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ABSTRACT: The sinusoid anatomy of the penis is complex and requires complicated interaction between smooth muscle and endothelium in order to maintain homeostasis in the adult. The morphogen, Sonic hedgehog (Shh), is a crucial regulator of these processes, along with its down stream targets patched (Ptc), Hox, bone morphogenetic proteins (BMP's), vascular endothelial growth factor (VEGF) and nitric oxide synthase (NOS). Shh is critical for patterning and establishing tissue identity of the penis during embryonic development, is a crucial regulator of penile postnatal differentiation of the sinusoid morphology of the corpora cavernosa, and plays a fundamental role in maintaining sinusoidal structures pertinent to erectile function in the adult rat. Shh and its targets are active in human penes, and decreased in human diabetic penes in parallel with observations in the rat, thus lending clinical significance to the role of abnormal Shh signaling in erectile dysfunction (ED). Application of exogenous Shh protein to rat corpora cavernosa, induces VEGF and NOS proteins, suggesting a potential mechanism through which decreased Shh protein can cause ED. The studies outlined in this review provide in depth analysis of the Shh pathway and signal transduction, its role in penile development, how Shh signaling is altered in a rat model of ED and neuropathy, how abnormal Shh signaling can cause ED, and the clinical significance of the Shh pathway to human ED. These studies will provide valuable insight, at the molecular level, into understanding the mechanisms that under lie ED and lead to new treatment strategies for diabetic impotence.
Current Pharmaceutical Design 02/2005; 11(31):4011-27. · 3.87 Impact Factor
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ABSTRACT: The thoracolumbar and lumbosacral spinal cord contain respectively sympathetic and parasympathetic preganglionic neurons that supply the organs of the pelvis including the penis. These neurons are influenced by supraspinal information and receive aminergic projections from the brainstem. The presence of the alpha(1)- and alpha(2)-adrenoceptor subtypes has been demonstrated in the rat spinal cord. In this species, we looked for the presence of alpha(2a)- and alpha(2c)-adrenoceptor subtypes in the sympathetic and parasympathetic preganglionic neurons controlling erection. In adult male rats, transsynaptic axonal transport of pseudorabies virus injected into the penis was combined with immunohistochemistry against alpha(2a)- and alpha(2c)-adrenoceptor subtypes. At 4 days survival time, neurons infected with the pseudorabies virus were solely found in the intermediolateral cell column and dorsal gray commissure of segment T12-L2 and in the intermediolateral cell column of segment L6-S1. Neurons and fibers immunoreactive for alpha(2a)- and alpha(2c)-adrenoceptor subtypes were mainly present in the intermediolateral cell column, the dorsal gray commissure and the ventral horn of the T12-L2 and L5-S1 spinal cord, the dorsal horn displayed only immunoreactive fibers. Pseudorabies virus-infected neurons in the autonomic nuclei were both immunoreactive for alpha(2a)- and alpha(2c)-adrenoceptor subtypes and closely apposed by alpha(2a)- and alpha(2c)-immunoreactive fibers. The results suggest an intraspinal modulation of the noradrenergic and adrenergic control of the autonomic outflow to the penis by pre- and postsynaptic alpha(2) adrenoceptors.
Neuroscience 02/2002; 114(4):945-60. · 3.38 Impact Factor
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ABSTRACT: Optimal treatment of erectile dysfunction (ED) following radical prostatectomy remains a subject of much controversy and is a significant concern for prostate cancer patients requiring surgical intervention. Neural stimulation involving nitric oxide synthase (NOS) is a crucial aspect of the normal erection process. In this study NOS isoform interaction was evaluated to improve our understanding of molecular changes pertaining to erection post radical prostatectomy. Bilateral cavernous nerve (CN) resected and control adult male Sprague-Dawley rats were killed 7, 14 and 21 days after injury. RT-PCR, in situ hybridization, Western blot and immunohistochemical analysis were used to evaluate changes in NOS isoform expression and distribution. NOS-I protein was dramatically decreased after CN injury while NOS-III and NOS-II remained unchanged. A profound decrease in smooth muscle and endothelium was observed in the corpora. To our knowledge this is the first report of differential altered NOS isoform protein abundance under conditions which mimic radical prostatectomy. These results show the importance of maintaining at least partial innervation of the penis after surgical intervention and that endothelial and smooth muscle changes resulting from loss of innervation may account for the ED observed in prostatectomy patients.
International Journal of Impotence Research 01/2002; 13 Suppl 5:S1-15. · 1.71 Impact Factor
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ABSTRACT: Erectile dysfunction is a common pathological development in individuals with diabetes mellitus. Nitric oxide synthase (NOS) is essential for regulation of normal penile erection and NOS protein activity has been shown to be altered with diabetes. Several different isoforms and subtypes of NOS exist. However, little is known about how the distribution and abundance of these isoforms are altered with diabetes. We characterized the distribution and abundance of NOS isoforms and explored how they are altered with diabetes and result in erectile failure.
In situ hybridization and quantitative reverse transcriptase-polymerase chain reaction were done to measure the abundance and distribution of NOS-Ia, NOS-Ib, NOS-Ic, NOS-II and NOS-III in control and diabetic (BB/WOR) rats. Protein was localized by immunohistochemical analysis and alterations in protein abundance with diabetes were examined by Western blot analysis.
NOS-I, NOS-II and NOS-III were observed in the endothelium lining the cavernous spaces and in the epithelium of the urethra. NOS-I protein was also present in the nerves of control and diabetic penes. We observed an increase in NOS-II expression around the dorsal nerves of diabetic penes, a decrease in NOS-III expression in diabetic pelvic ganglia and a decrease in NOS-Ib expression in the diabetic penis. NOS-I protein abundance was significantly decreased in diabetic pelvic ganglia.
To our knowledge this is the first report of regional differences in the distribution of NOS-III in the urethra and altered NOS-Ib gene expression with diabetes.
The Journal of Urology 09/2001; 166(2):746-55. · 3.75 Impact Factor
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K E McKenna
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ABSTRACT: Neurological injury results in devastating sexual deficits in both men and women. Effective treatment requires an understanding of the central nervous system (CNS) pathways and physiology. This article emphasizes the essential similarities in the pathways and physiology of sexual function in men and women.
Literature review.
Systems within the spinal cord are fully capable of generating a large number of sexual responses. Spinal sexual centers may be activated by genital afferents or by descending commands from higher CNS sites. Normal functioning probably involves activation of spinal centers by both descending pathways and afferent stimulation. Afferent stimulation also modulates the activity of supraspinal sites, creating a positive feedback system. Descending control consists of powerful inhibitory and excitatory pathways. An important serotonergic inhibitory pathway has been demonstrated. The medial preoptic region participates in the integration of hormonal and sensory cues necessary for sexual behavior. The medial amygdala and paraventricular nucleus of the hypothalamus also play essential excitatory roles. The paraventricular nucleus projects directly to relevant spinal sites, indicating another important pathway for excitatory control.
Recent advances have markedly enhanced our understanding of the physiology, pharmacology, molecular biology and pathology of sexual mechanisms. This knowledge base is essential in order to understand changes in sexual mechanisms that follow spinal cord injury, and for the development of effective interventions to maximize sexual function in men and women with spinal cord injury.
The journal of spinal cord medicine 02/2001; 24(3):148-54. · 2.11 Impact Factor
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K E McKenna
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ABSTRACT: Recent research on the central nervous control of penile erection is discussed. A framework for this control is based upon principles put forward by Frank Beach regarding the neuroendocrine regulation of male copulatory behavior. The current discussion is focused primarily on a subset, penile erection. The spinal cord contains all the necessary components for the production of penile erection. This requires a multisegmental coordination among penile vasodilator and vasoconstrictor autonomic neurons, pudendal motoneurons responsible for penile rigidity and autonomic neurons which control extra-penile blood flow. Genital sensory stimulation can activate this spinal network. The spinal cord is also under excitatory and inhibitory control from supraspinal sites. Penile erection can be driven by supraspinal input alone and supraspinal control can inhibit the erectile effects of genital stimulation.An important aspect of the CNS control of penile erection is that there are extensive interconnections between most of the brain sites identified to date. Most of the pathways are characterized by reciprocal connections. A large number of the CNS sites also receive genital sensory information. Thus, descending control may itself be modulated by ascending sensory pathways which relay information from the genitalia. This raises the possibility that penile erection may involve a positive feedback system. Receptors for gonadal hormones have been identified throughout the neuraxis. However, strong evidence for the control of male sexual function by gonadal hormones has been identified only for forebrain sites. The functional role of brainstem and spinal gonadal hormone receptors has not yet been clarified.
Neuroscience & Biobehavioral Reviews 08/2000; 24(5):535-40. · 8.65 Impact Factor
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ABSTRACT: Some authors have advocated the daily use of sildenafil for prophylaxis against, or treatment of, erectile dysfunction. However, no information has been published to support such a dosage regimen. The safety profile of uninterrupted use of sildenafil has not been evaluated as it pertains to alteration of PDE type 6 in the retina. In the present study we investigated whether short- or long-term exposure to a variety of sildenafil doses affect the expression of an enzyme important in the normal phototransduction cascade.
Sustained-release sildenafil pellets were implanted in 120-day-old male rats with concentrations from 1-200mg. Rat retinal tissue was harvested 7, 14, and 29 days after implantation. Quantitative reverse transcriptase-polymerase chain reaction (RT-PCR) using GAPDH as an endogenous internal standard was used to quantitate PDE type 6 gene expression.
Expression of PDE type 6 was upregulated after 7 days with dosages < or =5 mg (P<0.02). Significant downregulation of PDE type 6 expression was first noted with high dose sildenafil 14 days after implantation (P<0.02). Expression of PDE type 6 was significantly and profoundly downregulated 29 days after implantation for all pellet formulations > or =10 mg (P<0.01).
Sildenafil downregulates PDE type 6 expression in a dose- and time-dependent fashion. These findings support the explanation that PDE type 6 inhibition causes the dose-dependent clinical effects of visual disturbance in men taking sildenafil. Implications for long-term, daily use of sildenafil in men are not clear.
International Journal of Impotence Research 09/1999; 11 Suppl 1:S9-14. · 1.71 Impact Factor
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K E McKenna
Annual review of sex research 02/1999; 10:157-83.
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ABSTRACT: The localization of 5-hydroxytryptamine2C receptors in the lumbosacral spinal cord of the rat was investigated using selective antibodies raised against the carboxyl-terminal part of the rat receptor. The distribution of immunoperoxidase labelling at the light microscope level revealed numerous labelled neurons in the gray matter, with a higher intensity in the sacral parasympathetic nucleus, the dorsal gray commissure and particularly the motoneurons of the ventral horn. Confocal microscope analysis showed that immunostaining was mainly intracellular (motoneurons), but could also be associated with the membrane of cell bodies and dendrites. Actually, electron microscope immunogold experiments demonstrated an exclusive staining of the cis-Golgi apparatus. Following pseudo-rabies virus transsynaptic retrograde labelling from the corpus cavernosum, labelled neurons were found in the sacral parasympathetic nucleus and the dorsal gray commissure of the L6-S1 segments. All virus-labelled neurons exhibited 5-hydroxytryptamine2C receptor immunoreactivity. These results indicate that all parasympathetic preganglionic neurons and their related interneurons which contribute to the innervation of cavernosal tissue bear 5-hydroxytryptamine2C receptors. In the sacral parasympathetic nucleus, most neurons which were retrogradely-labelled from the pelvic ganglion with Fast Blue also showed 5-hydroxytryptamine2C receptor immunoreactivity. In the ventral horn, motoneurons retrogradely labelled from the ischiocavernosus muscle and the bulbospongiosus muscle, both of which are involved in erection and ejaculation, were also 5-hydroxytryptamine2C receptor-immunopositive. The supraspinal serotoninergic control of erection at the lumbosacral level therefore appears to be strongly associated with the activation of 5-hydroxytryptamine2C receptors, consistent with the proerectile properties of 5-hydroxytryptamine2C agonists.
Neuroscience 02/1999; 92(4):1523-37. · 3.38 Impact Factor
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ABSTRACT: In the rat, spinal autonomic neurons controlling penile erection receive descending pathways that modulate their activity. The paraventricular nucleus of the hypothalamus contributes oxytocinergic fibers to the dorsal horn and preganglionic sympathetic and parasympathetic cell columns. We used retrograde tracing techniques with pseudorabies virus combined with immunohistochemistry against oxytocin and radioligand binding detection of oxytocinergic receptors to evidence the oxytocinergic innervation of thoracolumbar and lumbosacral spinal neurons controlling penile erection. Spinal neurons labelled with pseudo-rabies virus transsynaptically transported from the corpus cavernosum were present in the intermediolateral cell column and the dorsal gray commissure of the thoracolumbar and lumbosacral spinal cord. Confocal laser scanning microscopic observation of the same preparations revealed close appositions between oxytocinergic varicosities and pseudorabies virus-infected neurons, suggesting strongly the presence of synaptic contacts. Electron microscopy confirmed this hypothesis. Oxytocin binding sites were present in the superficial layers of the dorsal horn, the dorsal gray commissure and the intermediolateral cell column in both the thoracolumbar and lumbosacral segments. In rats, stimulation of the paraventricular nucleus induces penile erection, but the link between the nucleus and penile innervation remains unknown. Our findings support the hypothesis that oxytocin, released by descending paraventriculo-spinal pathways, activates proerectile spinal neurons.
Neuroscience 02/1999; 93(4):1437-47. · 3.38 Impact Factor
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K E McKenna
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ABSTRACT: Recent work on the central nervous system control of penile erection is reviewed. Penile erection is completely dependent on commands from the central nervous system. Clinical experience and experimental studies clearly demonstrate that systems within the spinal cord are fully capable of generating penile erection. Spinal erectile centers may be activated by genital afferents or by descending commands from higher CNS sites. An important inhibitory pathway from the nucleus paragigantocellularis has been demonstrated. The inhibition of spinal sexual responses is mediated by the neurotransmitter serotonin. The medial preoptic region has been demonstrated to be crucially involved in sexual behavior. It is likely that it participates in the integration of hormonal and sensory cues necessary for sexual behavior. The medial amygdala and paraventricular nucleus of the hypothalamus have also been shown to play key roles. Future CNS research may lead to new therapeutic approaches as well as the avoidance of untoward sexual side effects from centrally acting drugs.
International Journal of Impotence Research 06/1998; 10 Suppl 1:S25-34. · 1.71 Impact Factor
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ABSTRACT: The growth of the prostate gland has been considered to be controlled exclusively by endocrine means. The abundance of alpha adrenergic and muscarinic receptors and nerve fibers suggests that the autonomic nervous system may in fact play a role in the growth maturation and secretory functions of the prostate. The predominant adrenergic input to the prostate is from short adrenergic neurons, while cholinergic nerves are closely related to the glandular epithelium, presumably affecting a secretory function. The prostate has a high density of alpha-1 and beta-2 adrenergic receptors, and the presence of these receptors, as well as their regulation by androgens, suggests and supports the direct mitogenic effect of catecholamines on prostate growth. The activated signal transduction pathways in these neural systems also appear to modulate prostatic function and growth. Denervation of the prostate results in a loss of functional and structural integrity of the gland. The effects of sympathectomy and parasympathectomy support the conclusion that the dichotomy of function in prostatic autonomic innervation has a fundamental regulatory purpose. The majority of the afferent innervation to the ventral prostate is localized to sensory nerves from the L5 and L6 segments. There is some smaller degree of innervation from T13-L2. There is evidence of extensive bilateral innervation of pelvic viscera. Despite the importance of afferent sensory feedback in regulating the control of prostate growth, its effect is of a smaller magnitude than that observed with androgens. Regardless of the specific control mechanisms suggested by neural involvement in the growth differentiation and secretory function of the prostate, the presence of innervation appears to be consistent and reproducible, and holds great potential for increasing our understanding of pathologic influences in prostate disease.
The Prostate. Supplement 02/1998; 8:2-13.
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ABSTRACT: The pathophysiological mechanisms of diabetic impotence remain obscure. We have presented an analysis of sexual function in a diabetic rat (BB/WOR) model characterized by diffuse neuropathic changes without a confounding vasculopathy that allows us to define the neural components of erectile failure. Copulatory behavioral testing demonstrated that diabetic males were severely impaired: the controls mounted three times more than the diabetics and had about one-half the latency to first mount. The diabetics had about one-fourth the number of intromissions and took nearly twice as long to achieve first ejaculation. The number of ejaculations was drastically reduced as well. We examined sexual reflexes in the anesthetized acutely spinalized rat. These experiments tested the integrity of spinal circuits controlling sexual function. Reflex testing demonstrated that spinal sexual reflexes were also severely impaired: the onset latency of reflexes was more than doubled, and the duration of reflexes was less than one-half. More than one-half of the diabetic rats showed no penile erections. Neural studies showed even more derangement in reflex measures in rats, without erection. Nerve conduction velocity experiments suggested a peripheral neuropathic change in hypogastric nerve and motor pudendal nerve fibers. These dysfunctional findings were seen without any androgen deficiency. These results indicate that diabetic impotence in this model reflects central and peripheral neuropathic disease processes.
The American journal of physiology 02/1997; 272(1 Pt 2):R259-67.
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ABSTRACT: Transneuronal tracing techniques were used to identify spinal and brainstem neurons involved in the control of perineal muscles in the male rat. Two penile muscles, the bulbospongiosus and ischiocavernosus muscles, were injected with Bartha's strain of pseudorabies virus. After survival periods of 2, 4, and 5 days, the rats were killed and viral labeled neurons identified by immunohistochemistry. After a 2 day survival period, only pudendal motoneurons were labeled. More spinal and brainstem neurons were labeled at longer survival times. Putative spinal interneurons were found from T13 to S1. Large numbers of neurons were found in the lateral horn of the T13-L2 and L6-S1 segments which contain sympathetic and parasympathetic preganglionic neurons, respectively. However, retrograde labeling experiments verified that very few of the viral neurons were preganglionic neurons. Other labeled neurons were found in the intermediate cord, especially around the central canal. Relatively few labeled neurons were seen in the dorsal or ventral horn. In the brainstem, consistent labeling was seen in the ventrolateral medulla, raphe pallidus, and magnus, the A5 and locus ceruleus noradrenergic cell groups. Barrington's nucleus in the pontine tegmentum, the periaqueductal gray, and the paraventricular nucleus of the hypothalamus. The transneuronal labeling was consistent with what is currently known of the central nervous system (CNS) control of the perineal muscles.
The Journal of Comparative Neurology 11/1996; 374(2):161-79. · 3.81 Impact Factor
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ABSTRACT: Many factors are implicated in the development of prostatic growth: androgens, growth factors, and stromo-epithelial interaction. This study examines the role of the sympathetic and parasympathetic branches of the autonomic nervous system control of different aspects of rat prostate growth and atrophy. Unilateral sympathectomy leads to decreases in ventral prostate weight, DNA, and protein content in the lesioned side. Unilateral parasympathectomy leads to increases in ventral prostate weight, DNA, and protein content in the intact side. The separate effects of sympathectomy and parasympathectomy are maintained across a diverse combination of neural manipulations. Significant re-innervation does not occur by 60 days after manipulation as assessed by tissue norepinephrine levels. There appears to be a differential effect of the autonomic nervous system on growth and maintenance of the ventral prostate. The mechanism of contralateral hyperplasia and ipsilateral atrophy has potential significance in understanding human abnormal prostate growth.
Biology of Reproduction 08/1994; 51(1):99-107. · 4.01 Impact Factor
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ABSTRACT: The effects of the neurotoxin 5,7 dihydroxytryptamine (5,7 DHT) on the urethrogenital reflex was examined in anesthetized male rats. Both ICV and intrathecal administration of 5,7 DHT produced a marked depletion (92%) of spinal 5-hydroxytryptamine (5-HT) and 5-hydroxyindole acetic acid (5-HT IAA) levels. ICV but not intrathecal administration of 5,7 DHT also caused a moderate reduction in 5-HT and 5-HT IAA levels in the medulla and hypothalamus (40-48%). No reduction in adrenergic levels were observed. In spinally intact, vehicle-treated rats the urethrogenital reflex could not be evoked. However, the urethrogenital reflex could be evoked in rats pretreated with either ICV or intrathecal 5,7 DHT prior to section of the spinal cord. These data support the hypothesis that 5-HT mediates the descending inhibition of male sexual reflexes.
Pharmacology Biochemistry and Behavior 05/1994; 47(4):883-8. · 2.53 Impact Factor
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ABSTRACT: The urethrogenital (UG) reflex is a spinal sexual reflex which is tonically inhibited in the intact male rat by neurons in the nucleus paragigantocellularis (nPGi). The medial preoptic area of the hypothalamus (MPOA) is involved in the activation of male sexual behavior. The present study examines the effect of hypothalamic stimulation on the UG reflex in the intact male rat. Areas of the hypothalamus were stimulated bilaterally with either electrical stimulation or D,L-homocysteic acid (DLH) and the presence of the UG reflex examined. Stimulation of discrete aras of the hypothalamus evoked the UG reflex. The UG reflex could be initiated in the absence of genital stimulation. Microinjections of DLH into the MPOA also initiate the UG reflex. These data suggest that stimulation of neurons in the MPOA overcome the inhibition by the nPGi and facilitate spinal genital reflexes leading to ejaculation.
Brain Research 03/1994; 638(1-2):103-8. · 2.73 Impact Factor
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ABSTRACT: Transneuronal tracing techniques were used in order to identify putative spinal interneurons and brainstem sites involved in the control of penile function. Pseudorabies virus was injected into the corpus cavernosus tissue of the penis in rats. After a four day survival period, rats were perfused with fixative and virus-labelled neurons were identified by immunohistochemistry. Postganglionic neurons were retrogradely labelled in the major pelvic ganglia. In the spinal cord, sympathetic and parasympathetic preganglionic neurons were labelled transneuronally. Presumptive interneurons were also labelled in the lower thoracic and lumbosacral spinal cord in locations consistent with what is currently known about such interneurons. In the brainstem, transneuronally labelled neurons were found in the medulla, pons and hypothalamus. Regions consistently labelled included the nucleus paragigantocellularis, parapyramidal reticular formation of the medulla, raphe pallidus, raphe magnus, A5 noradrenergic cell group, Barrington's nucleus and the paraventricular nucleus of the hypothalamus. This study confirmed previous studies from our lab and others concerning the preganglionic and postganglionic neurons innervating the penis. The number, morphology and location of these neurons were consistent with labelling seen following injection of conventional tracers into the penis. The brainstem nuclei labelled in this study were also consistent with what is currently known about the brainstem control of penile function. The labelling appeared to be highly specific, in that descending systems involved in other functions were not labelled. These results provide further evidence that the pseudorabies virus transneuronal tracing technique is a valuable method for identifying neural circuits mediating specific functions.
Neuroscience 08/1993; 55(1):263-80. · 3.38 Impact Factor
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ABSTRACT: The effects of electrolytic lesions of the rostral nucleus paragigantocellularis (nPGi) were examined on ex copula sexual reflexes in male rats. Bilateral lesions of the nPGi significantly reduced (by 50%) the onset of the first ex copula reflex, which usually was a glans erection. In addition, the number of dorsiflexions (flips) was significantly increased. In the anesthetized spinally intact rat the urethrogenital reflex cannot be evoked. However, after chronic bilateral lesions of the rostral nPGi, half of the rats tested displayed the urethrogenital reflex prior to section of the spinal cord. These data support a role for the rostral nPGi in the descending inhibition of male sexual reflexes.
Brain Research 11/1992; 592(1-2):187-92. · 2.73 Impact Factor
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ABSTRACT: The contribution of C1-adrenergic and nonadrenergic neurons to the spinal projection from the rostral ventrolateral medulla (RVLM) and their relative innervation density throughout thoracic spinal segments were examined by combining the Fluorogold (FG) retrograde tracing technique with immunofluorescent labeling for the epinephrine-synthesis enzyme phenylethanolamine N-methyltransferase (PNMT). The results indicate that the RVLM-spinal projection is comprised of both PNMT-positive and PNMT-negative neurons located in the subretrofacial area of the RVLM, approximately 1 to 1.7 mm rostral to obex. The bulbospinal projection from the RVLM is predominantly ipsilateral, and bulbospinal neurons do not appear to be organized within the RVLM in a manner indicating their segmental termination site. Eighty-one percent (+/- 4%, n = 2) of the PNMT-positive cells in the ipsilateral subretrofacial RVLM were retrogradely labeled after unilateral FG injections into multiple thoracic levels of the intermediolateral cell column (IML). Following single level FG injections, the number of retrogradely labeled PNMT-positive neurons in the subretrofacial RVLM decreased with injections in more caudal thoracic segments, indicating a heavier innervation of the upper thoracic IML by C1 neurons. PNMT-negative neurons were the main component of the RVLM-spinal population with 63 +/- 8% (n = 7) of the non-PNMT-containing neurons within the ipsilateral subretrofacial RVLM innervating all thoracic levels of the IML. The results indicate that both C1-adrenergic and nonadrenergic neurons in the RVLM make a substantial contribution to the innervation of the IML.
The Journal of Comparative Neurology 11/1992; 324(1):1-13. · 3.81 Impact Factor
