Ovarian Hormones Mediate Changes in Adaptive Choice and Motivation in Female Rats

Abstract

In female rodents, sexual receptivity is coordinated with cyclic changes in the release of gonadal hormones. Increases in estradiol (E) and progesterone (P) during proestrus and estrus not only induce ovulation but also modulate behaviors that increase the likelihood that the female will find a mate and reproduce. This includes changes in receptive behaviors, such as lordosis, as well as changes in appetitive or proceptive behaviors, including motivation. Interestingly, the direction of these changes in motivation is dependent on the type of reward that is being pursued. While induction of sexual receptivity by E and P increases motivation for access to a male, motivation for a palatable food reward is decreased. These concurrent changes may facilitate adaptive choice across the estrous cycle; females bias their choice for sex when fertilization is most likely to occur, but for food when copulation is unlikely to result in impregnation. In order to test this hypothesis, we developed a novel paradigm to measure the motivated choice between a palatable food reward and access to a male conspecific. Ovariectomized, hormone primed females were trained to operantly respond for both food and sex on a fixed interval (FI) schedule. After training, unprimed and primed females were tested in a chamber that allows them to choose between food and sex while still requiring responding on the FI schedule for reach reward. From this we can not only determine the impact of hormone priming on female choice for food or sex, but also how this is reflected by changes in motivation for each specific reward, as measured by the average number of responses made during each fixed interval. Induction of sexual receptivity by hormone priming biases choice toward sex over food and this change is accompanied by an increase in motivation for sex but a decrease in motivation for food. This work provides evidence in support of a novel framework for understanding how the release of ovarian hormones over the course of the estrous cycle modulates adaptive behavioral choice in females by directly assessing motivation via operant responding when multiple rewards are available.

Keywords: feeding; females; motivation; ovarian hormones; sexual behavior.

Figure 1

An operant paradigm for concurrent measurement of motivation for food and sex. Female rats were trained to respond for both food and sex on a 15 s fixed-interval (FI15) schedule. Activation of either active port initiated an FI15 for that specific reward (food or sex), and animals could only respond for access to the initially selected reward for the duration of the trial. Completion of the FI15 on the active port located adjacent to the food trough resulted in the delivery of a palatable food pellet (45 mg banana flavor, BioServ, Flemington, NJ, USA) accompanied by presentation of a discrete light cue for 1 s. Completion of the FI15 on the active port located adjacent to the door leading to the other chamber resulted in the door opening and presentation of a different light cue for 1 s. The door remained open until the female crossed into the male side to interact with the male and then closed upon her return to the female side. Failure to complete the FI15 did not result in reward delivery, and the next response made on either port would initiate a new trial.

Figure 2

Reproductive status biases choice for food vs. sex. Hormone treatment reduced the total number of trials that animals initiated (A), specifically by reducing the number of pellet trials (B). The proportion of mate or pellet trials that animals initiated was altered following hormone treatment (C). Animals initiated more mate trials when hormone primed than when unprimed, and more pellet trials when unprimed than when hormone primed. Changes in the proportion of pellet or mate trials that animals initiated were driven by increases in completed trials, without altering the total number of trials that animals failed (D). Although the total number of failed trials remained unchanged, changes in the corresponding number of completed trials resulted in a significant interaction between hormone treatment and trial type on the proportion of trials that animals failed (E). Data are shown as mean ± SEM. Data points represent within session means for individual animals, n = 8, within subject design. *p < 0.05, **p < 0.01, ***p < 0.001.

Figure 3

Hormone treatment alters the amount of time animals spend in pursuit of each reward. (A) Mate trials are on average longer than pellet trials, and trial length for both rewards is increased in after hormone priming. (B) The total amount of time that animals spent engaged in mate trials was increased following hormone priming, which was accompanied by a decrease in the amount of time spent engaged in pellet trials. Data are shown as mean ± SEM. Data points represent within-session means for individual animals, n = 8, within-subject design. *p < 0.05.

Figure 4

Hormone priming increases motivation for sex while simultaneously decreasing motivation for palatable food reward. The effect of hormone priming on motivated responding is dependent on the reward being pursued (A). Unprimed animals show greater motivation for food than for access to a mate. Induction of sexual receptivity by hormone priming reduces motivation for food, but increases motivation for access to a mate, resulting in similar levels of motivated responding for both rewards. The effect of hormone priming on motivated responding is not mediated by changes in overall locomotor behavior, as there was no effect of hormone priming on the number of responses made on the inactive ports (B). Hormone priming specifically increased responding during completed mate trials, without changing the number of active mate responses during failed trials (C). Similarly, hormone priming only reduced responding for pellet during completed pellet trials, but not during failed pellet trials (D). Although responding for the active reward was not altered during failed trials, hormone primed animals made more responses for the inactive reward during failed trials than completed trials during both mate (E) and pellet (F) trials. Both primed and unprimed animals made more responses for the alternate reward during failed trials when compared to all trials that were initiated. Data are shown as mean ± SEM. Data points represent within-session means for individual animals, n = 8, within-subject design. *p < 0.05, **p < 0.01, ***p < 0.001.

Figure 5

Motivation for access to a mate decreases following ejaculation in sexually receptive female rats. (A) Motivation for access to a mate was attenuated during three trials following ejaculation. (B) As expected, only sexually receptive animals engaged in sexual behavior. Data are shown as mean ± SEM. For panel (A), data are shown as mean n = 12 across eight animals. For panel (B), data shown are mean ± SEM, n = 8, within-subject design. *p < 0.05, **p < 0.01.

Figure 6

Changes in motivation for food over time. (A) Motivation for food increases significantly in over the course of each session in ovariectomized female rats. (B) Primed females do not increase their motivation for food from the beginning to the end of each session. Data represent the number of responses during individual trials, n = 56 across eight animals for unprimed trials and n = 23 across eight animals for primed trials.

Figure 7

Hormone priming alters the behavior of female rats within the chamber. (A) Females spent a similar amount of time in the female (instrumental) compartment regardless of hormone treatment. (B) However, when females were given access to the male chamber, hormone primed animals spent more time with the male, while unprimed animals spent more time in the doorway, out of reach of the male. (C) Hormone priming altered the distribution of time that animals spent engaging in various aspects of the task. (D) Hormone primed animals spent a similar amount of time engaging with the mate paired cue, active mate port, and door, but reduced the amount of time they spent engaging with the food paired cue, active food port, and food trough. This was true when considering the amount of time animals engaged with each aspect of the apparatus individually for both mate (E) and food (F) paired cues. For panels (A,B,D), data are shown as mean ± SEM, n = 8, within-subject design. Mean values are used in panel (C). In panels (E,F), bars represent mean values and data points for individual values, connected to indicate within-subject changes. *p < 0.05, **p < 0.01, ***p < 0.001.