The bed nucleus of the stria terminalis is critical for sexual solicitation, but not for opposite-sex odor preference, in female Syrian hamsters

Abstract

Successful reproduction in vertebrates depends critically upon a suite of precopulatory behaviors that occur prior to mating. In Syrian hamsters (Mesocricetus auratus), these behaviors include vaginal scent marking and preferential investigation of male odors. The neural regulation of vaginal marking and opposite-sex odor preference likely involves an interconnected set of steroid-sensitive nuclei that includes the medial amygdala (MA), the bed nucleus of the stria terminalis (BNST), and the medial preoptic area (MPOA). For example, lesions of MA eliminate opposite-sex odor preference and reduce overall levels of vaginal marking, whereas lesions of MPOA decrease vaginal marking in response to male odors. Although BNST is densely interconnected with both MA and MPOA, little is known about the role of BNST in female precopulatory behaviors. To address this question, females received either bilateral, excitotoxic lesions of BNST (BNST-X) or sham lesions (SHAM), and were tested for scent marking and for investigatory responses to male and female odors. Whereas SHAM females vaginal marked more to male odors than female odors on two days of the estrous cycle, BNST-X females marked at equivalent levels to both odors. This deficit is not due to alterations in social odor investigation, as both BNST-X and SHAM females investigated male odors more than female odors. Finally, BNST lesions did not generally disrupt the cyclic changes in reproductive behaviors that occur across the estrous cycle. Taken together, these results demonstrate that BNST is critical for the normal expression of solicitational behaviors by females in response to male odor stimuli.

Endogenous oxytocin is necessary for preferential Fos expression to male odors in the bed nucleus of the stria terminalis in female Syrian hamsters

“…We have found that injections of OTA into either MPOA-AH or BNST decreased vaginal marking to male, but not female odors (Martinez et al, 2010). Furthermore, in hamsters binding sites for oxytocin are present in BNST, but not MPOA-AH, (Dubois-Dauphin et al, 1992), and as mentioned above, lesions of BNST, but not MPOA, disrupt vaginal marking responses to sexual odors (Martinez and Petrulis, 2011, 2013). Considered together, it seems likely that oxytocin acts within BNST to regulate vaginal marking responses to male odors; however, the underlying mechanisms underlying this effect are not known.…”

“…Once the day of behavioral estrus was identified, the two cycle days prior to estrus were defined as diestrous day 2 and proestrus, respectively (Johnston, 1977). It has been our experience that this technique for determining estrous cycle stage correctly predicts the day of behavioral receptivity with perfect accuracy (Martinez and Petrulis, 2011, 2013). …”

“…This behavior deposits vaginal secretion such that ‘trails’ are formed along the ground as the animal scent marks throughout its environment (Lisk et al, 1983). Although females will vaginal mark in response to various types of stimuli, this behavior is preferentially directed towards males or their odors (Johnston, 1977; Martinez and Petrulis, 2011; Petrulis and Johnston, 1999; Petrulis et al, 1999), suggesting that vaginal marking may be particularly important for mate attraction. Indeed, the deposited vaginal secretion is highly attractive to male hamsters (Johnston and Schmidt, 1979; Johnston, 1974; Kwan and Johnston, 1980), and females deposit these marks in such a way as to direct the male to her nesting area (Lisk et al, 1983).…”

“…These areas also appear to be important for regulating the expression of vaginal marking. Lesions centered on MA decrease overall levels of vaginal marking (Petrulis and Johnston, 1999), whereas lesions of BNST specifically decrease vaginal marking in response to male, but not female odors (Martinez and Petrulis, 2011). In contrast, lesions of MPOA do not affect the expression of vaginal marking, although this area is important for other forms of proceptive behaviors in female hamsters (Floody, 1989; Martinez and Petrulis, 2013).…”

X-ray kinematics analysis of vaginal scent marking in female Syrian hamsters (Mesocricetus auratus)

“…Although studies have examined how hormones and odors stimulate vaginal marking both systemically and at the level of the forebrain [9–14], the descending motor control of vaginal marking is unknown. Unlike more complex social behaviors, vaginal marking is relatively simple and can be divided into several discrete and stereotyped behavioral events, including the lowering of the pelvis, deflection of the tail from the substrate, pelvic rotation and/or forward motion, and expulsion of vaginal secretion [4].…”