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

Abstract

The in vivo autoradiographic deoxyglucose method was used to identify the functional brain circuits that are involved in the performance of appetitive and consummatory components of male sexual behavior in Japanese quail ( Coturnix japonica). Two groups of castrated, testosterone-treated male quail were trained during 12 sessions to associate the view of a female behind a window with the opportunity to interact freely and to copulate with her. They developed, as a consequence, a social proximity response (staying close and looking through the window providing a view of the female) that has been used in previous experiments to measure appetitive sexual behavior. A third control group (also castrated and treated with testosterone) was allowed to view the female but not to copulate with her and therefore did not develop this proximity response. 2- 14C-deoxyglucose was then injected i.p. to these birds and they were allowed to either copulate freely with a female (consummatory 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 stimuli as birds in the appetitive group, did not express the social proximity response 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 consummatory aspects of male sexual behavior was associated with significant increases by comparison with the control group in the deoxyglucose incorporation in the nucleus mesencephalicus lateralis, pars dorsalis and in the nucleus leminsci lateralis. In addition, an increase in the deoxyglucose incorporation was specifically observed in the paleostriatum primitivum, rostral preoptic area, nucleus intercollicularis, nucleus interpeduncularis and third nerve but a decrease was observed in the dorsomedial part of the hippocampus and in the nucleus nervi oculomotori in birds of the consummatory sexual behavior group by comparison with controls. By contrast, in the appetitive sexual behavior group, significant increases in deoxyglucose incorporation were observed in two telencephalic areas, the intermediate hyperstriatum ventrale and neostriatum caudolaterale by comparison with the controls, but decreases were detected in the stratum griseum et fibrosum superficiale of optic tectum by comparison with the consummatory behavior group. These studies demonstrate that the performance of appetitive or consummatory components of male sexual behavior affects in a specific manner the deoxyglucose uptake and accumulation in specific regions of the quail brain. Changes in metabolic activity were observed in steroid-sensitive areas, in auditory, visual and vocal brain regions, and in brain nuclei related to motor behavior but also in association telencephalic and limbic structures. These changes in oxidative metabolism overlap to some extent with metabolic changes as revealed by immunocytochemistry for the immediate early gene products Fos and Zenk, but many specific reactions are also detected indicating that these techniques are not necessarily redundant and, together, they can provide a more complete picture of the brain circuits that are implicated in the control and performance of complex behaviors.