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.