Quantitative mapping reveals age and sex differences in vasopressin, but not oxytocin, immunoreactivity in the rat social behavior neural network

DiBenedictis, Brett T.; Nussbaum, Elizabeth R.; Cheung, Harry K.; Veenema, Alexa H.

doi:10.1002/cne.24216

Cited by 70 publications

(61 citation statements)

References 107 publications

(169 reference statements)

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“…Indeed, a thorough analysis of the extant literature (for which there are fewer studies targeting OT/OTR) reveals many more sex differences in VP/V1aR systems compared to OT/ OTR differences (Dumais & Veenema 2016). A systematic cross-species characterization of OT-ir and VP-ir across developmental time and between the sexes exhibited plentiful differences in VP-ir in the social behavior network (Newman 1999;Goodson 2005), but none on OT-ir in rats (DiBenedictis et al 2017). Taken together, there is substantial evidence indicating that the vasopressin system varies more than that of oxytocin, particularly as a function of sex and developmental experiences.…”

Section: Stability and Variability Among The Nonapeptide Systemsmentioning

confidence: 99%

Interactions of sex and early life social experiences at two developmental stages shape nonapeptide receptor profiles

Hiura

Ophir

2018

Integrative Zoology

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Early life social experiences are critical to behavioral and cognitive development, and can have a tremendous influence on developing social phenotypes. Most work has focused on outcomes of experiences at a single stage of development (e.g. perinatal or post-weaning). Few studies have assessed the impact of social experience at multiple developmental stages and across sex. Oxytocin and vasopressin are profoundly important for modulating social behavior and these nonapeptide systems are highly sensitive to developmental social experience, particularly in brain areas important for social behavior. We investigated whether oxytocin receptor (OTR) and vasopressin receptor (V1aR) distributions of prairie voles (Microtus ochrogaster) change as a function of parental composition within the natal nest or social composition after weaning. We raised pups either in the presence or absence of their fathers. At weaning, offspring were housed either individually or with a same-sex sibling. We also examined whether changes in receptor distributions are sexually dimorphic because the impact of the developmental environment on the nonapeptide system could be sex-dependent. We found that differences in nonapeptide receptor expression were region-specific, sex-specific and rearing condition-specific, indicating a high level of complexity in the ways that early life experiences shape the social brain. We found many more differences in V1aR density compared to OTR density, indicating that nonapeptide receptors demonstrate differential levels of neural plasticity and sensitivity to environmental and biological variables. Our data highlight that critical factors including biological sex and multiple experiences across the developmental continuum interact in complex ways to shape the social brain.

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Section: Stability and Variability Among The Nonapeptide Systemsmentioning

confidence: 99%

Interactions of sex and early life social experiences at two developmental stages shape nonapeptide receptor profiles

Hiura

Ophir

2018

Integrative Zoology

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“…Understanding the development of this system can provide insight into how individual differences in social behavior arise, and elucidate sources of behavioral dysfunction. The ontogeny of VP and OT neuronal populations has been examined in rodents (DiBenedictis et al 2017; Grinevich et al 2014; Swaab and Ter Borg 1981; Boer et al 1980; Yamamoto et al 2004), demonstrating that these cell groups are present at parturition, although dendritic and axonal growth, and neuron number, continue to grow in the first weeks after birth (Hammock 2015; Grinevich et al 2014; Tamborski et al 2016). Although the anatomical distribution of nonapeptide neurons throughout development has been described, their functional roles during the early development are surprisingly understudied.…”

Section: Introductionmentioning

confidence: 99%

“…The ontogeny of rodent nonapeptide neuron and receptor anatomical distributions has been described in rats (Boer et al 1980; DiBenedictis et al 2017; Krisch 1980; Smith et al 2017; Swaab and Ter Borg 1981), mice (Godefroy et al 2017), jirds (Rabhi et al 1996, 1999), and voles (lateral septum nonapeptide receptors only, Wang and Young 1997; PVN VP and OT neurons only; Yamamoto et al 2004). However, to our knowledge, it is largely unknown whether nonapeptide neurons exhibit distinct functional properties or play different functional roles in behavior at different stages of development, particularly during rapid brain growth stages.…”

Section: Introductionmentioning

confidence: 99%

Rapid nonapeptide synthesis during a critical period of development in the prairie vole: plasticity of the paraventricular nucleus of the hypothalamus

2018

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Vasopressin (VP) and oxytocin (OT) are involved in modulating basic physiology and numerous social behaviors. Although the anatomical distributions of nonapeptide neurons throughout development have been described, the functional roles of VP and OT neurons during development are surprisingly understudied, and it is unknown whether they exhibit functional changes throughout early development. We utilized an acute social isolation paradigm to determine if VP and OT neural responses in eight nonapeptide cell groups differ at three different stages of early development in prairie voles. We tested pups at ages that are representative of the three rapid growth stages of the developing brain: postnatal day (PND)2 (closed eyes; poor locomotion), PND9 (eye opening; locomotion; peak brain growth spurt), and PND21 (weaning). Neural responses were examined in pups that (1) were under normal family conditions with their parents and siblings, (2) were isolated from their parents and siblings and then reunited, and (3) were isolated from their parents and siblings. We found that VP and OT neural activity (as assessed via Fos co-localization) did not differ in response to social condition across development. However, remarkably rapid VP and OT synthesis in response to social isolation was observed only in the paraventricular nucleus of the hypothalamus (PVN) and only in PND9 pups. These results suggest that PVN nonapeptide neurons exhibit distinct cellular properties during a critical period of development, allowing nonapeptide neurons to rapidly upregulate peptide production in response to stressors on a much shorter timescale than has been observed in adult animals.

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“…In mice, Avp mRNA is found in the hypothalamus as early as E13.5, while AVPR1A binding is observed at P0 in the neocortex, as well as the septum, hippocampus, and VTA . So far, the data suggest that both AVP and AVPR1A expression tend to increase over the course of development, and that AVPR1A expression tends to shift in terms of its region‐specific expression . Perhaps due to these types of dynamic changes in the system, there have been few studies that have made comparisons across time points.…”

Section: Introductionmentioning

confidence: 99%

“…27 So far, the data suggest that both AVP and AVPR1A expression tend to increase over the course of development, and that AVPR1A expression tends to shift in terms of its region-specific expression. 21,27,28 Perhaps due to these types of dynamic changes in the system, there have been few studies that have made comparisons across time points. Even more scarce are studies that have compared males and females within the same study.…”

Section: Introductionmentioning

confidence: 99%

Subtle sex differences in vasopressin mRNA expression in the embryonic mouse brain

Aulino

Caldwell

2020

J Neuroendocrinology

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Arginine vasopressin (AVP) is a neuropeptide which acts centrally to modulate numerous social behaviors. One receptor subtype through which these effects occur is the AVP 1a receptor (AVPR1A). The modulatory effects of Avp via the AVPR1A varies by species as well as sex, since both AVP and the AVPR1A tend to be expressed more prominently in males. Beyond these neuromodulatory effects there are also indications that the AVP system may play a role in early development to, in part, organize sex‐specific neural circuitry that is important to sexually dimorphic social behaviors in adulthood. However, to date, AVP's role in early development is poorly understood, particularly with respect to its differential effect on males and females. In order to determine the timing and distribution of the AVP system in early brain development, we examined the brains of male and female C57BL/6J mice between embryonic day (E) 12.5 and postnatal day (P) 2 and quantified Avp and Avpr1a mRNA using qPCR and AVPR1A protein using receptor autoradiography. The mRNA for Avp was measurable in males and females starting at E14.5, with males producing more than females, while Avpr1a mRNA was found as early as E12.5, with no difference in expression between sexes. AVPR1A binding was observed in both sexes starting at E16.5, and while there were no observed sex differences, binding density and the number of neuroanatomical areas did increase over time. These data are significant as they provide the first whole‐brain characterization of the vasopressin system in the embryonic mouse. Further, these findings are consistent with data from other species, that have documented a sex difference in the vasopressin system during early brain formation.

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Quantitative mapping reveals age and sex differences in vasopressin, but not oxytocin, immunoreactivity in the rat social behavior neural network

Cited by 70 publications

References 107 publications

Interactions of sex and early life social experiences at two developmental stages shape nonapeptide receptor profiles

Interactions of sex and early life social experiences at two developmental stages shape nonapeptide receptor profiles

Rapid nonapeptide synthesis during a critical period of development in the prairie vole: plasticity of the paraventricular nucleus of the hypothalamus

Subtle sex differences in vasopressin mRNA expression in the embryonic mouse brain

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