The effects of stress on social preferences are sexually dimorphic in prairie voles.

DeVries, A. Courtney; DeVries, M B; Taymans, Susan E.; Carter, C S

doi:10.1073/pnas.93.21.11980

Cited by 213 publications

(191 citation statements)

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“…We also examined neural substrates involved in stress and anxiety, because alcohol is known to act as an anxiolytic and stress and corticosterone have been shown to stimulate PP in male prairie voles but to inhibit PP in female prairie voles (51). In agreement with alcohol's effect on decreasing anxiety, we find a decrease in the levels of CRF within the BNST after alcohol exposure.…”

Section: Discussionsupporting

confidence: 72%

“…To date, stress is the only mechanism that has shown opposite effects on PP in male and female prairie voles: A short swim stress before cohabitation, or administration of corticosterone, facilitated PP in males but inhibited it in females, whereas adrenalectomy reversed these effects (51). Combined with results from the present study indicating the sex-dependent effects of alcohol on neuropeptides and brain regions relevant to stress and anxiety, this evidence leads us to hypothesize that alcohol selfadministration during cohabitation acts as an anxiolytic, thereby facilitating PP in females but inhibiting it in males.…”

Section: Discussionmentioning

confidence: 99%

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Drinking alcohol has sex-dependent effects on pair bond formation in prairie voles

Anacker

Ahern

Hostetler³

et al. 2014

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

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Alcohol use and abuse profoundly influences a variety of behaviors, including social interactions. In some cases, it erodes social relationships; in others, it facilitates sociality. Here, we show that voluntary alcohol consumption can inhibit male partner preference (PP) formation (a laboratory proxy for pair bonding) in socially monogamous prairie voles (Microtus ochrogaster). Conversely, female PP is not inhibited, and may be facilitated by alcohol. Behavior and neurochemical analysis suggests that the effects of alcohol on social bonding are mediated by neural mechanisms regulating pair bond formation and not alcohol's effects on mating, locomotor, or aggressive behaviors. Several neuropeptide systems involved in the regulation of social behavior (especially neuropeptide Y and corticotropin-releasing factor) are modulated by alcohol drinking during cohabitation. These findings provide the first evidence to our knowledge that alcohol has a direct impact on the neural systems involved in social bonding in a sexspecific manner, providing an opportunity to explore the mechanisms by which alcohol affects social relationships.anxiety | ethanol | substance use | oxytocin | vasopressin P rairie voles are a valuable animal model of social monogamy. Males and female mates form durable bonds in the wild and in the laboratory (1, 2), and the neural mechanisms of social bonding delineated in this model species have translated with high predictive validity to humans (3, 4). In both species, social reward and drug reward show striking parallels at the behavioral and neurobiological levels (5-9). Prairie voles are now being used to explore the interactions between social relationships and drug abuse (10)(11)(12)(13)(14)(15)(16)(17)(18)(19).We previously demonstrated that prairie voles voluntarily selfadminister substantial amounts of alcohol (ethanol) and can influence the drinking patterns of a social partner (16)(17)(18)(19), similar to social drinking in humans (20). Because alcohol is known to influence social bonds in humans (21-24), we asked here whether alcohol consumption can affect the formation of adult social attachments in prairie voles. Adult male and female prairie voles were paired for 24 h and simultaneously given access to alcohol (10% ethanol by volume in water) and water or only water. They were then tested in the 3-h partner preference (PP) test (PPT), which has proved to be a remarkably sensitive assay for assessing the effects of genetics (25, 26), early social environment (27), and a range of pharmacological agents on social bond formation (28, 29).Results PP was first measured in female prairie voles that drank alcohol during cohabitation without mating. Animals consumed 12.48 ± 1.03 (mean ± SE) grams of alcohol per kilogram of body weight (g/kg) in the 24-h drinking period and showed a 58 ± 5.7% preference for alcohol. Analysis of behavior in the PPT revealed a significant effect of stimulus animal (partner or stranger) on huddling time [F(1,56) = 26.86, P < 0.0001]; no main effect of alcohol on tot...

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Section: Discussionsupporting

confidence: 72%

Section: Discussionmentioning

confidence: 99%

Drinking alcohol has sex-dependent effects on pair bond formation in prairie voles

Anacker

Ahern

Hostetler³

et al. 2014

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

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“…Rather than showing this preference, females in the 8 mg/ kg group spent significantly more time in contact with a stranger. Stranger preferences have also been previously demonstrated in female voles which were given exogenous corticosterone (DeVries et al, 1996). In both cases it is possible that state changes in these females (such as changes in emotionality or anxiety) caused them to avoid the familiar partner; however, the partner preference test provides the experimental animal with the option of avoiding either partner, thus avoiding social contact in general.…”

Section: Discussionmentioning

confidence: 97%

“…Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. (DeVries et al, 1996;DeVries and Villalba, 1997). OT may be particularly related to pair-bond formation and parenting behavior in female voles (Liu and Wang, 2003;Olazabal and Young, 2006), and is also associated with mating (Carter, 1992).…”

mentioning

confidence: 99%

Oxytocin has dose-dependent developmental effects on pair-bonding and alloparental care in female prairie voles

Bales¹,

Westerhuyzen²,

Lewis-Reese³

et al. 2007

Hormones and Behavior

157

108

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The present study examines the developmental consequences of neonatal exposure to oxytocin on adult social behaviors in female prairie voles (Microtus ochrogaster). Female neonates were injected within 24 hours of birth with isotonic saline or one of four dosages of oxytocin (OT). As adults, females were tested in an elevated plus-maze paradigm (a measure of anxiety and exploratory behavior), and for alloparental behavior and partner preferences. At 2 mg/kg OT, females took longer to approach pups, but were the only group to form a statistically significant within-group partner preference. At 4 mg/kg OT, females retrieved pups significantly more frequently but no longer displayed a partner preference; while females treated developmentally with 8 mg/kg spent significantly more time in side-to-side contact with a male stranger than any other treatment group. OT may have broad developmental consequences, but these effects are not linear and may both increase and decrease the propensity to display behaviors such as pair-bonding.The neuropeptide oxytocin (OT) has been implicated in social behavior in both male and female mammals. OT's peripheral effects include the induction of parturition and milk let-down, while central OT has been associated with the onset of maternal behavior (Pedersen and Prange Jr., 1979;Pedersen et al., 1982;Pedersen and Boccia, 2002), and other positive social behaviors such as pair-bonding (Insel and Hulihan, 1995;Carter and Altemus, 1997;Cho et al., 1999) and male parental care (Bales et al., 2004b). It is also becoming evident that manipulations of OT and a related peptide, arginine vasopressin (AVP) during the perinatal period of life can have life-long implications for social behavior and neuroendocrine function (Stribley and Carter, 1999;Diaz-Cabiale et al., 2000;Carter, 2003;Lipschitz et al., 2003). These exposures can be either endogenous, through responses to touch, warmth (Uvnas-Moberg, 1998) or perhaps through OT in breast milk (Leake et al., 1981); they could also be pharmacological, for example through use of pitocin or an oxytocin antagonist to manipulate labor (Husslein, 2002).In this context, we have begun to examine the consequences of OT manipulations in early life for subsequent social behaviors and neuroendocrine variables. Because we were particularly interested in the developmental control of social behaviors such as pair-bond formation and biparental behaviors, we chose to study the socially monogamous prairie vole (Microtus ochrogaster). In this species both males and females display parental care and form selective partner preferences indicative of pair-bonding, although the mechanisms for these behaviors Please direct correspondence to: Karen L. Bales, Dept. of Psychology, One Shields Ave., University of California, Davis, CA 95616. Ph: (530) 754−5890, Fax: (530) 752−2087, email: klbales@ucdavis.edu Publisher's Disclaimer: This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this e...

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“…Third, the VTA projects to [43] brain regions that have been implicated in pair bond formation such as the amygdala, lateral septum, prefrontal cortex, and NAcc [1,15,20,32,34,51], while brain regions implicated in pair bonding, in turn, can influence the VTA [17,18]. Finally, stress, which affects pair bonding in monogamous voles [16], also alters the activity of dopaminergic cells within the VTA [40]. Thus, the VTA may represent an important point of convergence for processes critical for pair bond formation.…”

Section: Introductionmentioning

confidence: 99%

Ventral tegmental area involvement in pair bonding in male prairie voles

Curtis

Wang

2005

Physiology & Behavior

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Dopamine is known to play a critical role in social attachment in monogamous voles. However, little is known about the neurochemical regulation of central dopamine release during pair bond formation. Here we examine the effects on partner preference formation in male prairie voles of neurochemical manipulations in the ventral tegmental area (VTA), a major source of dopamine to brain regions implicated in pair bonding. Administration of NBQX, an AMPA receptor antagonist, or bicuculline, a GABA receptor antagonist, into the VTA induced partner preferences within 6 h in the absence of mating. We also found that, after unilateral administration of NBQX into the VTA, neuronal activation, as indicated by the expression of the immediate early gene c-fos, was decreased in the nucleus accumbens, prefrontal cortex, and medial amygdala, but was unchanged in the lateral septum and in a control region, the arcuate nucleus. These results confirm a role for the VTA in partner preference formation in monogamous voles and extend the list of neurochemicals important in pair bonding to include glutamate and GABA. D

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The effects of stress on social preferences are sexually dimorphic in prairie voles.

Cited by 213 publications

References 28 publications

Drinking alcohol has sex-dependent effects on pair bond formation in prairie voles

Drinking alcohol has sex-dependent effects on pair bond formation in prairie voles

Oxytocin has dose-dependent developmental effects on pair-bonding and alloparental care in female prairie voles

Ventral tegmental area involvement in pair bonding in male prairie voles

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