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.

Figure 1

Timeline and Testing Apparatus. A. Timeline of behavioral testing and surgeries in experiment. D2=diestrous day 2; PE=proestrus. B. Side view of testing apparatus for Scent marking tests. C. Top-down view of apparatus used for Odor investigation tests.

Figure 2

Lesion Reconstruction. A. Coronal sections depicting largest (light gray) and smallest (dark gray) excitotoxic lesion damage in bed nucleus of the stria terminalis of female hamsters included in the BNST-X group. Sections are organized from anterior (top) to posterior (bottom), all relative to bregma. Neuronal damage was visualized following immunohistochemistry for NeuN for both (B) SHAM and (C) BNST-X subjects. In all cases, damage depicted on atlas plates that comprised less than 50% of BNST was derived from females with greater than 50% damage to BNST on two other consecutive plates (see Results section). Scale bar = 200 μM. 3V=third ventricle;LV=lateral ventricle; ac=anterior commissure; sm=stria medullaris; f=fornix.

Figure 3

Mean (± SEM) Number of Vaginal Marks to Male and Female Odors. SHAM, but not BNST-X, females preferentially marked at higher levels to male odors compared to female odors on both (A) diestrous day 2, and (B) proestrus. * p < .01, male vs. female odor condition.

Figure 4

Median (± IQR) Duration of Odor Investigation. Subjects investigated male odors more than female odors, irrespective of lesion condition, in both the (A) Non-contact and (B) Contact tests. * p < .01, male vs. female within each test.