Role of the striatum and nucleus accumbens in paced copulatory behavior in the female rat

Abstract

Female rats engage in a series of approach and avoidance behaviors (pacing behavior) directed at the male in order to achieve a preferred rate of intromissions that make pregnancy more likely to occur with insemination. The striatum and nucleus accumbens have been implicated in the modulation of pacing behavior. It is unclear, however, whether these areas of the brain are necessary for the display of pacing behavior. To address this question, ovariectomized female rats received either bilateral quinolinic acid lesions of the striatum or nucleus accumbens or sham surgeries. After hormone priming, rats were allowed to engage in mating behaviors in an apparatus in which they could pace the rate of the copulatory bout. There was a significant reduction in pacing efficiency after striatal lesions, in that females were less likely to leave the male's side of the chamber after a contact. Animals with lesions of the nucleus accumbens that included the shell were more likely to avoid sexual interaction altogether than animals with control lesions. Therefore, it is concluded that the striatum and nucleus accumbens modulate specific aspects of pacing behavior in the female rat.

Introduction

Copulation in rats begins with a series of mounts and intromissions that ultimately lead to an ejaculation [1], [7], [8]. However, male and female rats differ in terms of the optimal rates at which these interactions occur. If the male controls the rate of copulation, he will intromit with a female at a relatively rapid rate. Females, however, will establish longer latencies between sexual contacts if given the opportunity [1], [2], [11], [16].

These seemingly inconsistent patterns of copulation are reconciled, however, under natural or semi-natural conditions. In the wild, rats engage in mating in groups of several females and males. Under these conditions, males achieve relatively rapid intromissions with different females. The females, in turn, engage in a series of approach and avoidance behaviors of the males to achieve their preferred rate of copulation [16]. The female's display of approach and avoidance behaviors, with proceptive behaviors (i.e. ear wiggling, hopping and darting), is known as pacing behavior [11].

Pacing behavior allows the female to control both the rate and duration of the copulatory bout [17]. It is important to note that each female has a preferred rate of copulation that is independent of the absolute amount of vaginocervical stimulation [14]. When vaginocervical stimulation is received at the preferred rate, a neuroendocrine reflex is triggered that makes pregnancy more likely [12], [16]. In the laboratory, female rats pace sexual behavior when testing occurs in an experimental apparatus, designed so the female can escape from the male after each contact. In such an apparatus, pacing is defined by two measures. The percent exits is the number of times a female leaves the male's side of the chamber after a given sexual stimulus. Return latency is the amount of time the female stays away from the male after the given stimulus. Pacing results in a pattern of behavior such that the percent exits and return latency increase, as sexual stimuli become more intense (mounts<intromissions<ejaculations; as discussed in Ref. [11]).

While many areas of the brain are likely to be important for pacing behavior, estrogen implants into the striatum and nucleus accumbens (NAcc) have been shown to differentially modulate percent exits and return latency, respectively [25]. Furthermore, increased dopamine (DA) activity has been reported to occur in both brain areas during sexual behavior in male and female rats [20], [21], [22], [23]. What is not known is whether the striatum and NAcc are necessary for pacing behavior to occur. The purpose of this study is to investigate this question.