55581.x

   • PubMed
   • Google Scholar
10. 1. Caffé AR
    2. Van Ryen PC
    3. Van der Woude TP
    4. Van Leeuwen FW

    (1989) Vasopressin and oxytocin systems in the brain and upper spinal cord of Macaca fascicularis

    The Journal of Comparative Neurology 287:302–325.

    https://doi.org/10.1002/cne.902870304

    • PubMed
    • Google Scholar
11. 1. Caldwell JD
    2. Prange AJ
    3. Pedersen CA

    (1986) Oxytocin facilitates the sexual receptivity of estrogen-treated female rats

    Neuropeptides 7:175–189.

    https://doi.org/10.1016/0143-4179(86)90093-4

    • PubMed
    • Google Scholar
12. 1. Camerino C

    (2009) Low sympathetic tone and obese phenotype in oxytocin-deficient mice

    Obesity 17:980–984.

    https://doi.org/10.1038/oby.2009.12

    • PubMed
    • Google Scholar
13. 1. Dreifuss JJ
    2. Raggenbass M
    3. Charpak S
    4. Dubois-Dauphin M
    5. Tribollet E

    (1988) A role of central oxytocin in autonomic functions: its action in the motor nucleus of the vagus nerve

    Brain Research Bulletin 20:765–770.

    https://doi.org/10.1016/0361-9230(88)90089-5

    • PubMed
    • Google Scholar
14. 1. Dubois-Dauphin M
    2. Pévet P
    3. Barberis C
    4. Tribollet E
    5. Dreifuss JJ

    (1992) Localization of binding sites for oxytocin in the brain of the golden hamster

    Neuroreport 3:797–800.

    https://doi.org/10.1097/00001756-199209000-00019

    • PubMed
    • Google Scholar
15. 1. Dumais KM
    2. Veenema AH

    (2016) Vasopressin and oxytocin receptor systems in the brain: Sex differences and sex-specific regulation of social behavior

    Frontiers in Neuroendocrinology 40:1–23.

    https://doi.org/10.1016/j.yfrne.2015.04.003

    • PubMed
    • Google Scholar
16. 1. Dyball RE
    2. Paterson AT

    (1983) Neurohypophysial hormones and brain function: the neurophysiological effects of oxytocin and vasopressin

    Pharmacology & Therapeutics 20:419–436.

    https://doi.org/10.1016/0163-7258(83)90035-9

    • PubMed
    • Google Scholar
17. 1. Elands J
    2. Beetsma A
    3. Barberis C
    4. de Kloet ER

    (1988)

    Topography of the oxytocin receptor system in rat brain: an autoradiographical study with a selective radioiodinated oxytocin antagonist

    Journal of Chemical Neuroanatomy 1:293–302.

    • PubMed
    • Google Scholar
18. 1. Fahrbach SE
    2. Morrell JI
    3. Pfaff DW

    (1984) Oxytocin induction of short-latency maternal behavior in nulliparous, estrogen-primed female rats

    Hormones and Behavior 18:267–286.

    https://doi.org/10.1016/0018-506x(84)90016-3

    • PubMed
    • Google Scholar
19. 1. Fenselau H
    2. Campbell JN
    3. Verstegen AMJ
    4. Madara JC
    5. Xu J
    6. Shah BP
    7. Resch JM
    8. Yang Z
    9. Mandelblat-Cerf Y
    10. Livneh Y
    11. Lowell BB

    (2017) A rapidly acting glutamatergic ARC→PVH satiety circuit postsynaptically regulated by α-MSH

    Nature Neuroscience 20:42–51.

    https://doi.org/10.1038/nn.4442

    • PubMed
    • Google Scholar
20. 1. Ferguson JN
    2. Aldag JM
    3. Insel TR
    4. Young LJ

    (2001) Oxytocin in the medial amygdala is essential for social recognition in the mouse

    The Journal of Neuroscience 21:8278–8285.

    https://doi.org/10.1523/JNEUROSCI.21-20-08278.2001

    • PubMed
    • Google Scholar
21. 1. Fliers E
    2. Swaab DF
    3. Pool CW
    4. Verwer RW

    (1985) The vasopressin and oxytocin neurons in the human supraoptic and paraventricular nucleus; changes with aging and in senile dementia

    Brain Research 342:45–53.

    https://doi.org/10.1016/0006-8993(85)91351-4

    • PubMed
    • Google Scholar
22. 1. Grippo AJ
    2. Trahanas DM
    3. Zimmerman RR
    4. Porges SW
    5. Carter CS

    (2009) Oxytocin protects against negative behavioral and autonomic consequences of long-term social isolation

    Psychoneuroendocrinology 34:1542–1553.

    https://doi.org/10.1016/j.psyneuen.2009.05.017

    • PubMed
    • Google Scholar
23. 1. Inada K
    2. Tsujimoto K
    3. Yoshida M
    4. Nishimori K
    5. Miyamichi K

    (2022) Oxytocin signaling in the posterior hypothalamus prevents hyperphagic obesity in mice

    eLife 11:e75718.

    https://doi.org/10.7554/eLife.75718

    • PubMed
    • Google Scholar
24. 1. Insel TR

    (1990) Regional changes in brain oxytocin receptors post-partum: time-course and relationship to maternal behaviour

    Journal of Neuroendocrinology 2:539–545.

    https://doi.org/10.1111/j.1365-2826.1990.tb00445.x

    • PubMed
    • Google Scholar
25. 1. Insel TR

    (1992) Oxytocin--a neuropeptide for affiliation: evidence from behavioral, receptor autoradiographic, and comparative studies

    Psychoneuroendocrinology 17:3–35.

    https://doi.org/10.1016/0306-4530(92)90073-g

    • PubMed
    • Google Scholar
26. 1. Insel TR
    2. Young L
    3. Wang Z

    (1997) Central oxytocin and reproductive behaviours

    Reviews of Reproduction 2:28–37.

    https://doi.org/10.1530/ror.0.0020028

    • PubMed
    • Google Scholar
27. 1. Ishunina TA
    2. Swaab DF

    (1999) Vasopressin and oxytocin neurons of the human supraoptic and paraventricular nucleus: size changes in relation to age and sex

    The Journal of Clinical Endocrinology and Metabolism 84:4637–4644.

    https://doi.org/10.1210/jcem.84.12.6187

    • PubMed
    • Google Scholar
28. 1. Japundžić-Žigon N

    (2013) Vasopressin and oxytocin in control of the cardiovascular system

    Current Neuropharmacology 11:218–230.

    https://doi.org/10.2174/1570159X11311020008

    • PubMed
    • Google Scholar
29. 1. Kammel LG
    2. Correa SM

    (2020) Selective sexual differentiation of neurone populations may contribute to sex-specific outputs of the ventromedial nucleus of the hypothalamus

    Journal of Neuroendocrinology 32:e12801.

    https://doi.org/10.1111/jne.12801

    • PubMed
    • Google Scholar
30. 1. Klockars OA
    2. Klockars A
    3. Levine AS
    4. Olszewski PK

    (2018) Oxytocin administration in the basolateral and central nuclei of amygdala moderately suppresses food intake

    Neuroreport 29:504–510.

    https://doi.org/10.1097/WNR.0000000000001005

    • PubMed
    • Google Scholar
31. 1. Kombian SB
    2. Mouginot D
    3. Pittman QJ

    (1997) Dendritically released peptides act as retrograde modulators of afferent excitation in the supraoptic nucleus in vitro

    Neuron 19:903–912.

    https://doi.org/10.1016/s0896-6273(00)80971-x

    • PubMed
    • Google Scholar
32. 1. Krause EG
    2. de Kloet AD
    3. Flak JN
    4. Smeltzer MD
    5. Solomon MB
    6. Evanson NK
    7. Woods SC
    8. Sakai RR
    9. Herman JP

    (2011) Hydration state controls stress responsiveness and social behavior

    The Journal of Neuroscience 31:5470–5476.

    https://doi.org/10.1523/JNEUROSCI.6078-10.2011

    • PubMed
    • Google Scholar
33. 1. Landgraf R
    2. Neumann ID

    (2004) Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication

    Frontiers in Neuroendocrinology 25:150–176.

    https://doi.org/10.1016/j.yfrne.2004.05.001

    • PubMed
    • Google Scholar
34. 1. Lee PR
    2. Brady DL
    3. Shapiro RA
    4. Dorsa DM
    5. Koenig JI

    (2005) Social interaction deficits caused by chronic phencyclidine administration are reversed by oxytocin

    Neuropsychopharmacology 30:1883–1894.

    https://doi.org/10.1038/sj.npp.1300722

    • PubMed
    • Google Scholar
35. 1. Liu CM
    2. Davis EA
    3. Suarez AN
    4. Wood RI
    5. Noble EE
    6. Kanoski SE

    (2020) Sex differences and estrous influences on oxytocin control of food intake

    Neuroscience 447:63–73.

    https://doi.org/10.1016/j.neuroscience.2019.10.020

    • PubMed
    • Google Scholar
36. 1. Liu CM
    2. Spaulding MO
    3. Rea JJ
    4. Noble EE
    5. Kanoski SE

    (2021) Oxytocin and food intake control: neural, behavioral, and signaling mechanisms

    International Journal of Molecular Sciences 22:10859.

    https://doi.org/10.3390/ijms221910859

    • PubMed
    • Google Scholar
37. 1. Ludwig M
    2. Leng G

    (2006) Dendritic peptide release and peptide-dependent behaviours

    Nature Reviews. Neuroscience 7:126–136.

    https://doi.org/10.1038/nrn1845

    • PubMed
    • Google Scholar
38. 1. Marazziti D
    2. Baroni S
    3. Mucci F
    4. Piccinni A
    5. Moroni I
    6. Giannaccini G
    7. Carmassi C
    8. Massimetti E
    9. Dell’Osso L

    (2019) Sex-related differences in plasma oxytocin levels in humans

    Clinical Practice & Epidemiology in Mental Health 15:58–63.

    https://doi.org/10.2174/1745017901915010058

    • PubMed
    • Google Scholar
39. 1. Maric I
    2. Krieger J-P
    3. van der Velden P
    4. Börchers S
    5. Asker M
    6. Vujicic M
    7. Wernstedt Asterholm I
    8. Skibicka KP

    (2022) Sex and species differences in the development of diet-induced obesity and metabolic disturbances in rodents

    Frontiers in Nutrition 9:828522.

    https://doi.org/10.3389/fnut.2022.828522

    • PubMed
    • Google Scholar
40. 1. Mitre M
    2. Marlin BJ
    3. Schiavo JK
    4. Morina E
    5. Norden SE
    6. Hackett TA
    7. Aoki CJ
    8. Chao MV
    9. Froemke RC

    (2016) A distributed network for social cognition enriched for oxytocin receptors

    The Journal of Neuroscience 36:2517–2535.

    https://doi.org/10.1523/JNEUROSCI.2409-15.2016

    • PubMed
    • Google Scholar
41. 1. Moos F
    2. Richard P

    (1989) Paraventricular and supraoptic bursting oxytocin cells in rat are locally regulated by oxytocin and functionally related

    The Journal of Physiology 408:1–18.

    https://doi.org/10.1113/jphysiol.1989.sp017442

    • PubMed
    • Google Scholar
42. 1. Nakahara TS
    2. Camargo AP
    3. Magalhães PHM
    4. Souza MAA
    5. Ribeiro PG
    6. Martins-Netto PH
    7. Carvalho VMA
    8. José J
    9. Papes F

    (2020) Peripheral oxytocin injection modulates vomeronasal sensory activity and reduces pup-directed aggression in male mice

    Scientific Reports 10:19943.

    https://doi.org/10.1038/s41598-020-77061-7

    • PubMed
    • Google Scholar
43. 1. Neumann I
    2. Russell JA
    3. Landgraf R

    (1993) Oxytocin and vasopressin release within the supraoptic and paraventricular nuclei of pregnant, parturient and lactating rats: a microdialysis study

    Neuroscience 53:65–75.

    https://doi.org/10.1016/0306-4522(93)90285-n

    • PubMed
    • Google Scholar
44. 1. Neumann I
    2. Koehler E
    3. Landgraf R
    4. Summy-Long J

    (1994) An oxytocin receptor antagonist infused into the supraoptic nucleus attenuates intranuclear and peripheral release of oxytocin during suckling in conscious rats

    Endocrinology 134:141–148.

    https://doi.org/10.1210/endo.134.1.8275928

    • PubMed
    • Google Scholar
45. 1. Neumann I
    2. Douglas AJ
    3. Pittman QJ
    4. Russell JA
    5. Landgraf R

    (1996) Oxytocin released within the supraoptic nucleus of the rat brain by positive feedback action is involved in parturition-related events

    Journal of Neuroendocrinology 8:227–233.

    https://doi.org/10.1046/j.1365-2826.1996.04557.x

    • PubMed
    • Google Scholar
46. 1. Neumann ID

    (2007) Stimuli and consequences of dendritic release of oxytocin within the brain

    Biochemical Society Transactions 35:1252–1257.

    https://doi.org/10.1042/BST0351252

    • PubMed
    • Google Scholar
47. 1. Noble EE
    2. Billington CJ
    3. Kotz CM
    4. Wang C

    (2014) Oxytocin in the ventromedial hypothalamic nucleus reduces feeding and acutely increases energy expenditure

    American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 307:R737–R745.

    https://doi.org/10.1152/ajpregu.00118.2014

    • PubMed
    • Google Scholar
48. 1. Oettl L-L
    2. Ravi N
    3. Schneider M
    4. Scheller MF
    5. Schneider P
    6. Mitre M
    7. da Silva Gouveia M
    8. Froemke RC
    9. Chao MV
    10. Young WS
    11. Meyer-Lindenberg A
    12. Grinevich V
    13. Shusterman R
    14. Kelsch W

    (2016) Oxytocin enhances social recognition by modulating cortical control of early olfactory processing

    Neuron 90:609–621.

    https://doi.org/10.1016/j.neuron.2016.03.033

    • PubMed
    • Google Scholar
49. 1. Oettl LL
    2. Kelsch W

    (2018) Oxytocin and olfaction

    Current Topics in Behavioral Neurosciences 35:55–75.

    https://doi.org/10.1007/7854_2017_8

    • PubMed
    • Google Scholar
50. 1. Ong ZY
    2. Alhadeff AL
    3. Grill HJ

    (2015) Medial nucleus tractus solitarius oxytocin receptor signaling and food intake control: the role of gastrointestinal satiation signal processing

    American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 308:R800–R806.

    https://doi.org/10.1152/ajpregu.00534.2014

    • PubMed
    • Google Scholar
51. Book

    1. Paxinos G
    2. Franklin KBJ

    (2007)

    The Mouse Brain in Stereotaxic Coordinates

    Academic Press.

    • Google Scholar
52. 1. Pedersen CA
    2. Ascher JA
    3. Monroe YL
    4. Prange AJ

    (1982) Oxytocin induces maternal behavior in virgin female rats

    Science 216:648–650.

    https://doi.org/10.1126/science.7071605

    • PubMed
    • Google Scholar
53. 1. Pow DV
    2. Morris JF

    (1989) Dendrites of hypothalamic magnocellular neurons release neurohypophysial peptides by exocytosis

    Neuroscience 32:435–439.

    https://doi.org/10.1016/0306-4522(89)90091-2

    • PubMed
    • Google Scholar
54. 1. Raggenbass M
    2. Dubois-Dauphin M
    3. Charpak S
    4. Dreifuss JJ

    (1987) Neurons in the dorsal motor nucleus of the vagus nerve are excited by oxytocin in the rat but not in the guinea pig

    PNAS 84:3926–3930.

    https://doi.org/10.1073/pnas.84.11.3926

    • PubMed
    • Google Scholar
55. 1. Raggenbass M
    2. Charpak S
    3. Dubois-Dauphin M
    4. Dreifuss JJ

    (1988) Electrophysiological evidence for oxytocin receptors on neurones located in the dorsal motor nucleus of the vagus nerve in the rat brainstem

    Journal of Receptor Research 8:273–282.

    https://doi.org/10.3109/10799898809048992

    • PubMed
    • Google Scholar
56. 1. Rogers RC
    2. Hermann GE

    (1986) Hypothalamic paraventricular nucleus stimulation-induced gastric acid secretion and bradycardia suppressed by oxytocin antagonist

    Peptides 7:695–700.

    https://doi.org/10.1016/0196-9781(86)90046-x

    • PubMed
    • Google Scholar
57. 1. Rosen GJ
    2. de Vries GJ
    3. Goldman SL
    4. Goldman BD
    5. Forger NG

    (2008) Distribution of oxytocin in the brain of a eusocial rodent

    Neuroscience 155:809–817.

    https://doi.org/10.1016/j.neuroscience.2008.05.039

    • PubMed
    • Google Scholar
58. 1. Ryu V
    2. Garretson JT
    3. Liu Y
    4. Vaughan CH
    5. Bartness TJ

    (2015) Brown adipose tissue has sympathetic-sensory feedback circuits

    The Journal of Neuroscience 35:2181–2190.

    https://doi.org/10.1523/JNEUROSCI.3306-14.2015

    • PubMed
    • Google Scholar
59. 1. Ryu V
    2. Watts AG
    3. Xue B
    4. Bartness TJ

    (2017) Bidirectional crosstalk between the sensory and sympathetic motor systems innervating brown and white adipose tissue in male Siberian hamsters

    American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 312:R324–R337.

    https://doi.org/10.1152/ajpregu.00456.2015

    • PubMed
    • Google Scholar
60. 1. Ryu V
    2. Gumerova A
    3. Korkmaz F
    4. Kang SS
    5. Katsel P
    6. Miyashita S
    7. Kannangara H
    8. Cullen L
    9. Chan P
    10. Kuo T
    11. Padilla A
    12. Sultana F
    13. Wizman SA
    14. Kramskiy N
    15. Zaidi S
    16. Kim S-M
    17. New MI
    18. Rosen CJ
    19. Goosens KA
    20. Frolinger T
    21. Haroutunian V
    22. Ye K
    23. Lizneva D
    24. Davies TF
    25. Yuen T
    26. Zaidi M

    (2022) Brain atlas for glycoprotein hormone receptors at single-transcript level

    eLife 11:e79612.

    https://doi.org/10.7554/eLife.79612

    • PubMed
    • Google Scholar
61. 1. Ryu V
    2. Gumerova AA
    3. Witztum R
    4. Korkmaz F
    5. Cullen L
    6. Kannangara H
    7. Moldavski O
    8. Barak O
    9. Lizneva D
    10. Goosens KA
    11. Stanley S
    12. Kim SM
    13. Yuen T
    14. Zaidi M

    (2024) An atlas of brain-bone sympathetic neural circuits in mice

    eLife 13:e95727.

    https://doi.org/10.7554/eLife.95727

    • PubMed
    • Google Scholar
62. 1. Sato K
    2. Hamasaki Y
    3. Fukui K
    4. Ito K
    5. Miyamichi K
    6. Minami M
    7. Amano T

    (2020) Amygdalohippocampal area neurons that project to the preoptic area mediate infant-directed attack in male mice

    The Journal of Neuroscience 40:3981–3994.

    https://doi.org/10.1523/JNEUROSCI.0438-19.2020

    • PubMed
    • Google Scholar
63. 1. Shibuya I
    2. Kabashima N
    3. Ibrahim N
    4. Setiadji SV
    5. Ueta Y
    6. Yamashita H

    (2000) Pre- and postsynaptic modulation of the electrical activity of rat supraoptic neurones

    Experimental Physiology 85 Spec No:145S–151S.

    https://doi.org/10.1111/j.1469-445x.2000.tb00018.x

    • PubMed
    • Google Scholar
64. 1. Sofroniew MV

    (1983) Morphology of vasopressin and oxytocin neurones and their central and vascular projections

    Progress in Brain Research 60:101–114.

    https://doi.org/10.1016/S0079-6123(08)64378-2

    • PubMed
    • Google Scholar
65. 1. Son S
    2. Manjila SB
    3. Newmaster KT
    4. Wu Y-T
    5. Vanselow DJ
    6. Ciarletta M
    7. Anthony TE
    8. Cheng KC
    9. Kim Y

    (2022) Whole-brain wiring diagram of oxytocin system in adult mice

    The Journal of Neuroscience 42:5021–5033.

    https://doi.org/10.1523/JNEUROSCI.0307-22.2022

    • PubMed
    • Google Scholar
66. 1. Sun L
    2. Tamma R
    3. Yuen T
    4. Colaianni G
    5. Ji Y
    6. Cuscito C
    7. Bailey J
    8. Dhawan S
    9. Lu P
    10. Calvano CD
    11. Zhu LL
    12. Zambonin CG
    13. Di Benedetto A
    14. Stachnik A
    15. Liu P
    16. Grano M
    17. Colucci S
    18. Davies TF
    19. New MI
    20. Zallone A
    21. Zaidi M

    (2016) Functions of vasopressin and oxytocin in bone mass regulation

    PNAS 113:164–169.

    https://doi.org/10.1073/pnas.1523762113

    • PubMed
    • Google Scholar
67. 1. Sun L
    2. Lizneva D
    3. Ji Y
    4. Colaianni G
    5. Hadelia E
    6. Gumerova A
    7. Ievleva K
    8. Kuo TC
    9. Korkmaz F
    10. Ryu V
    11. Rahimova A
    12. Gera S
    13. Taneja C
    14. Khan A
    15. Ahmad N
    16. Tamma R
    17. Bian Z
    18. Zallone A
    19. Kim SM
    20. New MI
    21. Iqbal J
    22. Yuen T
    23. Zaidi M

    (2019) Oxytocin regulates body composition

    PNAS 116:26808–26815.

    https://doi.org/10.1073/pnas.1913611116

    • PubMed
    • Google Scholar
68. 1. Sun C
    2. Yin Z
    3. Li B-Z
    4. Du H
    5. Tang K
    6. Liu P
    7. Hang Pun S
    8. Lei TC
    9. Li A

    (2021) Oxytocin modulates neural processing of mitral/tufted cells in the olfactory bulb

    Acta Physiologica 231:e13626.

    https://doi.org/10.1111/apha.13626

    • PubMed
    • Google Scholar
69. 1. Swanson LW
    2. Sawchenko PE

    (1983) Hypothalamic integration: organization of the paraventricular and supraoptic nuclei

    Annual Review of Neuroscience 6:269–324.

    https://doi.org/10.1146/annurev.ne.06.030183.001413

    • PubMed
    • Google Scholar
70. 1. Takayanagi Y
    2. Kasahara Y
    3. Onaka T
    4. Takahashi N
    5. Kawada T
    6. Nishimori K

    (2008) Oxytocin receptor-deficient mice developed late-onset obesity

    Neuroreport 19:951–955.

    https://doi.org/10.1097/WNR.0b013e3283021ca9

    • PubMed
    • Google Scholar
71. 1. Tamma R
    2. Colaianni G
    3. Zhu L
    4. DiBenedetto A
    5. Greco G
    6. Montemurro G
    7. Patano N
    8. Strippoli M
    9. Vergari R
    10. Mancini L
    11. Colucci S
    12. Grano M
    13. Faccio R
    14. Liu X
    15. Li J
    16. Usmani S
    17. Bachar M
    18. Bab I
    19. Nishimori K
    20. Young LJ
    21. Buettner C
    22. Iqbal J
    23. Sun L
    24. Zaidi M
    25. Zallone A

    (2009) Oxytocin is an anabolic bone hormone

    PNAS 106:7149–7154.

    https://doi.org/10.1073/pnas.0901890106

    • PubMed
    • Google Scholar
72. 1. Tamma R
    2. Sun L
    3. Cuscito C
    4. Lu P
    5. Corcelli M
    6. Li J
    7. Colaianni G
    8. Moonga SS
    9. Di Benedetto A
    10. Grano M
    11. Colucci S
    12. Yuen T
    13. New MI
    14. Zallone A
    15. Zaidi M

    (2013) Regulation of bone remodeling by vasopressin explains the bone loss in hyponatremia

    PNAS 110:18644–18649.

    https://doi.org/10.1073/pnas.1318257110

    • PubMed
    • Google Scholar
73. 1. Tanimizu T
    2. Kenney JW
    3. Okano E
    4. Kadoma K
    5. Frankland PW
    6. Kida S

    (2017) Functional connectivity of multiple brain regions required for the consolidation of social recognition memory

    The Journal of Neuroscience 37:4103–4116.

    https://doi.org/10.1523/JNEUROSCI.3451-16.2017

    • PubMed
    • Google Scholar
74. 1. Tribollet E
    2. Dreifuss JJ
    3. Barberis C
    4. Jard S
    5. Dubois-Dauphin M

    (1992) Oxytocin receptors in the central nervous system

    Annals of the New York Academy of Sciences 652:29–38.

    https://doi.org/10.1111/j.1749-6632.1992.tb34343.x

    • PubMed
    • Google Scholar
75. 1. van Wimersma Greidanus TB
    2. Maigret C

    (1996) The role of limbic vasopressin and oxytocin in social recognition

    Brain Research 713:153–159.

    https://doi.org/10.1016/0006-8993(95)01505-1

    • PubMed
    • Google Scholar
76. 1. Wang Z
    2. Zhou L
    3. Hulihan TJ
    4. Insel TR

    (1996) Immunoreactivity of central vasopressin and oxytocin pathways in microtine rodents: a quantitative comparative study

    The Journal of Comparative Neurology 366:726–737.

    https://doi.org/10.1002/(SICI)1096-9861(19960318)366:4<726::AID-CNE11>3.0.CO;2-D

    • PubMed
    • Google Scholar
77. 1. Wang Z
    2. Moody K
    3. Newman JD
    4. Insel TR

    (1997a) Vasopressin and oxytocin immunoreactive neurons and fibers in the forebrain of male and female common marmosets (Callithrix jacchus)

    Synapse 27:14–25.

    https://doi.org/10.1002/(SICI)1098-2396(199709)27:1<14::AID-SYN2>3.0.CO;2-G

    • PubMed
    • Google Scholar
78. 1. Wang Z
    2. Toloczko D
    3. Young LJ
    4. Moody K
    5. Newman JD
    6. Insel TR

    (1997b) Vasopressin in the forebrain of common marmosets (Callithrix jacchus): studies with in situ hybridization, immunocytochemistry and receptor autoradiography

    Brain Research 768:147–156.

    https://doi.org/10.1016/s0006-8993(97)00636-7

    • PubMed
    • Google Scholar
79. 1. Wang X
    2. Zhan Y

    (2022) Regulation of social recognition memory in the hippocampal circuits

    Frontiers in Neural Circuits 16:839931.

    https://doi.org/10.3389/fncir.2022.839931

    • PubMed
    • Google Scholar
80. 1. Wierda M
    2. Goudsmit E
    3. Van der Woude PF
    4. Purba JS
    5. Hofman MA
    6. Bogte H
    7. Swaab DF

    (1991) Oxytocin cell number in the human paraventricular nucleus remains constant with aging and in Alzheimer’s disease

    Neurobiology of Aging 12:511–516.

    https://doi.org/10.1016/0197-4580(91)90081-t

    • PubMed
    • Google Scholar
81. 1. Windle RJ
    2. Shanks N
    3. Lightman SL
    4. Ingram CD

    (1997) Central oxytocin administration reduces stress-induced corticosterone release and anxiety behavior in rats

    Endocrinology 138:2829–2834.

    https://doi.org/10.1210/endo.138.7.5255

    • PubMed
    • Google Scholar
82. 1. Wsol A
    2. Cudnoch-Jedrzejewska A
    3. Szczepanska-Sadowska E
    4. Kowalewski S
    5. Puchalska L

    (2008)

    Oxytocin in the cardiovascular responses to stress

    Journal of Physiology and Pharmacology 59 Suppl 8:123–127.

    • PubMed
    • Google Scholar
83. 1. Xu L
    2. Pan Y
    3. Young KA
    4. Wang Z
    5. Zhang Z

    (2010) Oxytocin and vasopressin immunoreactive staining in the brains of Brandt’s voles (Lasiopodomys brandtii) and greater long-tailed hamsters (Tscherskia triton)

    Neuroscience 169:1235–1247.

    https://doi.org/10.1016/j.neuroscience.2010.05.064

    • PubMed
    • Google Scholar
84. 1. Yao S
    2. Bergan J
    3. Lanjuin A
    4. Dulac C

    (2017) Oxytocin signaling in the medial amygdala is required for sex discrimination of social cues

    eLife 6:e31373.

    https://doi.org/10.7554/eLife.31373

    • PubMed
    • Google Scholar
85. 1. Yoshimura R
    2. Kiyama H
    3. Kimura T
    4. Araki T
    5. Maeno H
    6. Tanizawa O
    7. Tohyama M

    (1993) Localization of oxytocin receptor messenger ribonucleic acid in the rat brain

    Endocrinology 133:1239–1246.

    https://doi.org/10.1210/endo.133.3.8396014

    • PubMed
    • Google Scholar
86. 1. Zaidi M
    2. New MI
    3. Blair HC
    4. Zallone A
    5. Baliram R
    6. Davies TF
    7. Cardozo C
    8. Iqbal J
    9. Sun L
    10. Rosen CJ
    11. Yuen T

    (2018) Actions of pituitary hormones beyond traditional targets

    The Journal of Endocrinology 237:R83–R98.

    https://doi.org/10.1530/JOE-17-0680

    • PubMed
    • Google Scholar

Author details

1. Vitaly Ryu

   1. Institute for Translational Medicine and Pharmacology (ITMaP), Icahn School of Medicine at Mount Sinai, New York, United States
   2. Departments of Medicine and of Pharmacological Sciences, Icahn School of Medicine at Mount Sinai, New York, United States

   Contribution

   Formal analysis, Investigation, Methodology, Writing – original draft

   For correspondence

   vitaly.ryu@mssm.edu

   Competing interests

   Reviewing editor, eLife

   "This ORCID iD identifies the author of this article:" 0000-0001-8068-4577

2. Anisa Azatovna Gumerova

   1. Institute for Translational Medicine and Pharmacology (ITMaP), Icahn School of Medicine at Mount Sinai, New York, United States
   2. Departments of Medicine and of Pharmacological Sciences, Icahn School of Medicine at Mount Sinai, New York, United States

   Contribution

   Investigation, Visualization, Methodology

   Competing interests

   No competing interests declared

3. Georgii Pevnev

   1. Institute for Translational Medicine and Pharmacology (ITMaP), Icahn School of Medicine at Mount Sinai, New York, United States
   2. Departments of Medicine and of Pharmacological Sciences, Icahn School of Medicine at Mount Sinai, New York, United States

   Contribution

   Investigation

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-2015-9310

4. Funda Korkmaz

   1. Institute for Translational Medicine and Pharmacology (ITMaP), Icahn School of Medicine at Mount Sinai, New York, United States
   2. Departments of Medicine and of Pharmacological Sciences, Icahn School of Medicine at Mount Sinai, New York, United States

   Contribution

   Validation, Investigation

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-9174-8369

5. Hasni Kannangara

   1. Institute for Translational Medicine and Pharmacology (ITMaP), Icahn School of Medicine at Mount Sinai, New York, United States
   2. Departments of Medicine and of Pharmacological Sciences, Icahn School of Medicine at Mount Sinai, New York, United States

   Contribution

   Formal analysis, Validation

   Competing interests

   No competing interests declared

6. Liam Cullen

   1. Institute for Translational Medicine and Pharmacology (ITMaP), Icahn School of Medicine at Mount Sinai, New York, United States
   2. Departments of Medicine and of Pharmacological Sciences, Icahn School of Medicine at Mount Sinai, New York, United States

   Contribution

   Investigation

   Competing interests

   No competing interests declared

7. Farhath Sultana

   1. Institute for Translational Medicine and Pharmacology (ITMaP), Icahn School of Medicine at Mount Sinai, New York, United States
   2. Departments of Medicine and of Pharmacological Sciences, Icahn School of Medicine at Mount Sinai, New York, United States

   Contribution

   Formal analysis, Investigation

   Competing interests

   No competing interests declared

8. Ronit Witztum

   1. Institute for Translational Medicine and Pharmacology (ITMaP), Icahn School of Medicine at Mount Sinai, New York, United States
   2. Departments of Medicine and of Pharmacological Sciences, Icahn School of Medicine at Mount Sinai, New York, United States

   Contribution

   Investigation

   Competing interests

   No competing interests declared

9. Steven Lee Sims

   1. Institute for Translational Medicine and Pharmacology (ITMaP), Icahn School of Medicine at Mount Sinai, New York, United States
   2. Departments of Medicine and of Pharmacological Sciences, Icahn School of Medicine at Mount Sinai, New York, United States

   Contribution

   Investigation

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-1636-084X

10. Tal Frolinger

    1. Institute for Translational Medicine and Pharmacology (ITMaP), Icahn School of Medicine at Mount Sinai, New York, United States
    2. Departments of Medicine and of Pharmacological Sciences, Icahn School of Medicine at Mount Sinai, New York, United States

    Contribution

    Investigation

    Competing interests

    No competing interests declared

11. Ofer Moldavski

    1. Institute for Translational Medicine and Pharmacology (ITMaP), Icahn School of Medicine at Mount Sinai, New York, United States
    2. Departments of Medicine and of Pharmacological Sciences, Icahn School of Medicine at Mount Sinai, New York, United States

    Contribution

    Investigation

    Competing interests

    No competing interests declared

12. Orly Barak

    1. Institute for Translational Medicine and Pharmacology (ITMaP), Icahn School of Medicine at Mount Sinai, New York, United States
    2. Departments of Medicine and of Pharmacological Sciences, Icahn School of Medicine at Mount Sinai, New York, United States

    Contribution

    Investigation, Project administration

    Competing interests

    No competing interests declared

13. Emily Weiss

    1. Institute for Translational Medicine and Pharmacology (ITMaP), Icahn School of Medicine at Mount Sinai, New York, United States
    2. Departments of Medicine and of Pharmacological Sciences, Icahn School of Medicine at Mount Sinai, New York, United States

    Contribution

    Formal analysis, Investigation

    Competing interests

    No competing interests declared

14. Jay J Cao

    United States Department of Agriculture, Grand Forks Human Nutrition Research Center, Grand Forks, ND 58203, Grand Forks, United States

    Contribution

    Resources, Investigation

    Competing interests

    Reviewing editor, eLife

15. Daria Lizneva

    1. Institute for Translational Medicine and Pharmacology (ITMaP), Icahn School of Medicine at Mount Sinai, New York, United States
    2. Departments of Medicine and of Pharmacological Sciences, Icahn School of Medicine at Mount Sinai, New York, United States

    Contribution

    Investigation, Project administration

    Competing interests

    Reviewing editor, eLife

16. Ki A Goosens

    1. Institute for Translational Medicine and Pharmacology (ITMaP), Icahn School of Medicine at Mount Sinai, New York, United States
    2. Departments of Medicine and of Pharmacological Sciences, Icahn School of Medicine at Mount Sinai, New York, United States

    Contribution

    Data curation, Supervision

    Competing interests

    Reviewing editor, eLife

    "This ORCID iD identifies the author of this article:" 0000-0002-5246-2261

17. Tony Yuen

    1. Institute for Translational Medicine and Pharmacology (ITMaP), Icahn School of Medicine at Mount Sinai, New York, United States
    2. Departments of Medicine and of Pharmacological Sciences, Icahn School of Medicine at Mount Sinai, New York, United States

    Contribution

    Conceptualization, Supervision, Funding acquisition, Project administration, Writing – review and editing

    Competing interests

    Senior editor, eLife

18. Mone Zaidi

    1. Institute for Translational Medicine and Pharmacology (ITMaP), Icahn School of Medicine at Mount Sinai, New York, United States
    2. Departments of Medicine and of Pharmacological Sciences, Icahn School of Medicine at Mount Sinai, New York, United States

    Contribution

    Conceptualization, Funding acquisition, Writing – original draft, Project administration, Writing – review and editing

    For correspondence

    mone.zaidi@mountsinai.org

    Competing interests

    consults for Gershon Lehmann, Guidepoint and Coleman groups

    "This ORCID iD identifies the author of this article:" 0000-0001-5911-9522

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