Chronic social stress in puberty alters appetitive male sexual behavior and neural metabolic activity

Abstract

Repeated social subjugation in early puberty lowers testosterone levels. We used hamsters to investigate the effects of social subjugation on male sexual behavior and metabolic activity within neural systems controlling social and motivational behaviors. Subjugated animals were exposed daily to aggressive adult males in early puberty for postnatal days 28 to 42, while control animals were placed in empty clean cages. On postnatal day 45, they were tested for male sexual behavior in the presence of receptive female. Alternatively, they were tested for mate choice after placement at the base of a Y-maze containing a sexually receptive female in one tip of the maze and an ovariectomized one on the other. Social subjugation did not affect the capacity to mate with receptive females. Although control animals were fast to approach females and preferred ovariectomized individuals, subjugated animals stayed away from them and showed no preference. Cytochrome oxidase activity was reduced within the preoptic area and ventral tegmental area in subjugated hamsters. In addition, the correlation of metabolic activity of these areas with the bed nucleus of the stria terminalis and anterior parietal cortex changed significantly from positive in controls to negative in subjugated animals. These data show that at mid-puberty, while male hamsters are capable of mating, their appetitive sexual behavior is not fully mature and this aspect of male sexual behavior is responsive to social subjugation. Furthermore, metabolic activity and coordination of activity in brain areas related to sexual behavior and motivation were altered by social subjugation.

Keywords: Appetitive male sexual behavior; Behavioral development; Cytochrome oxidase activity; Preoptic area; Social defeat; Social subjugation; Ventral tegmental area.

Figure 1

Timeline of events from postnatal day 25 (P-25) to P-45 during appetitive behavior testing. The animals were weaned on P-25, exposed to daily social subjugation from P-28 to P-42, habituated to the Y-maze daily from P-40 to P-44 and tested with females on P-45.

Figure 2

Comparison between control and subjugated hamsters for different behavioral measures (Mean ± SEM) performed in each section of the Y-maze: start box, stem, arm with non- receptive female (NR Arm), arm with the receptive female (R Arm), proximity of the screen by the non receptive female (NR Screen), and proximity of screen by the receptive female (R Screen). The behaviors included duration of time in section of the maze, latency to enter the arms of the maze, locomotor activity (expressed as lines crossed), and duration of time spent performing olfactory investigations. Subjugated hamsters were exposed daily to aggressive males from postnatal day 28 (P-28) to P-42, while Controls were placed in empty clean cages. All tests were conducted at mid-puberty on P-45. Groups were compared for each section of the maze (Student t-tests; * p<0.05, ** p<0.01, *** p<0.001). Comparisons were also made between R and NR arms within the groups (Paired t-tests, a p<0.05).