Mating is a socially rewarding experience that may exert protective benefits to health and fitness and buffers against the deleterious effects of stress across a number of mammalian and non-mammalian species. However, the neurobiological mechanisms that underlie these effects are poorly understood, and studies inclusive of female subjects are extremely limited. Using both male and female rodent models, the investigators will utilize a combination of behavioral, cellular, and neurochemical studies to better understand the impact of mating history on stress-related systems. In-vivo neurochemical studies will also allow for the collection and analysis of neurotransmitter release in awake and behaving animals during mating and a stressful encounter. Mating history is expected to dampen stress reactivity through neurochemical changes in regions of the brain that differ between males and females, and differences may be observed between males and females. The evolutionary advantage for the anxiety-reducing, stress-buffering, and rewarding aspects of mating may be to increase an animal's willingness to explore new environments to search for mating partners, and thus facilitate reproduction and ultimately pass on its genes. This research will advance a broader scientific field that includes our understanding of differences between males and females and similarities in the behavioral and neurobiological systems regulating stress and reproduction and how these systems interact. In addition, it will have a broader impact on a number of undergraduates who are trained in neuroscience research in this lab. These students currently include members of groups traditionally underrepresented in science. Further, the investigators will talk to K-12 students about the dissertation research and teach basic neuroscience through outreach activities including Brain Awareness Week and the North Florida Brain Bee, to promote scientific interest in the local community.

Project Report

Dissertation Research: Jenna A. McHenry Faculty Advisor: Elaine M. Hull Mating is a socially rewarding experience that yields protective benefits to health, confers resistance to stress, and lowers anxiety-like behaviors in a number of mammalian species. Preliminary data for this project showed that repeated mating by male rats resulted in their showing less anxiety-like behavior in several behavioral tests and also decreased their neuronal stress responses following restraint in a plastic tube for 30 minutes. In addition, androgen receptors in a brain area that is critical for male sexual behavior, the medial preoptic area (MPOA), contribute to the stress-reducing effects of mating. The funded research added to this picture by clarifying a neural mechanism for these effects and by extending them to female rats. In one preliminary experiment, restraint stress caused less neural activation in neurons in the paraventricular nucleus (PVN), which controls hormonal stress responses and which is located about 1 millimeter behind the MPOA. The PVN of sexually experienced males also contained fewer neurons that contained corticotropin releasing hormone (CRH), which ultimately elicits the release of corticosterone, the rat equivalent of the stress hormone cortisol. In addition, fewer of the CRH-containing neurons were activated by restraint stress in the sexually experienced males. Therefore, sexual experience dampened hormonal stress responsiveness. Much of the funded research examined the neural mechanisms of that stress reduction. First, a new behavioral test was added: the novelty-induced hypophagia test. Male rats were initially given peanut butter-flavored pieces of candy in their home cage; all animals quickly consumed all of the candy pieces. Then the candy pieces were placed in the middle of a large plastic enclosure. All of the sexually experienced males, but only half of the sexually naïve males retrieved the candies, and those that did, took about twice as long to consume them as did the experienced males. Next, an experiment examined the functional characteristics of neural projections from the MPOA to the PVN. We had hoped to use microdialysis to detect the inhibitory neurotransmitter GABA released in the PVN during restraint stress in sexually experienced and naïve males. However, the high-performance liquid chromatography equipment used to detect GABA in dialysate from the PVN was not functioning properly. Therefore, we first tested whether neurons that project from the MPOA to the PVN are activated by mating and whether they also contain androgen receptors. A preliminary experiment showed that androgen receptors in the MPOA were necessary for mating to decrease the responsiveness of PVN neurons to restraint stress. Indeed, some neural projections from the MPOA to the PVN were activated by mating (i.e., produced a protein that would have activated gene transcription). Further, more than half of these projections contained androgen receptors, and some androgen receptor-containing neurons were also GABAergic. Another experiment showed that repeated mating increased the number of androgen receptors in the MPOA. Therefore, one way in which mating decreases stress responsiveness may be via GABAergic neurons in the MPOA that are activated by mating, contain increased numbers of androgen receptors, and project to (and inhibit) stress-related neurons in the PVN. Finally, plasma levels of the stress hormone corticosterone (analogous to cortisol in humans) were measured after restraint stress in sexually experienced or naïve males. Males were given repeated mating experiences, and either 4 hours or 2 days after the last mating experience, they were restrained in a plastic tube for 30 minutes. Sexually naïve males were only handled according to the same schedule as mating, as a control. Sexually experienced males that also mated on the day of the stressor had lower corticosterone levels than did the naïve males. Experienced males that did not mate on that day had intermediate levels that were not significantly different from either the controls or experienced males that mated on the day of the stressor. Therefore, both previous and recent mating experience contribute to reduction of stress hormones. Finally, female rats were allowed to control the pace of mating by passing through a hole that was large enough for the female, but not for the larger male, to go through. Indeed, paced-mating did decrease the latency to consume the candies in the novelty-induced hypophagia test described above. It also increased the amount of candy consumed. Finally, sexually experienced females displayed less restraint stress-induced activation of PVN neurons. Therefore, mating can decrease both behavioral and neuronal stress responsiveness in both males and females. This research illustrates how an animal’s reproductive history may affect its willingness to explore new environments to find a mating partner and thus pass on its genes.

Agency
National Science Foundation (NSF)
Institute
Division of Integrative Organismal Systems (IOS)
Type
Standard Grant (Standard)
Application #
1311145
Program Officer
tamra mendelson
Project Start
Project End
Budget Start
2013-08-01
Budget End
2014-07-31
Support Year
Fiscal Year
2013
Total Cost
$19,110
Indirect Cost
Name
Florida State University
Department
Type
DUNS #
City
Tallahassee
State
FL
Country
United States
Zip Code
32306