Differential control of appetitive and consummatory sexual behavior by neuroestrogens in male quail

Abstract

Contribution to Special Issue on Fast effects of steroids. Estrogens exert pleiotropic effects on multiple physiological and behavioral traits including sexual behavior. These effects are classically mediated via binding to nuclear receptors and subsequent regulation of target gene transcription. Estrogens also affect neuronal activity and cell-signaling pathways via faster, membrane-initiated events. Although the distinction between appetitive and consummatory aspects of sexual behavior has been criticized, this distinction remains valuable in that it facilitates the causal analysis of certain behavioral systems. Effects of neuroestrogens produced by neuronal aromatization of testosterone on copulatory performance (consummatory aspect) and on sexual motivation (appetitive aspect) are described in male quail. The central administration of estradiol rapidly increases expression of sexual motivation, as assessed by two measures of sexual motivation produced in response to the visual presentation of a female but not sexual performance in male Japanese quail. This effect is mimicked by membrane-impermeable analogs of estradiol, indicating that it is initiated at the cell membrane. Conversely, blocking the action of estrogens or their synthesis by a single intracerebroventricular injection of estrogen receptor antagonists or aromatase inhibitors, respectively, decreases sexual motivation within minutes without affecting performance. The same steroid has thus evolved complementary mechanisms to regulate different behavioral components (motivation vs. performance) in distinct temporal domains (long- vs. short-term) so that diverse reproductive activities can be properly coordinated. Changes in preoptic aromatase activity and estradiol as well as glutamate concentrations are observed during or immediately after copulation. The interaction between these neuroendocrine/neurochemical changes and their functional significance is discussed.

Keywords: Dual action of estrogens; Membrane estrogen receptors; Membrane-initiated effects; Preoptic aromatase; Sexual motivation; Testosterone.

Figure 1

Appetitive sexual behavior of male quail as measured by the Learned Social Proximity Response (LSPR) in the fast version of the test during which 6 males are exposed for 5 min to the view of a female before they have an opportunity to copulate with her (E males) or not (C males). In these conditions during phase I of the experiment, E males quickly learned to spend at least two thirds of the test time (more than 200 out of 300 s) in front of the window providing a view of the female. They do not develop the response until the first copulation has occurred (indicated by an arrow in the figure) or if copulation is prevented because the female is never released into the male chamber (the 3 C males). Once established the response remains stable even if testing is interrupted for a few weeks (phase II of the experiment) or if the female is no longer released into the male chamber so that the behavior is no longer reinforced by copulation (phase 3 of the experiment). Redrawn from data in (Balthazart et al., 1995).

Figure 2

Appetitive and consummatory components of male sexual behavior are activated by the chronic action of testosterone and these effects are blocked if the testosterone treatment is associated with an aromatase inhibitor. A. Aromatase activity increases in the preoptic area within one day after implantation of Silastic™ capsule filled with testosterone (T) and reaches its plateau after approximately 4 days. This increased enzymatic activity is blocked by the aromatase inhibitor ATD (left). Sexual behavior (mount attempts frequencies) increases a few days after the increase in aromatase activity and the behavioral activation is blocked or markedly delayed by ATD (right). B. The Learned Social Proximity Response (LSPR) is acquired by two groups of castrated males treated with exogenous testosterone (tests 1-8, left) but its expression progressively disappears in the group treated with the aromatase inhibitor Vorozole™ (VOR; tests 9-18, right). Note that effects of Vorozole™ were tested almost entirely in extinction mode, i.e, birds were not given access to the female after the visual exposure except during tests 13 and 18. C. Testosterone increases the frequency in Rhythmic Contractions of the cloacal Sphincter Muscles (RCSM) in response to the view of a female (left) but this response is progressively inhibited in males treated with the aromatase inhibitor Vorozole™ (VOR, right). Redrawn from data in (Balthazart et al., 1990b), (Balthazart et al., 1997a) and (Taziaux et al., 2004).

Figure 3

Rapid effects of neuroestrogens on the appetitive but not the consummatory components of male sexual behavior in quail. A-D. After 30 min, the acute blockade of aromatase activity by a single injection of Vorozole™ (VOR) inhibits and a single injection of E2 stimulates with 15 min the expression of two measures of ASB, the time spent looking at the female in the Learned Social Proximity Response (A) and the frequency of Rhythmic Contractions of the cloacal Sphincter Muscles (RCSM)(B) but the copulatory performance assessed by the frequency of Cloacal Contact Movements (CCM) is not affected (C) unless tests are performed in a large arena where the male has to chase the female to achieve copulation (D). E. The effects of an acute deprivation of estrogens by an injection of VOR are also counteracted by a single injection of the membrane-impermeable E2-biotin. F-G. The frequency of RCSM is similarly inhibited after 30 min by an injection of a steroidal (ATD) or a non-steroidal (VOR) aromatase inhibitor (F) and after 15 min by an injection of an antiestrogen, ICI-182,780 (fluvestran, ICI) or tamoxifen (TMX). H. The acute inhibition of RCSM induced by a single injection of VOR is partially reversed by a single injection of the ERβ agonist DPN but not the ERα agonist PPT. I. Restoration of the RCSM frequency by DPN following its acute inhibition by VOR is blocked by a single injection of the mGluR1 antagonist LY-367,385 (I). Significant differences between groups as identified by Newman-Keuls post hoc tests following a significant effect of treatment in the general ANOVAs (see original papers for detail of these analyses) are indicated as follows: **=p<0.01 and ***=p<0.001 compared to the controls (C); ##=p<0.01 and ###=p<0.001 compared to the VOR group and †††= p<0.001 compared to VOR+ DPN. Redrawn from data in (Seredynski et al., 2013) (A-G) and (Seredynski et al., 2015)(H-I).

Figure 4

Schematic representation of the rapid effects of an acute treatment with an aromatase activity (AA) inhibitor or with exogenous estradiol (E2) on the performance of appetitive and consummatory sexual behavior (ASB and CSB respectively)(Panels A-B) and of the neuroendocrine and neurochemical changes that take place in the preoptic area during and immediately after expression of CSB (Panels C-E). The X axis is graduated in minutes. Dotted parts of the red curves in D indicate that, due to technical limitations, we do not know how quickly the changes in E2 concentrations take place after the first interaction with a female nor how long this elevation lasts after 30 min.

Figure 5

Schematic presentation of two putative scenarios that link in a causal manner the neuroendocrine and neurochemical changes that take place in the preoptic area during and immediately after expression of sexual behavior and the control of appetitive and consummatory components of male sexual behavior in quail. In both hypotheses, the baseline aromatase activity (AA) and E2 concentration is the same but under the first hypothesis this concentration of E2 is sufficient to activate both ASB and CSB while under the second hypothesis, only CSB is activated at this concentration of E2 and an additional release induced by the view of a female is needed to activate ASB.