The role of the medial preoptic area in appetitive and consummatory reproductive behaviors depends on sexual experience and odor volatility in male Syrian hamsters

Abstract

In Syrian hamsters (Mesocricetus auratus), the expression of reproductive behavior requires the perception and discrimination of sexual odors. The behavioral response to these odors is mediated by a network of ventral forebrain nuclei, including the medial preoptic area (MPOA). The role of MPOA in male copulatory behavior has been well-studied, but less is known about the role of MPOA in appetitive aspects of male reproductive behavior. Furthermore, many previous studies that examined the role of MPOA in reproductive behavior have used large lesions that damaged other nuclei near MPOA or fibers of passage within MPOA, making it difficult to attribute post-lesion deficits in reproductive behavior to MPOA specifically. Thus, the current study used discrete, excitotoxic lesions of MPOA to test the role of this nucleus in opposite-sex odor preference and copulatory behavior in both sexually-naïve and sexually-experienced males. Lesions of MPOA eliminated preference for volatile, opposite-sex odors in sexually-naïve, but not sexually-experienced, males. When males were allowed to contact the sexual odors, however, preference for female odors remained intact. Surprisingly, lesions of MPOA caused severe copulatory deficits only in sexually-naïve males, suggesting previous reports of copulatory deficits following MPOA lesions in sexually-experienced males were not due to damage to MPOA itself. Together, these results demonstrate that the role of MPOA in appetitive and consummatory aspects of reproductive behavior varies with the volatility of the sexual odors and the sexual experience of the male.

Figure 1. Lesion Reconstruction

a) Coronal sections through rostral to caudal extent of MPOA showing largest (light gray) and smallest (dark gray) lesions included in MPOA-X group. Immunohistochemical localization of neuronal nuclei (NeuN) protein was used to visualize cell loss in males with b) excitotoxic lesions of MPOA; some males also sustained damage to c) the most caudal portions of the posterior bed nucleus of the stria terminalis (pBNSTc) and were excluded from the MPOA-X lesion group. Measurements in mm relative to bregma, scale bars = 200 μm

Figure 2. Investigation Times for Non-Contact Preference Test

a) In sexually-naïve males, lesions of MPOA eliminated preference for opposite-sex odors, whereas b) preference for opposite-sex odors remained intact in sexually-experienced males. Dissimilar letters indicate significant differences in investigation duration within lesion group, P < 0.05. * indicates significant differences in investigation duration between lesion groups, P < 0.05. Data expressed as means ± standard error of means.

Figure 3. Investigation Times for Contact Preference Test

In a) sexually-naïve or b) sexually-experienced males, lesions of MPOA did not affect preference for opposite sex odors. Dissimilar letters indicate significant differences in investigation duration within lesion group, P < 0.05. Data expressed as means ± standard error of means.

Figure 4. Investigation Times for Odor Discrimination Test

Sexually-naïve SHAM and MPOA-X males both habituated their investigation to repeated presentations of male odors and increased their investigation to a subsequently presented female odor. * indicates a significant decrease between Male 1 and Male 4, P ≤ 0.05, # indicates a significant increase between Male 4 and Female, P < 0.05. Data expressed as means ± standard error of means.

Figure 5. Total number of Mating Events in NVE and EXP males

In sexually-naïve males, the proportion of MPOA-X males displaying mounts, intromissions, ejaculations, ectopic mounts, and long intromissions was significantly less than in SHAM males. b) In EXP males, the proportion of subjects displaying any mating event did not differ between SHAM and MPOA-X males. * indicates significant differences in proportions, P < 0.05. Data expressed as means ± standard error of means.

Figure 6. Total Durations of Mating Events in NVE and EXP males

a) In sexually-naïve males, the total duration of anogenital and head/body investigation did not differ between SHAM and MPOA-X males, but MPOA-X males spent significantly less time self-grooming than did SHAM males. b) In sexually-experienced males, the total duration of anogenital investigation, head/body investigation, and self-grooming did not differ between SHAM and MPOA-X males. * indicates significant differences between lesion groups, P < .05. Data expressed as means ± standard error of means.

Figure 7. Latencies to Mating Events in EXP males

Lesions of MPOA increased the latency to a) begin anogenital investigation and c) ejaculate in sexually-experienced males, although the latencies to display mounts, intromissions, and long intromissions did not differ between SHAM and MPOA-X males, * indicates P < 0.05. Data expressed as means ± standard error of means.