Mating and social exposure induces an opioid-dependent conditioned place preference in male but not in female prairie voles (Microtus ochrogaster)

Abstract

In rodents, sexual stimulation induces a positive affective state that is evaluated by the conditioned place preference (CPP) test. Opioids are released during sexual behavior and modulate the rewarding properties of this behavior. Prairie voles (Microtus ochrogaster) are a socially monogamous species, in which copulation with cohabitation for 6h induces a pair bond. However, the mating-induced reward state that could contribute to the establishment of the long-term pair bond has not been evaluated in this species. The present study aimed to determine whether one ejaculation or cohabitation with mating for 6h is rewarding for voles. We also evaluated whether this state is opioid dependent. Our results demonstrate that mating with one ejaculation and social cohabitation with mating for 6h induce a CPP in males, while exposure to a sexually receptive female without mating did not induce CPP. In the female vole, mating until one ejaculation, social cohabitation with mating, or exposure to a male without physical interaction for 6h did not induce CPP. To evaluate whether the rewarding state in males is opioid dependent, the antagonist naloxone was injected i.p. The administration of naloxone blocked the rewarding state induced by one ejaculation and by social cohabitation with mating. Our results demonstrate that in the prairie vole, on the basis of the CPP in the testing conditions used here, the stimulation received with one ejaculation and the mating conditions that lead to pair bonding formation may be rewarding for males, and this reward state is opioid dependent.

Keywords: Conditioned place preference; Opioids and voles; Sexual reward; Social cohabitation with mating.

Fig. 1

Schematic representation of the experiments. Timeline of experiment 1 (A), 2 (B), and 3 (C–E). Females were ovariectomized and treated with estradiol benzoate (EB) for four consecutive days before the conditioned place preference test.

Fig. 2

Schematic representation of the sexual parameters in male voles. A) anogenital investigation; B) mount; C) intromission; D) ejaculation; and E) post-ejaculatory interval, time elapsed between the ejaculation and the first intromission after ejaculation.

Fig. 3

Time in the reinforced compartment in social exposure (Soc.Exp) and one ejaculation (1E) groups in male (A) and female voles (B). Data are expressed in seconds as the mean ± S.E.M. *Different from pretest in the same group. P < 0.05.

Fig. 4

Time in the reinforced compartment in control (C), social exposure (Soc.Exp), and social cohabitation with mating (SCM) groups in male (A) and female voles (B). Data are expressed in seconds as the mean ± S.E.M. *Different from pretest in the same group. P < 0.05.

Fig. 5

Time in the reinforced compartment in voles treated with morphine (M) or morphine plus naloxone (M + N). Data are expressed in seconds as the mean ± S.E.M. *Different from pretest in the same group. P < 0.05.

Fig. 6

Time in the reinforced compartment in different groups of voles. Control males treated with naloxone (C + N), males with social cohabitation with mating for 6 h plus NaCl injections (SCM + S), males that cohabitated and mated with a receptive female for 6 h and received three naloxone injections (SCM + N), and males that were allowed to mate until one ejaculation and received one naloxone injection (1E + N). Data are expressed in seconds as the mean ± S.E.M. *Different from pretest in the same group. P < 0.05.