Male Faces and Odours Evoke Differential Patterns of Neurochemical Release in the Mediobasal Hypothalamus of the Ewe During Oestrus: An Insight Into Sexual Motivation?

Abstract

During behavioural oestrus female sheep, like females of many species, become both attracted to and sexually receptive towards males, whereas at other times they will avoid them. The mediobasal hypothalamus is the main site for the feedback action of sex steroids to induce sexual behaviour in the sheep and in previous studies we have shown that noradrenaline and serotonin are released in this region during sexual interactions with males. The current study investigated whether such changes are specific to interactions with males and if visual or olfactory cues or somatosensory stimulation during mating are critical. In vivo microdialysis sampling was carried out in the mediobasal hypothalamus of ovariectomized ewes submitted to artificial oestrous cycles. Release of monoamines and amino acid transmitters was first measured in animals during and after oestrus when they were exposed to interactions with either males or females or presentation of food. Noradrenaline concentrations only increased significantly when the females were in oestrus and interacted with males irrespective of whether intromissions were permitted. Females were then exposed to visual (faces) or odour (a home pen) cues from males or to the males themselves. Slide images of male faces increased concentrations of amines, glutamate and GABA during early oestrus, when females spent most time looking at them. During late oestrus noradrenaline, glutamate and GABA concentrations also increased in response to the male faces but no transmitter changes were seen during the luteal phase or at any time where the females were exposed to female faces, or inverted male faces. Exposure to male odour produced a lower increase in noradrenaline concentrations when females were in early oestrus but marked increases 20 and 30 min after exposure to male odours in late oestrus. No other transmitters were affected. Exposure to a male and mating with him when females were in early or late oestrus produced increased noradrenaline concentrations similar to those seen with face stimuli alone although other neurotransmitters were unaffected. These results show that noradrenaline, and to a lesser extent dopamine, serotonin, glutamate and GABA release in the mediobasal hypothalamus, can be modulated specifically in the oestrous female by sensory information coming from the male during oestrus. The differential effects of male cues during early and late oestrus suggest their involvement in (i) proceptive or anticipatory sexual responses shown by the female to male cues, and (ii) receptive sexual responses, and suggest that the mediobasal hypothalamus plays a key role in the integration of hormonal action on sexual motivation and processing of sensory information during oestrus.

Substantial changes in central nervous system neurotransmitters and neuromodulators accompany phase change in the locust

“…Neuromodulation of neuronal networks or intrinsic changes in the amounts of neurotransmitters within these networks are two means of effecting such behavioural change, as has been reported to accompany the onset of sexual maturity or reproductive status (Fabre-Nys et al, 1997;Broad et al, 2002), the development and metamorphosis of insects and amphibians (Homberg and Hildebrand, 1994;Kloas et al, 1997;Takeda, 1997;Sillar et al, 1998;Lehman et al, 2000a,b;Consoulas et al, 2000;Mercer and Hildebrand, 2002), and during caste differentiation Nagao, 2001, 2002) and the division of labour between workers in social insects (Taylor et al, 1992;Wagener-Hulme et al, 1999;Schulz and Robinson, 1999). In the shorter term, neuromodulation by octopamine and serotonin in insects and Crustacea is associated in complex ways with social status arising from agonistic encounters (Kravitz, 2000;Sneddon et al, 2000;Stevenson et al, 2000), and serotonin has an important role in regulating the sensitivity of photoreceptors between night and day (Cuttle et al, 1995;Hevers and Hardie, 1995).…”

Steroid control of monoamines in relation to sexual behaviour

“…In this respect, changes in neurotransmitter release and receptor function seems to be particularly important. But, measurements of c-fos expression (Ohkura et al, 1997) suggest that steroids also indirectly alter the activity of several brain areas and, thereby, change the way the animal reacts to changes in its environment. In adults, the regulatory role of steroids seems more marked in females than in males.…”

“…Treatment with oestradiol and progesterone also increases noradrenaline release in the VMH. This has been observed in the rat after KCl stimulation or exposure to a male (Etgen et al 1992) and in sheep after exposure to a male as well as exposure to pictures of male faces or to male odour (Fabre-Nys et al, 1997). Oestradiol or progesterone alone, however, have no effect on dopamine or noradrenaline release in the VMH in response to male cues (Etgen et al 1992;Fabre-Nys et al, 1994) or, as in the mouse hypothalamus, decrease dopamine release (Dluzen et al, 1994).…”

“…As in males, noradrenaline may alter female behaviour by enhancing responsiveness to somatosensory information. Observations on changes in the extracellular concentration of noradrenaline in the VMH in oestrous female rats or sheep exposed to male behaviour or to pictures of male faces or odours support this hypothesis (Etgen et al, 1992;Fabre-Nys et al, 1997). Pharmacological studies reveal that noradrenaline has different behavioural effects depending on receptor type, brain area and species (Crowley et al, 1989;Etgen et al, 1992).…”

Central genomic regulation of the expression of oestrous behaviour in dairy cows: a review

“…In ewes, dopaminemediated D2 receptor (DRD2) signalling in the mediobasal hypothalamus is known to affect female sexual motivation and receptivity (Fabre-Nys et al, 2003). Furthermore, the perception and awareness of male-related cues differ with the stage of oestrous cycle, with releases of monoamines (linked to serotonin (HTR2A) and DRD2) and γ-aminobutyric acid (GABA) (linked to GABRA6) in the mediobasal hypothalamus being triggered by such cues only when ewes are in oestrus (Fabre-Nys et al, 1997). Studies on female rats and Table 3 Oestrous behaviour-associated genes and processes in dairy cows grouped in the GAPPS modules described for female sexual behaviour in rodents (Mong and Pfaff, 2004) …”