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ERECTILE DYSFUNCTION Neurophysiology of Penile Erection the Penis Is Innervated by Autonomic and Somatic TOM F

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ERECTILE DYSFUNCTION Neurophysiology of Penile Erection the Penis Is Innervated by Autonomic and Somatic TOM F The New England Journal of Medicine Drug Therapy mitter release, the breakdown of second messengers by phosphodiesterases, or sympathetic discharge dur- ing ejaculation. Contraction of the trabecular smooth A LASTAIR J.J. WOOD, M.D., Editor muscle reopens the venous channels, the trapped blood is expelled, and flaccidity returns. ERECTILE DYSFUNCTION Neurophysiology of Penile Erection The penis is innervated by autonomic and somatic TOM F. LUE, M.D. nerves. In the pelvis, the sympathetic and parasym- pathetic nerves merge to form the cavernous nerves, which enter the corpora cavernosa, corpus spongio- sum, and glans penis to regulate blood flow during RECTILE dysfunction is defined as the inabil- erection and detumescence. The somatic component, ity to achieve and maintain an erection suffi- the pudendal nerve, is responsible for penile sensa- cient to permit satisfactory sexual intercourse.1 E tion and the contraction and relaxation of the extra- It has been estimated to affect 20 million to 30 mil- corporeal striated muscles (bulbocavernous and is- lion men in the United States.2,3 It may result from chiocavernous). psychological, neurologic, hormonal, arterial, or cav- ernosal impairment or from a combination of these Penile Flaccidity factors. In this article we provide a brief overview of The maintenance of the intracorporeal smooth the physiology of erection and the pathophysiology muscle in a semicontracted state (Fig. 2) results from of erectile dysfunction, followed by a discussion of three factors: intrinsic myogenic activity,7 adrenergic drug treatment for the disorder. neurotransmission,8 and endothelium-derived con- PHYSIOLOGY OF PENILE ERECTION tracting factors such as prostaglandin F2a and endo- thelins.9,10 Penile erection is a neurovascular event modulated by psychological factors and hormonal status. On Penile Erection sexual stimulation, nerve impulses cause the release of Nitric oxide released during nonadrenergic, non- neurotransmitters from the cavernous nerve termi- cholinergic neurotransmission and from the endothe- nals and of relaxing factors from the endothelial cells lium is probably the principal neurotransmitter me- in the penis, resulting in the relaxation of smooth diating penile erection.11,12 Within the muscle, nitric muscle in the arteries and arterioles supplying the oxide activates a soluble guanylyl cyclase, which rais- erectile tissue and a severalfold increase in penile es the intracellular concentration of cyclic guanosine blood flow. At the same time, relaxation of the tra- monophosphate (GMP). Cyclic GMP in turn activates becular smooth muscle increases the compliance of a specific protein kinase, which phosphorylates cer- the sinusoids, facilitating rapid filling and expansion tain proteins and ion channels, resulting in the open- of the sinusoidal system (Fig. 1). The subtunical venu- ing of potassium channels and hyperpolarization of lar plexuses are thus compressed between the trabec- the muscle-cell membrane, sequestration of intracel- ulae and the tunica albuginea, resulting in almost to- lular calcium by the endoplasmic reticulum, and block- tal occlusion of venous outflow.4,5 These events trap ing of calcium influx by the inhibition of calcium the blood within the corpora cavernosa and raise the channels. The consequence is a drop in cytosolic cal- penis from a dependent position to an erect position, cium concentrations and relaxation of the smooth with an intracavernous pressure of approximately 100 muscle (Fig. 3). During the return to the flaccid state, mm Hg (the phase of full erection). cyclic GMP is hydrolyzed to GMP by phosphodies- During masturbation or sexual intercourse, both terase type 5. Other phosphodiesterases are also found of which trigger the bulbocavernous reflex, the is- in the corpus cavernosum, but they do not appear to chiocavernous muscles forcefully compress the base have an important role in erection. Communication of the blood-filled corpora cavernosa and the penis among smooth-muscle cells takes place through gap becomes even harder, with an intracavernous pressure junctions in the membranes of adjacent cells, which reaching several hundred millimeters of mercury (the allow the passage of ions and second messengers to phase of rigid erection). During this phase, the inflow synchronize muscle activity.13 and outflow of blood temporarily cease.6 Detumes- cence can be the result of a cessation of neurotrans- PATHOPHYSIOLOGY OF ERECTILE DYSFUNCTION From the University of California School of Medicine, San Francisco. Erectile dysfunction can be classified as psychogen- Address reprint requests to Dr. Lue at the Department of Urology, U-575, ic, organic (neurogenic, hormonal, arterial, cavernos- University of California, San Francisco, CA 94143-0738, or at tlue@urol. ucsf.edu. al, or drug-induced), or mixed psychogenic and or- ©2000, Massachusetts Medical Society. ganic (Table 1). The last form is the most common. 1802 · June 15, 2000 The New England Journal of Medicine Downloaded from nejm.org at UC SHARED JOURNAL COLLECTION on February 27, 2013. For personal use only. No other uses without permission. Copyright © 2000 Massachusetts Medical Society. All rights reserved. DRUG THERAPY Prostate Cavernous nerve (autonomic) Deep dorsal vein Dorsal artery Dorsal nerve (somatic) Dorsal artery Dorsal nerve (somatic) Erect Circumflex artery Circumflex Sinusoidal vein spaces Flaccid Helicine arteries Deep dorsal vein Tunica albuginea Trabecular smooth muscle Sinusoidal spaces Corpora cavernosa Subtunical venular plexus Cavernous artery Figure 1. Anatomy and Mechanism of Penile Erection. The cavernous nerves (autonomic), which travel posterolaterally to the prostate, enter the corpora cavernosa and corpus spongio- sum to regulate penile blood flow during erection and detumescence. The dorsal nerves (somatic), which are branches of the pu- dendal nerves, are primarily responsible for penile sensation. The mechanisms of erection and flaccidity are shown in the upper and lower inserts, respectively. During erection, relaxation of the trabecular smooth muscle and vasodilatation of the arterioles re- sults in a severalfold increase in blood flow, which expands the sinusoidal spaces to lengthen and enlarge the penis. The expansion of the sinusoids compresses the subtunical venular plexus against the tunica albuginea. In addition, stretching of the tunica com- presses the emissary veins, thus reducing the outflow of blood to a minimum. In the flaccid state, inflow through the constricted and tortuous helicine arteries is minimal, and there is free outflow via the subtunical venular plexus. Psychogenic Erectile Dysfunction prove libido but lead to difficulties with erection, or- Common causes of psychogenic erectile dysfunc- gasm, and sexual satisfaction.16 tion include performance anxiety, a strained relation- ship, lack of sexual arousability, and overt psychiatric Neurogenic Erectile Dysfunction disorders such as depression and schizophrenia. The Neurologic disorders such as Parkinson’s disease, strong association between depression and erectile Alzheimer’s disease, stroke, and cerebral trauma often dysfunction has been confirmed in two recent stud- cause erectile dysfunction by decreasing libido or pre- ies.14,15 In men with schizophrenia, decreased libido venting the initiation of an erection. In men with spi- is the main problem reported; neuroleptic drugs im- nal cord injuries, the degree of erectile function de- Volume 342 Number 24 · 1803 The New England Journal of Medicine Downloaded from nejm.org at UC SHARED JOURNAL COLLECTION on February 27, 2013. For personal use only. No other uses without permission. Copyright © 2000 Massachusetts Medical Society. All rights reserved. The New England Journal of Medicine ygy Receptors ygy Receptors cyclase Protein Protein Endothelins kinase C Increased kinase C Decreased Increased Adrenergic inositol Smooth-cAMP inositol triphosphate triphosphate muscle cell Endothelial Norepinephrine cell Prostaglandin F G protein a a2 Effector 1 Ca2+– Myosin light- Ca2+– (phospholipase C) Endoplasmic calmodulin chain kinase Endoplasmic calmodulin reticulum reticulum Inactive Diacylglycerol Receptors Adenylyl Ca2+–calmodulin–myosincyclase Ca2+–calmo light-chain kinase complex light-chain ki Protein Active Endothelins kinase C Increased Myosin light-chainDecreased Myosin l inositol phosphorylationcAMP phosph triphosphate Increased Increased Ca2+ Ca2+ Ca2+ Ca2+ Cycling of myosin ProstaglandinCycling F2a o cross-bridges along actin Stimulationcross-bridge 2+ Ca – Myosin light- Inhibition Endoplasmic calmodulin chain kinase reticulum InactiveSmooth-muscle contraction Ca2+–calmodulin–myosin light-chain kinase complex Active COLOR FIGURE Myosin light-chain Rev 2 5/12/2000 phosphorylation Author Lue Increased Fig # Ca2 2+ Size 38p4 Ca2+ Title Cycling of myosin ME cross-bridges along actin Stimulation DE RDU Artist SEW Inhibition AUTHOR PLEASE NOTE: Smooth-muscle Figure has been redrawn and type has been reset contraction Issue date Figure 2. Molecular Mechanism of Penile Smooth-Muscle Contraction. Norepinephrine from sympathetic nerve endings, and endothelins and prostaglandin F2a from the endothelium, activate receptors on smooth-muscle cells to initiate the cascade of reactions that results in elevation of intracellular calcium concentrations and smooth-muscle contraction. Protein kinase C is a regulatory component of the calcium-independent, sustained phase of agonist- induced contractile responses. Figure 3 (facing page). Molecular
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