Review
Hypothalamic interaction with the mesolimbic DA system in the control of the maternal and sexual behaviors in rats

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Abstract

The medial preoptic area (MPOA) of the hypothalamus regulates maternal behavior, male sexual behavior, and female sexual behavior. Functional neuroanatomical evidence indicates that the appetitive aspects of maternal behavior are regulated through MPOA interactions with the mesolimbic dopamine (DA) system; a major focus of this review is to explore whether or not the MPOA participates in the appetitive aspects of sexual behavior via its interaction with the mesolimbic DA system. A second focus of this review is to examine the extent to which estradiol interactions with DA within this circuit regulate all three reproductive behaviors. One mechanism through which estradiol activates male sexual behavior is through the potentiation of DA activity in the MPOA. In the hypothalamus, estradiol has also been found to act in concert with DA, through the activation of similar intracellular signaling pathways, in order to stimulate female sexual behavior. Finally, recent evidence suggests that some effects of estradiol are mediated by direct action of estradiol on the mesolimbic DA system.

Research highlights

▶ Hypothalamic input to mesolimbic dopamine system affects reproductive behaviors. ▶ Distinct hypothalamic output systems regulate appetitive and consummatory behaviors. ▶ Estrogen influences reproductive behavior via genomic and nongenomic effects. ▶ Estradiol and dopamine interact to affect reproductive behavior.

Introduction

Reproductive behaviors, as well as other motivated behaviors, were dichotomized by early ethologists into appetitive and consummatory components based on the observation that reproductive behavior began with an anticipatory stage and terminated with a final or fulfilling stage (Ball and Balthazart, 2008, Craig, 1918). The initial phase of attraction and pursuit, termed the appetitive phase, is comprised of behaviors that bring an organism into contact with a goal stimulus, and is followed by the final phase of consummation, or the consummatory phase, in which the organism interacts with the acquired stimulus.

The hypothalamus is the neural region credited with the regulation of behaviors that are essential for survival of the organism or survival of the species (Swanson, 1987). It is sensitive to the internal environment (for example, fluctuations in hormone release) and receives inputs from most sensory modalities (Risold et al., 1997, Simerly and Swanson, 1986). One view of hypothalamic function is that distinct nuclei within the hypothalamus can become receptive to particular external stimuli, depending on the internal environment, and then respond to these external stimuli by activating motor systems to initiate behavioral responsiveness (Numan, 2006, Stellar, 1954). In this way, the hypothalamus might be conceived of as gating the types of stimuli that elicit responses at certain time points by modulating a sensory-motor integration apparatus. We propose that the regulation of the appetitive and consummatory aspects of maternal behavior and sexual behaviors most likely corresponds to distinct hypothalamic output systems, with a consummatory output descending to the brainstem and spinal cord to promote relatively stereotyped and reflexive motor patterns, and an appetitive output ascending to the telencephalon to initiate more complex goal-directed responses (Numan and Insel, 2003, Risold et al., 1997).

In what follows, we will present a general model to explain how hypothalamic efferents may regulate the appetitive and consummatory aspects of reproductive behaviors in rodents (see Fig. 1). While it is important to distinguish hypothalamic projections that regulate consummatory aspects of reproductive behavior from those that regulate appetitive responses, a major objective of this review is to examine MPOA and mesolimbic DA interactions and their role in the appetitive aspects of maternal and sexual behavior in rodents (see Fig. 1). In particular, we will emphasize the importance of MPOA projections to ventral tegmental area (VTA) DA neurons that project to the nucleus accumbens (NA) in the telencephalon. In order to evaluate this proposal we begin with an overview of appetitive and consummatory aspects of reproductive behaviors and a description of the neuroanatomical basis of the proposed model. Evidence will be presented which suggests that steroid hormones might act at level of the hypothalamus as well as the mesolimbic DA system to influence reproductive behavior. The literature will be examined with respect to each reproductive behavior in order to evaluate the evidence which supports our proposed model.

Section snippets

Appetitive and consummatory aspects of reproductive behavior

In the context of maternal behavior, mother rats display both appetitive and consummatory behaviors to ensure the survival of the young. After giving birth, female rats naturally respond to their infants by building a nest and crouching over the poikilothermic pups, allowing them to suckle and receive milk. Females lick and groom pups, which aids in urination and defecation, and has been found to impact their emotional and social development (Champagne and Curley, 2009). Should pups become

A proposed neural model

The evidence necessary to support the aspect of our model that proposes that MPOA projections to the mesolimbic DA system promote the appetitive aspects of maternal and sexual behaviors (see Fig. 1) can be organized as follows: (1) neuroanatomical data should support the idea that the MPOA projects to the VTA; (2) behavioral evidence should indicate that the mesolimbic DA system mediates the appetitive components of reproductive behavior; (3) if DA release into NA is directed via the output of

Hormonal mediation of maternal behavior in the rat

Wiesner and Sheard (1933) were the first to determine that parturient female rats display maternal behavior toward both biological and foster offspring, whereas virgin females do not. This distinction indicates the significance of the hormonal events of pregnancy and parturition in the stimulation of maternal behavior. However, in the absence of hormonal inputs the virgin rat is still capable of displaying maternal behavior; these females just require much more exposure to pups to elicit

Hormonal mediation of male sexual behavior in the rat

Male sexual behavior is highly dependent upon hormones. The testes secrete constant levels of androgens, including the primary male sex hormone, testosterone (T). The absence of T interferes with both the appetitive and consummatory aspects of male sexual behavior (Everitt, 1990). Castrated males are still capable of copulating for about two weeks after castration, after which expression of sexual behavior is highly variable and subsequently declines. Administration of T to a castrated male

Hormonal mediation of female sexual behavior in the rat

Female sexual behavior in rodents only occurs near the time of ovulation, in the presence of hormones (Pfaff and Schwartz-Giblin, 1988). The estrous cycle of the female rat has the following general characteristics (Freeman, 1994): Blood estradiol levels peak during the late morning of vaginal proestrus which contributes to the occurrence of a surge of lutenizing hormone from the anterior pituituary on the afternoon of proestrus, followed by a peak in ovarian progesterone secretion on the

Conclusions

One focus of this review has been to apply our model of MPOA interaction with the mesolimbic DA system in the regulation of appetitive maternal behavior to other reproductive behaviors: male and female sexual behavior in rodents. One implication of this proposal is that the MPOA to VTA projection, which has been found to regulate the appetitive aspects of maternal behavior, at least as measured through the retrieval response, is not specific for maternal behavior, but rather may be part of a

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