Estrogen Receptor-α in the Bed Nucleus of the Stria Terminalis Regulates Social Affiliation in Male Prairie Voles (Microtus ochrogaster)

Abstract

Estrogen receptor alpha (ERα) typically masculinizes male behavior, while low levels of ERα in the medial amygdala (MeA) and the bed nucleus of the stria terminalis (BST) are associated with high levels of male prosocial behavior. In the males of the highly social prairie vole (Microtus ochrogaster), increasing ERα in the MeA inhibited the expression of spontaneous alloparental behavior and produced a preference for novel females. To test for the effects of increased ERα in the BST, a viral vector was used to enhance ERα expression in the BST of adult male prairie voles. Following treatment, adult males were tested for alloparental behavior with 1–3-day-old pups, and for heterosexual social preference and affiliation. Treatment did not affect alloparental behavior as 73% of ERα-BST males and 62.5% of control males were alloparental. Increasing ERα in the BST affected heterosexual affiliation, with ERα-BST males spending significantly less total time in side-by-side contact with females relative to time spent with control males. ERα-BST males did not show a preference for either the familiar or novel female. These findings differed significantly from those reported in ERα-MeA enhanced males, where ERα inhibited alloparental behavior and produced a preference for a novel female. The findings from this study suggest two things: first, that increased ERα in the BST decreases social affiliation and second, that altering ERα in different regions of the social neural circuit differentially impacts the expression of social behavior.

Chronic social isolation enhances reproduction in the monogamous prairie vole (Microtus ochrogaster)

“…In socially monogamous prairie and pine ( M. pinetorum ) voles, ERα expression in the MEApd and BSTpm is sexually dimorphic (Cushing et al 2004, Cushing and Wynne-Edwards 2006) and low levels are “necessary” for the expression of prosocial behavior in males (Cushing et al 2008, Lei et al 2010). Males of these species also display relatively longer EL and PEI compared to the closely-related polygynous montane ( M. montanus ) and meadow ( M. pennsylvanicus ) voles (Dewsbury, 1973; 1976; Gray and Dewsbury, 1973).…”

“…A comparison of polygynous and monogamous species shows this to be a general pattern (Cushing and Wynne-Edwards, 2006; Wu et al, 2010). Additionally, increasing ERα expression in the MEApd or BSTpm of IL males significantly reduced prosocial behavior (Cushing et al, 2008; Lei et al, 2010), whereas down-regulation of hypothalamic ERα expression reduces sexual activity in female rats (Spiteri et al, 2012). A role for TH neurons in the MEApd and BSTpm in sociosexual organization has also been inferred, as polygynous species possess fewer TH neurons in these regions than monogamous species, which project primarily to the MPOA and are activated by sociosexual stimuli (Cavanaugh and Lonstein, 2010; Northcutt and Lonstein, 2011; Northcutt et al, 2006).…”

A Novel Model for Neuroendocrine Toxicology: Neurobehavioral Effects of BPA Exposure in a Prosocial Species, the Prairie Vole (Microtus ochrogaster)

“…The distribution of ER␣ differs across social and nonsocial species and plays a significant role in regulating speciesspecific sociality (93). Increased ER␣ in the pBNST, for example, reduces male prosocial behaviors (13,94). The male prairie vole pBNST is also richly populated with TH-ir cells, some of which are colocalized with ER␣.…”

Paternal Care in Biparental Rodents: Intra- and Inter-individual Variation

“…Few other studies have investigated effects of estrogen on allopaternal or paternal behavior in juvenile or adult males. In prairie voles, however, Cushing et al (2008) found that experimentally increasing the expression of estrogen receptor a (ERa) in the medial amygdala (MeA) via a viral vector inhibited parental behavior in adult males, while increasing ERa expression in the bed nucleus of the stria terminalis (BNST) had no effect (Lei et al 2010).…”