Performance of appetitive or consummatory components of male sexual behavior is mediated by different brain areas: A 2-deoxyglucose autoradiographic study

The in vivo autoradiographic deoxyglucose method was used to identify the f unctional brain circuits that are involved in the performance of appetitive and consummatory components of male sexual behavior in Japanese quail (Cot urnix japonica). Two groups of castrated, testosterone-treated male quail w ere trained during 12 sessions to associate the view of a female behind a w indow with the opportunity to interact freely and to copulate with her. The y developed, as a consequence, a social proximity response (staying close a nd looking through the window providing a view of the female) that has been used in previous experiments to measure appetitive sexual behavior. A thir d control group (also castrated and treated with testosterone) was allowed to view the female but not to copulate with her and therefore did not devel op this proximity response. 2-C-14-deoxyglucose was then injected i.p. to t hese birds and they were allowed to either copulate freely with a female (c onsummatory sexual behavior group) or express the social proximity response (appetitive sexual behavior group). The control group was provided a view of the female but these birds, although they were exposed to the same stimu li as birds in the appetitive group, did not express the social proximity r esponse because they had never learned the association with the opportunity to copulate. Birds were killed 45 min after the deoxyglucose injection and their brains were processed for autoradiography. Densitometric analyses of the autoradiograms revealed that the expression of appetitive or consummat ory aspects of male sexual behavior was associated with significant increas es by comparison with the control group in the deoxyglucose incorporation i n the nucleus mesencephalicus lateralis, pars dorsalis and in the nucleus l eminsci lateralis. In addition, an increase in the deoxyglucose incorporati on was specifically observed in the paleostriatum primitivum, rostral preop tic area, nucleus intercollicularis, nucleus interpeduncularis and third ne rve but a decrease was observed in the dorsomedial part of the hippocampus and in the nucleus nervi oculomotori in birds of the consummatory sexual be havior group by comparison with controls. By contrast, in the appetitive se xual behavior group, significant increases in deoxyglucose incorporation we re observed in two telencephalic areas, the intermediate hyperstriatum vent rale and neostriatum caudolaterale by comparison with the controls, but dec reases were detected in the stratum griseum et fibrosum superficiale of opt ic tectum by comparison with the consummatory behavior group. These studies demonstrate that the performance of appetitive or consummator y components of male sexual behavior affects in a specific manner the deoxy glucose uptake and accumulation in specific regions of the quail brain. Cha nges in metabolic activity were observed in steroid-sensitive areas, in aud itory, visual and vocal brain regions, and in brain nuclei related to motor behavior but also in association telencephalic and limbic structures. Thes e changes in oxidative metabolism overlap to some extent with metabolic cha nges as revealed by immunocytochemistry for the immediate early gene produc ts Fos and Zenk, but many specific reactions are also detected indicating t hat these techniques are not necessarily redundant and, together, they can provide a more complete picture of the brain circuits that are implicated i n the control and performance of complex behaviors. (C) 1999 IBRO. Publishe d by Elsevier Science Ltd.