Low Daytime Light Intensity Disrupts Male Copulatory Behavior, and Upregulates Medial Preoptic Area Steroid Hormone and Dopamine Receptor Expression, in a Diurnal Rodent Model of Seasonal Affective Disorder

Abstract

Seasonal affective disorder (SAD) involves a number of psychological and behavioral impairments that emerge during the low daytime light intensity associated with winter, but which remit during the high daytime light intensity associated with summer. One symptom frequently reported by SAD patients is reduced sexual interest and activity, but the endocrine and neural bases of this particular impairment during low daylight intensity is unknown. Using a diurnal laboratory rodent, the Nile grass rat (Arvicanthis niloticus), we determined how chronic housing under a 12:12 h day/night cycle involving dim low-intensity daylight (50 lux) or bright high-intensity daylight (1,000 lux) affects males' copulatory behavior, reproductive organ weight, and circulating testosterone. We also examined the expression of mRNAs for the aromatase enzyme, estrogen receptor 1 (ESR1), and androgen receptor (AR) in the medial preoptic area (mPOA; brain site involved in the sensory and hormonal control of copulation), and mRNAs for the dopamine (DA) D1 and D2 receptors in both the mPOA and nucleus accumbens (NAC; brain site involved in stimulus salience and motivation to respond to reward). Compared to male grass rats housed in high-intensity daylight, males in low-intensity daylight displayed fewer mounts and intromissions when interacting with females, but the groups did not differ in their testes or seminal vesicle weights, or in their circulating levels of testosterone. Males in low-intensity daylight unexpectedly had higher ESR1, AR and D1 receptor mRNA in the mPOA, but did not differ from high-intensity daylight males in D1 or D2 mRNA expression in the NAC. Reminiscent of humans with SAD, dim winter-like daylight intensity impairs aspects of sexual behavior in a male diurnal rodent. This effect is not due to reduced circulating testosterone and is associated with upregulation of mPOA steroid and DA receptors that may help maintain some sexual motivation and behavior under winter-like lighting conditions.

Keywords: hormones; light; medial preoptic area; nucleus accumbens; seasonal affective disorder; sexual behavior.

Figure 1

Behavioral response to dim daylight. Male grass rats were housed in bright daylight intensity (brLD) or dim daylight intensity (dimLD) and their (A) latency to sniff an estrus female, (B) latency to mount an estrus female, (C) frequency of mounts, and (D) frequency of intromissions is shown (Means ± SEMs). *p < 0.05.

Figure 2

Hormonal response to dim daylight. Circulating levels (Mean ± SEM) of testosterone in male grass rats housed in bright daylight intensity condition (brLD) or dim daylight intensity (dimLD) condition, and sacrificed during the day (hatched) or night (gray). ^#Significant main effect of time of day, p < 0.05.

Figure 3

Neural response to dim daylight. (A) Relative levels (Mean ± SEM) of mRNAs for aromatase (Arom), estrogen receptor 1 (ESR1), androgen receptor (AR), D1 and D2 in the medial preoptic area (mPOA) of male grass rats housed in bright daylight intensity condition (brLD) or dim daylight intensity (dimLD) condition. (B) Relative levels (Mean ± SEM) of mRNAs for D1 and D2 in the nucleus accumbens (NAC) of male grass rats housed in brLD or dimLD conditions. *p < 0.05.