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23 septembre 2001
J Neuroscience
2000, 20(17):6640-6647
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Role of the Lateral Preoptic Area in Sleep-Related Erectile Mechanisms and Sleep Generation in the Rat
Markus H. Schmidt, Jean-Louis Valatx, Kazuya Sakai, Patrice Fort, and Michel Jouvet
Cleveland Clinic Foundation, Department of Neurology, Cleveland, Ohio 44195, and University of Claude Bernard, Institut National de la Santé et de la Recherche Médicale U480, Lyon, France


Resume : Penile erections are a characteristic phenomenon of paradoxical sleep (PS), or rapid eye movement sleep. Although the neural mechanisms of PS-related erections are unknown, the forebrain likely plays a critical role (Schmidt et al., 1999). The preoptic area is implicated in both sleep generation and copulatory mechanisms, suggesting it may be a primary candidate in PS erectile control. Continuous recordings of penile erections, body temperature, and sleepÐwake states were performed before and up to 3 weeks after ibotenic acid lesions of the preoptic forebrain in three groups of rats. Neurotoxic lesions involving the medial preoptic area (MPOA) and anterior hypothalamus (n 5 5) had no significant effects on either erectile activity or sleepÐwake architecture. In contrast, bilateral lesions of the lateral preoptic region, with (n 5 4) or without (n 5 5) MPOA involvement, resulted in a significant decrease in the number of erections per hour of PS, number of PS-related erections, and PS phases exhibiting an erection. Lesion analysis revealed that the candidate structuresfor PS erectile control include both the lateral preoptic area (LPOA) and ventral division of the bed nucleus of the stria terminalis; however, lesions of the LPOA were the most effective in disrupting PS erectile activity. LPOA lesioning also resulted in a long-lasting insomnia, characterized by the significant increase in wakefulness and decrease in slow wave sleep (SWS). PS architecture and waking-state erections remained unchanged after lesion in all groups. These data identify an essential role of the LPOA in both PS-related erectile mechanisms and SWS generation. Moreover, higher erectile mechanisms appear to be context-specific because LPOA lesioning selectively disrupted PS-related erections while leaving waking-state erections intact.

Intro : Paradoxical sleep (PS), also known as rapid eye movement sleep, is characterized by several tonic and phasic phenomena, including cortical desynchronization, rapid eye movements, general muscle atonia, and penile erections. Whereas the neural control of PS related erections remains unknown, the executive mechanisms generating PS and its other tonic and phasic events are relatively well elucidated and localized within the mesopontine tegmentum and rostral medulla (Sakai 1985; Jones 1991). Using a new technique of chronic penile erection recording in the rat (Schmidt et al.,1995), we recently demonstrated that mesencephalic transections disrupt PS erectile activity even though PS remains otherwise qualitatively intact (Schmidt et al., 1999). These data suggest that forebrain structures rostral to the transection are necessary for the production of PS-related erections. The source of this forebrain control currently is a matter of speculation. Numerous forebrain structures have been implicated in reproductive mechanisms and, therefore, are potential candidates in sleep-related erectile control. Lesion, stimulation, and unit recording studies have elucidated an erectile role of the paraventricular nucleus (Melis et al., 1994), medial preoptic area (MPOA) (Giuliano et al., 1996), bed nucleus of the stria terminalis (BNST) (Valcourt and Sachs 1979), hippocampus (Chen et al., 1992), amygdala (Kondo 1992), and olfactory bulbs (Fernandez-Fewell and Meredith, 1995). Recent data suggest that some of these structures may be responsible for context-specific erectile control (Sachs, 1995). We hypothesize that the preoptic area may be a primary forebrain candidate in sleep-related erectile control given its role in both reproductive physiology and slow wave sleep (SWS) generation. The MPOA, for example, has long been implicated in copulatory mechanisms because its lesioning eliminates copulatory behavior in every species examined (Sachs and Meisel, 1988). Moreover, low androgen states disrupt PS-related erections in humans (Carani et al., 1992), and the MPOA contains androgensensitive neurons important for reproductive physiology (Cherry et al., 1992). With regard to sleep and wakefulness, both the MPOA and lateral preoptic area (LPOA) are described as "sleep centers" because their lesioning results in a long-lasting insomnia (Lucas and Sterman, 1975; Szymusiak, and McGinty 1986; Sallanon et al., 1989). Stimulation, neuroanatomical, and single-unit recording studies suggest an important role of the preoptic area in the generation of SWS and inhibition of waking mechanisms (Siegel and Wang, 1974; Ogawa and Kawamura, 1988; Sherin et al., 1998). Although the importance of the MPOA in copulatory behavior is well established, the relative contribution of theMPOA and LPOA in sleep generation remains controversial. In the following experiments, cytotoxic lesions of the preoptic basal forebrain were performed using ibotenic acid in an attempt to localize forebrain structures involved in PS-related erections. Moreover, neurotoxic lesions primarily were limited to either the MPOA, LPOA, or both in three groups of rats to differentiate the relative contributions of these two structures in sleep-related erectile control and sleep generation. Continuous polygraphic recordings of penile erections, sleepÐwake states, and body temperature were performed before and up to 3 weeks after neurotoxic lesions.