Lateral septum DREADD activation alters male prairie vole prosocial and antisocial behaviors, not partner preferences

Sailer, Lindsay L.; Park, Ashley H.; Galvez, Abigail; Ophir, Alexander G.

doi:10.1038/s42003-022-04274-z

Cited by 10 publications

(3 citation statements)

References 67 publications

(87 reference statements)

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“…This finding is consistent with the context-dependent selective display of aggression in both sexes of these species: meadow voles show territorial aggression during the long days of the reproductive season, while prairie voles are aggressive towards strangers only following pair bond formation (Lee and Beery, 2022). Indeed, in prairie voles, activation of the LS in pair bonded males decreases aggression towards novel conspecifics (Sailer et al, 2022). It will be interesting to determine how neural activity within CA2 to LS projections is altered in different environmental, hormonal, or social contexts.…”

Section: Species Differences In Gonadal Hormone Receptor Expressionsupporting

confidence: 87%

Comparative analysis of gonadal hormone receptor expression in the house mouse, meadow vole, and prairie vole brain

Tollkühn

Denney

et al. 2023

Preprint

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The socially monogamous prairie vole (Microtus ochrogaster) and promiscuous meadow vole (Microtus pennsylvanicus) are closely related, but only prairie voles display long-lasting pair bonds, biparental care, and selective aggression towards unfamiliar individuals after pair bonding. These social behaviors in mammals are largely mediated by steroid hormone signaling in the social behavior network (SBN) of the brain. Hormone receptors are reproducible markers of sex differences that can provide more information than anatomy alone, and can even be at odds with anatomical dimorphisms. We reasoned that behaviors associated with social monogamy in prairie voles may emerge in part from unique expression patterns of steroid hormone receptors in this species, and that these expression patterns would be more similar across males and females in prairie than in meadow voles or the laboratory mouse. To obtain insight into steroid hormone signaling in the developing prairie vole brain, we assessed expression of estrogen receptor alpha (Esr1), estrogen receptor beta (Esr2), and androgen receptor (Ar) within the SBN, usingin situhybridization at postnatal day 14 in mice, meadow, and prairie voles. We found species-specific patterns of hormone receptor expression in the hippocampus and ventromedial hypothalamus, as well as species differences in the sex bias of these markers in the principal nucleus of the bed nucleus of the stria terminalis. These findings suggest the observed differences in gonadal hormone receptor expression may underlie species differences in the display of social behaviors.

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Section: Species Differences In Gonadal Hormone Receptor Expressionsupporting

confidence: 87%

Comparative analysis of gonadal hormone receptor expression in the house mouse, meadow vole, and prairie vole brain

Tollkühn

Denney

et al. 2023

Preprint

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“…Unfortunately, little is known about the mating system of pouched rats, though it seems unlikely that pouched rats demonstrate a socially monogamous mating system such as the one employed by prairie voles ( 62 ). On the other hand, coordination between BST-LS neural function might have more to do with how sociable an animal is (e.g., 63 – 65 ). Naked-mole rats are highly social (typically characterized as eusocial), and the asynchrony in OTR density in the LS and BST might play an important role in modulating this behavior ( 10 ).…”

Section: Discussionmentioning

confidence: 99%

Characterization of oxytocin and vasopressin receptors in the Southern giant pouched rat and comparison to other rodents

Freeman,

Arenas,

Lee

et al. 2024

Front. Endocrinol.

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Vasopressin and oxytocin are well known and evolutionarily ancient modulators of social behavior. The distribution and relative densities of vasopressin and oxytocin receptors are known to modulate the sensitivity to these signaling molecules. Comparative work is needed to determine which neural networks have been conserved and modified over evolutionary time, and which social behaviors are commonly modulated by nonapeptide signaling. To this end, we used receptor autoradiography to determine the distribution of vasopressin 1a and oxytocin receptors in the Southern giant pouched rat (Cricetomys ansorgei) brain, and to assess the relative densities of these receptors in specific brain regions. We then compared the relative receptor pattern to 23 other species of rodents using a multivariate ANOVA. Pouched rat receptor patterns were strikingly similar to hamsters and voles overall, despite the variation in social organization among species. Uniquely, the pouched rat had dense vasopressin 1a receptor binding in the caudate-putamen (i.e., striatum), an area that might impact affiliative behavior in this species. In contrast, the pouched rat had relatively little oxytocin receptor binding in much of the anterior forebrain. Notably, however, oxytocin receptor binding demonstrated extremely dense binding in the bed nucleus of the stria terminalis, which is associated with the modulation of several social behaviors and a central hub of the social decision-making network. Examination of the nonapeptide system has the potential to reveal insights into species-specific behaviors and general themes in the modulation of social behavior.

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“…Depression-like behavior following viral knockdown of OXTR expression in nucleus accumbens also suggests a potential role of this brain region in expression of other indices of pair bonding [ 60 ]. On the other hand, chemogenetic activation of the lateral septum in male prairie voles increased non-specific affiliative behavior and acquisition of pair bonding, but decreased selective aggression, an index of expression of pair bonding [ 85 ]. The latter observation suggest that varied brain regions could be involved in regulation of not only different phases of pair bonding but also different behaviors associated with pair bonding.…”

Section: Discussionmentioning

confidence: 99%

Effects of oxytocin receptor agonism on acquisition and expression of pair bonding in male prairie voles

Johnson,

Zweig,

Zhang

et al. 2024

Transl Psychiatry

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There is much interest in targeting the activity in the oxytocin system to regulate social bonding. However, studies with exogenous administration of oxytocin face the caveats of its low stability, poor brain permeability and insufficient receptor specificity. The use of a small-molecule oxytocin receptor-specific agonist could overcome these caveats. Prior to testing the potential effects of a brain-penetrant oxytocin receptor agonist in clinical settings, it is important to assess how such an agonist would affect social bonds in animal models. The facultatively monogamous prairie voles (Microtus ochrogaster), capable of forming long-term social attachments between adult individuals, are an ideal rodent model for such testing. Therefore, in a series of experiments we investigated the effects of the recently developed oxytocin receptor-specific agonist LIT-001 on the acquisition and expression of partner preference, a well-established model of pair bonding, in prairie voles. LIT-001 (10 mg/kg, intraperitoneal), as expected, facilitated the acquisition of partner preference when administered prior to a 4hr cohabitation. In contrast, while animals injected with vehicle after the 4hr cohabitation exhibited significant partner preference, animals that were injected with LIT-001 did not show such partner preference. This result suggests that OXTR activation during expression of pair bonding can inhibit partner preference. The difference in effects of LIT-001 on acquisition versus expression was not due to basal differences in partner preference between the experiments, as LIT-001 had no significant effects on expression of partner preference if administered following a shorter (2hr-long) cohabitation. Instead, this difference agrees with the hypothesis that the activation of oxytocin receptors acts as a signal of presence of a social partner. Our results indicate that the effects of pharmacological activation of oxytocin receptors crucially depend on the phase of social attachments.

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Lateral septum DREADD activation alters male prairie vole prosocial and antisocial behaviors, not partner preferences

Cited by 10 publications

References 67 publications

Comparative analysis of gonadal hormone receptor expression in the house mouse, meadow vole, and prairie vole brain

Comparative analysis of gonadal hormone receptor expression in the house mouse, meadow vole, and prairie vole brain

Characterization of oxytocin and vasopressin receptors in the Southern giant pouched rat and comparison to other rodents

Effects of oxytocin receptor agonism on acquisition and expression of pair bonding in male prairie voles

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