The Journal of Neuroscience

Brain mechanisms that control human sexual behavior in general, and ejaculation in particular, are poorly understood. We used positron emission tomography to measure increases in regional cerebral blood flow (rCBF) during ejaculation compared with sexual stimulation in heterosexual male volunteers. Manual penile stimulation was performed by the volunteer's female partner. Primary activation was found in the mesodiencephalic transition zone, including the ventral tegmental area, which is involved in a wide variety of rewarding behaviors. Parallels are drawn between ejaculation and heroin rush. Other activated mesodiencephalic structures are the midbrain lateral central tegmental field, zona incerta, subparafascicular nucleus, and the ventroposterior, midline, and intralaminar thalamic nuclei. Increased activation was also present in the lateral putamen and adjoining parts of the claustrum.

Neocortical activity was only found in Brodmann areas 7/40, 18, 21, 23, and 47, exclusively on the right side. On the basis of studies in rodents, the medial preoptic area, bed nucleus of the stria terminalis, and amygdala are thought to be involved in ejaculation, but increased rCBF was not found in any of these regions. Conversely, in the amygdala and adjacent entorhinal cortex, a decrease in activation was observed.

Remarkably strong rCBF increases were observed in the cerebellum. These findings corroborate the recent notion that the cerebellum plays an important role in emotional processing. The present study for the first time provides insight into which regions in the human brain play a primary role in ejaculation, and the results might have important implications for our understanding of how human ejaculation is brought about, and for our ability to improve sexual function and satisfaction in men.

Key words: amygdala; cerebellum; heroin; midbrain; PET (positron emission tomography); sex

The recent success of drugs that increase male sexual performance emphasizes the enormous impact of sexual function on the overall quality of life. Ejaculation represents a major component of male sexual behavior. It is the result of a coordinated action of male sexual organs such as the prostate, seminal vesicles, urethra, and pelvic floor muscles (Gil-Vernet et al., 1994) and is typically accompanied by orgasmic sensations.

Studies in rats and gerbils have revealed that the medial preoptic area (MPOA), medial nucleus of the amygdala (MeA), bed nucleus of the stria terminalis (BNST), midbrain lateral central tegmental field (LCTF), and parvocellular part of the subparafascicular nucleus (SPFp) express Fos activity with ejaculation (Baum and Everitt, 1992; Coolen et al., 1996; Heeb and Yahr, 1996). In primates, however, a decrease in c-Fos activity was found in the BNST and hypothalamic regions (Michael et al., 1999). Baum and Everitt (1992) suggest that in rats, genital and olfactory vomeronasal input induces c-Fos activity in the LCTF/SPFp and MeA, respectively, and that these regions, in turn, activate the MPOA and BNST. Lesions in the posterodorsal preoptic nucleus and posterodorsal MeA in gerbils (Heeb and Yahr, 2000) resulted in a delay in ejaculation, but lesions in the subparafascicular nucleus did not. In male rats, bilateral lesions in the area of the LCTF completely eliminated mating behavior (Brackett and Edwards, 1984), as was the case after a unilateral MPOA lesion combined with a lesion in the LCTF on the contralateral side. Apparently, in rodents, connections between the MPOA and LCTF are essential for copulation.

These studies did not elucidate the precise role of the respective regions in sexual behavior. There are two reasons for the problems with determining the precise role of c-Fos in these events: (1) c-Fos has a temporal resolution of >1 hr and, therefore, cannot be conclusively linked to one specific event. (2) There is a difference in sensitivity to c-Fos between different brain structures (Kovács, 1998). The impact of lesion studies is also limited, because they do not provide insight into which systems become dysfunctional as a result of various lesions. In conclusion, even in rodents, a complete concept regarding the sensory and motor systems involved in ejaculation is still lacking. In other species, however, almost nothing is known about the cerebral organization of ejaculation.

With the introduction of positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) it became possible to register and map activity in all parts of the human brain, including the brainstem. Several investigators have studied brain activation during human sexual arousal (Stoleru et al., 1999; Redouté et al., 2000; Bocher et al., 2001; Arnow et al., 2002; Karama et al., 2002). The present study is the first to reveal the brain regions in humans that are most active during ejaculation.

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