Sexually Dimorphic Vasopressin Cells Modulate Social Investigation and Communication in Sex-Specific Ways

Rigney, Nicole; Whylings, Jack; Mieda, Michihiro; Vries, Geert J. De; Petrulis, Aras

doi:10.1523/eneuro.0415-18.2019

Cited by 51 publications

(77 citation statements)

References 107 publications

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“…Blocking the OT receptor in the dorsolateral BNST reduced the acquisition of conditioned cued fear, but left the baseline startle and non-cued fear (background anxiety) intact 38 . Moreover, the ablation of AVP cells in the BNST of male mice reduced social investigation of other males, and increased their sucrose intake 39,40 . Indeed, the BNST receives OT and AVP projections from the paraventricular nucleus, but it also contains AVP and OT neurons.…”

Section: Discussionmentioning

confidence: 99%

Effects of neural estrogen receptor beta deletion on social and mood-related behaviors and underlying mechanisms in male mice

Dombret

Naulé

Trouillet

et al. 2020

Sci Rep

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Estradiol derived from neural aromatization of testosterone plays a key role in the organization and activation of neural structures underlying male behaviors. This study evaluated the contribution of the estrogen receptor (ER) β in estradiol-induced modulation of social and mood-related behaviors by using mice lacking the ERβ gene in the nervous system. Mutant males exhibited reduced social interaction with same-sex congeners and impaired aggressive behavior. They also displayed increased locomotor activity, and reduced or unaffected anxiety-state level in three paradigms. However, when mice were exposed to unescapable stress in the forced swim and tail suspension tests, they spent more time immobile and a reduced time in swimming and climbing. These behavioral alterations were associated with unaffected circadian and restraint stress-induced corticosterone levels, and unchanged number of tryptophan hydroxylase 2-immunoreactive neurons in the dorsal raphe. By contrast, reduced mRNA levels of oxytocin and arginine-vasopressin were observed in the bed nucleus of stria terminalis, whereas no changes were detected in the hypothalamic paraventricular nucleus. The neural ERβ is thus involved to different extent levels in social and mood-related behaviors, with a particular action on oxytocin and arginine-vasopressin signaling pathways of the bed nucleus of stria terminalis, yet the involvement of other brain areas cannot be excluded.aggressive behavior of mutant males can be observed in another behavioral test using a neutral testing cage 14 .Furthermore, yet another study on ERβ knockout males showed no impairment of social recognition memory 15 .Concerning mood-related behaviors, few studies have been conducted in male mice and rats. This either resulted in minor effects induced by global ERβ knockout in mice 16 , or significant changes following chronic administration of selective ERβ agonists or androgen metabolites acting at ERβ on the anxiety state level in rats [17][18][19] . By comparison, more studies are available on female behaviors and these all converge on the role of ERβ in mediating estradiol effects 6,16,[20][21][22][23] . This involves at least in part the maintenance of serotonergic neurons and regulation of the expression of tryptophan hydroxylase (TPH), the key enzyme involved in serotonin synthesis in the dorsal raphe 24 .In this context, the present work was undertaken in order to evaluate in the same study the neural role of ERβ in social and mood-related behaviors using male mice lacking the ERβ gene in the whole nervous system, without interference with peripheral effects of this receptor. For this purpose, control and mutant mice were subjected to behavioral tests that measure social interaction, anxiety-related behavior (elevated O-maze, dark-light box and open field), locomotor activity, despair-like behavior (forced swim and tail suspension tests), sucrose preference test, and aggressive behavior (resident-intruder test). Corticosterone levels were measured under basal circadian and induce...

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Section: Discussionmentioning

confidence: 99%

Effects of neural estrogen receptor beta deletion on social and mood-related behaviors and underlying mechanisms in male mice

Dombret

Naulé

Trouillet

et al. 2020

Sci Rep

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“…Importantly, ELS has been shown to alter postnatal circuit assembly in the BNST (Card, Levitt, Gluhovsky, & Rinaman, 2005), alter neuropeptide receptor kinetics in anterior regions of the BNST (Oliveira, Neumann, & de Jong, 2019), and influence the levels of neuropeptides such as OT and AVP in the BNST (Veenema & Neumann, 2009). ELS-altered neuropeptide levels in BNST could have implications for social behavioral expression because BNST AVP modulates social behavior in mice (Duque-Wilckens et al, 2016;Rigney, Whylings, Mieda, de Vries, & Petrulis, 2019), and studies have implicated OT in the anterior BNST in social motivation and social avoidance (Duque-Wilckens et al, 2018;Steinmann et al, 2016;Steinmann, Duque-Wilckens, & Trainor, 2019). While past studies have examined some aspects of ELS effects on BNST-mediated behaviors, the direct relationship between ELS-induced effects in the BNST and altered social behaviors is not fully understood.…”

Section: Introductionmentioning

confidence: 99%

Chemogenetic manipulation of the bed nucleus of the stria terminalis counteracts social behavioral deficits induced by early life stress in C57BL/6J mice

Emmons

Sadok

Rovero

et al. 2020

J of Neuroscience Research

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Trauma during critical periods of development can induce long‐lasting adverse effects. To study neural aberrations resulting from early life stress (ELS), many studies utilize rodent maternal separation, whereby pups are intermittently deprived of maternal care necessary for proper development. This can produce adulthood behavioral deficits related to anxiety, reward, and social behavior. The bed nucleus of the stria terminalis (BNST) encodes aspects of anxiety‐like and social behaviors, and also undergoes developmental maturation during the early postnatal period, rendering it vulnerable to effects of ELS. Mice underwent maternal separation (separation 4 hr/day during postnatal day (PD)2–5 and 8 hr/day on PD6‐16) with early weaning on PD17, which induced behavioral deficits in adulthood performance on two‐part social interaction task designed to test social motivation (choice between a same‐sex novel conspecific or an empty cup) and social novelty preference (choice between the original‐novel conspecific vs. a new‐novel conspecific). We used chemogenetics to non‐selectively silence or activate neurons in the BNST to examine its role in social motivation and social novelty preference, in mice with or without the history of ELS. Manipulation of BNST produced differing social behavior effects in non‐stressed versus ELS mice; social motivation was decreased in non‐stressed mice following BNST activation, but unchanged following BNST silencing, while ELS mice showed no change in social behavior after BNST activation, but exhibited enhancement of social motivation—for which they were deficient prior—following BNST silencing. Findings emphasize the BNST as a potential therapeutic target for social anxiety disorders instigated by childhood trauma.

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“…Changes in AVP signaling in the BNST, although not consistently found, can only be weakly linked to potential changes in aggression and social motivation. That is, administration of AVP in the BNST enhances aggression in one experimental group, whereas blocking AvpR1a in the BNST (Veenema et al, 2010), and lesioning BNST AVP neurons (Rigney et al, 2019) did not affect aggression in other studies. In females, however, blocking AvpR1a in the BNST reduced maternal aggression (Bosch et al, 2010).…”

Section: Causal Pathways Linking Es To Social Behaviormentioning

confidence: 85%

“…Changes in AVP are more consistently linked to social motivation. Lesioning BNST AVP neurons reduced social interaction in males, but not females in one study (Rigney et al, 2019), whereas an AvpR1a antagonist injected into the BNST reduced social motivation in both sexes in another (Duque-Wilckens et al, 2016). No changes in OXT in the BNST have been found after ES.…”

Section: Causal Pathways Linking Es To Social Behaviormentioning

confidence: 90%

“…These behaviors are at the very basis of more complex social behavior, and are often affected in psychiatric disorders that are associated with both ES and AVP/OXT (Blair, 2001; Blanchard et al, 2001; Robb, 2010; Soyka, 2011; Chevallier et al, 2012; Skuse et al, 2014) and can be and have been reliably assessed in rodents (Box 2) (Thompson et al, 2004; Kosfeld et al, 2005; Savaskan et al, 2008; Veenema and Neumann, 2008; Meyer-Lindenberg et al, 2011; Kelly and Goodson, 2014). Specifically, AVP in rodents has been found to generally promote inter-male aggression (Caldwell and Albers, 2004; Veenema et al, 2010; Terranova et al, 2017), facilitate social recognition (Bielsky et al, 2004, 2005; Veenema et al, 2012) and modulate social motivation and affiliation (Landgraf et al, 2003; Rigney et al, 2019). OXT also promotes social recognition (Ross and Young, 2009; Dumais et al, 2016; Oettl et al, 2016; Takayanagi et al, 2017), modulates social motivation and affiliation (Lukas et al, 2011b; Borland et al, 2019), and is an important regulator of maternal behavior (Olazábal and Young, 2006; Sabihi et al, 2014) and social learning (Choe et al, 2015; Nardou et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

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Early Life Adversity and Adult Social Behavior: Focus on Arginine Vasopressin and Oxytocin as Potential Mediators

Kompier

Keysers

Gazzola

et al. 2019

Front. Behav. Neurosci.

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Exposure to stress during the early postnatal period (i.e., early life stress, ES) can impact brain physiology and modify individual variability in adult social behavior. Arginine vasopressin (AVP) and oxytocin (OXT) are two centrally released neuropeptides that are involved in shaping essential social behaviors, like aggression, social recognition, and social motivation. AVP and OXT modulate activity in brain regions important for the establishment of social behavior, and may be particularly sensitive to ES. In this review, we discuss whether ES alters the characteristics of the AVP- and OXT- systems in rodents, and whether these changes are associated with later alterations in aggression, social recognition, and social motivation. We have integrated causal studies indicating that (1) ES affects AVP/OXT, and (2) that changing AVP/OXT in affected regions alters social behavior. Although there is encouraging evidence that ES causes AVP- and OXT-system changes, and that these may mediate social behavior, a comprehensive understanding of the exact nature of AVP- and OXT changes and whether they are causal in establishing these behavioral disturbances needs further investigation. As there are indications that ES alters AVP- and OXT characteristics in humans as well, and that these may interact with adult predisposition to psychopathology with social dysfunction, future rodent studies may lay ground for a better understanding of such changes in humans. Ultimately, this may assist in developing therapeutic strategies to target ES effects on social behavior.

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Sexually Dimorphic Vasopressin Cells Modulate Social Investigation and Communication in Sex-Specific Ways

Cited by 51 publications

References 107 publications

Effects of neural estrogen receptor beta deletion on social and mood-related behaviors and underlying mechanisms in male mice

Effects of neural estrogen receptor beta deletion on social and mood-related behaviors and underlying mechanisms in male mice

Chemogenetic manipulation of the bed nucleus of the stria terminalis counteracts social behavioral deficits induced by early life stress in C57BL/6J mice

Early Life Adversity and Adult Social Behavior: Focus on Arginine Vasopressin and Oxytocin as Potential Mediators

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