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Rhythmic Motor Patterns Accompanying Ejaculation in Spinal Cord-Transected Male Rats

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Rhythmic Motor Patterns Accompanying Ejaculation in Spinal Cord-Transected Male Rats International Journal of Impotence Research (2014) 26, 191–195 & 2014 Macmillan Publishers Limited All rights reserved 0955-9930/14 www.nature.com/ijir ORIGINAL ARTICLE Rhythmic motor patterns accompanying ejaculation in spinal cord-transected male rats M Carro-Jua´rez1, G Rodrı´guez-Manzo2, M de Lourdes Rodrı´guez Pen˜a1 and MA´ Franco1 A spinal pattern generator controls the ejaculatory response. Activation of this spinal generator elicits rhythmic motor patterns of the striated musculature that surrounds the genital tract that contributes to the expulsion of seminal secretions. In the present study, we elicited ejaculation in spinal cord-transected male rats by mechanically stimulating the urethra and registered rhythmic motor patterns in the cremasteric, iliopsoas and pubococcygeus muscles. The rhythmic motor activity recorded in these muscles was compared with that elicited in the bulbospongiosus muscles; the results revealed similarities in the motor parameters among all the muscles. Data of this study, showing the occurrence of rhythmic motor behaviour in the cremasteric, iliopsoas and pubococcygeus muscles during ejaculation, suggest that these muscles might be under the control of the spinal generator for ejaculation. International Journal of Impotence Research (2014) 26, 191–195; doi:10.1038/ijir.2014.4; published online 20 February 2014 Keywords: ejaculation; pelvic and abdominal striated muscles; rat; rhythmic motor pattern; spinal cord; spinal generator for ejaculation INTRODUCTION SGE’s initial activation by genital inputs, multiple rhythm- Ejaculation is the physiological process that describes the generating cores of the ejaculation circuit could be activated expulsion of semen from the urethra and consists of two different simultaneously within the lumbosacral spinal cord, initiating 4 phases, an emissive phase and an ejective phase.1–4 The emissive multiple motor patterns. Electromyographic (EMG) studies of 11 12 phase implies the closure of the bladder neck and the contraction the pudendo-pudendal, the bulbocavernosus and the glans- 13 of the sexual accessory glands, including the seminal vesicles, vasal, urethromuscular, cavernoso-urethral and abdominal- 14 prostate, vas deferens and coagulant glands.1–4 The ejective phase genital reflexes reported to participate in ejaculation, partially consists of the forceful ejection of semen from the urethral support these hypotheses and show that, after mechanical meatus, caused by the rhythmic contraction of the striated genital stimulation of genital structures, several rhythmic patterns of muscles.1–4 The ejective phase of ejaculation is considered the muscular activity occur. However, the whole striated muscular main indicator of ejaculation.4 activity observed during ejaculation, which could be considered as Experimental studies have provided the physiological evidence the entire somatic component of ejaculation, has not been fully for the involvement of a spinal pattern generator in the control of characterised. ejaculation.5–8 Activation of this spinal generator for ejaculation A general picture about the participation of striated muscles (SGE), by stimulation of genital structures in anaesthetised and and their neural control in ejaculation is now available. Thus, it has spinal cord-transected animals, elicits the complete sequence of been demonstrated that genital striated muscles such as the genital activities associated with seminal ejection, which includes levator ani, bulbospongiosus, ischiocavernosus and urethralis as the potent and rhythmic expulsion of seminal secretions, well as of the sphincters all participate in the ejective phase of movements and erections of the penis and the rhythmic ejaculation.4,5,13,15 However, other pelvic and abdominal muscles contraction of the genital striated muscles.4,9,10 Although it is are suggested to intervene in the ejaculatory phenomenon. This well known that the SGE mediates the genital autonomic and would be the case of the cremasteric (Cm) and the somatic outflow during the two phases of ejaculation and pubococcygeus (Pbc) muscles,16,17 as well as of muscles of the integrates sensory inputs necessary to trigger this sexual posterior abdominal wall, such as the iliopsoas (Ilps) muscles. It response, evidence regarding the neural mechanisms and has been proposed that these muscles contract rhythmically to substrates of this spinal network is scarce.4 lead to intense pelvic thrusting, resulting in deep deposition of Our recent hypotheses on the spinal control of ejaculation seminal secretions.18 suggest that the SGE has a modular structure and to attain In the present work, we hypothesised that these abdominal ejaculation, one major ejaculation generating core of this pattern muscles would exhibit rhythmic activity during the ejaculatory generator, located in the upper segments of the lumbar cord, response, simultaneous to the one exhibited by the genital drives the SGE pacemaker activity towards multiple rhythm- muscles already described, supporting the notion that they generating cores of the ejaculation circuit.4 As a consequence of participate in the ejaculatory response. To test this hypothesis, 1Laboratorio de Comportamiento Reproductivo, Escuela de Medicina Veterinaria y Zootecnia, Universidad Auto´noma de Tlaxcala, Tlaxcala, Me´xico and 2Departamento de Farmacobiologı´a, Cinvestav-SedeSur, Calzada de los Tenorios 235, Col Granjas Coapa, Delegacio´ n Tlalpan, Me´xico D.F., Mexico City, Me´xico. Correspondence: Dr M Carro-Jua´rez, Laboratorio de Comportamiento Reproductivo, Escuela de Medicina Veterinaria y Zootecnia, Universidad Auto´noma de Tlaxcala, AP 484, Huamantla Tlax domicilio conocido, Tlaxcala 9000, Mexico. E-mail: [email protected] Received 6 August 2013; revised 10 December 2013; accepted 9 January 2014; published online 20 February 2014 Rhythmic motor activity of ejaculation M Carro-Jua´rez et al 192 we used the fictive ejaculation model in spinal cord-transected muscles. This muscle was selected as a monitor of ejaculatory activity, male rats and evoked the reflexive activation of the selected owing to its superficial position in the perineum and given that it muscles by the mechanical stimulation of the urethra (5, for discharges rhythmically during ejaculation, in synchrony with all genital review; 19). The fictive ejaculation model permits the recording muscles. Thereafter, the RMPE were activated by mechanically stimulating and visualisation of the rhythmic motor pattern of ejaculation the pelvic urethra with saline solution. Saline was administered with a syringe pump, through a PE-50 catheter (0.965 mm OD) inserted into the (RMPE) in separated striated muscles that is accompanied by pelvic urethra via a bladder incision, at a rate of 200 ml min À 1 for 10 s, while complex pelvic activity including phasic and strong penile erec- occluding the penis meatus to achieve an intraurethral pressure, which tions, as well as penile movements, followed by the potent expul- ranged from 20–30 mm Hg. The RMPE was activated in the Bsp muscle by sion of urethral contents. urethral stimulation at 3-min intervals and the EMG activity of the other selected muscles, if present, was simultaneously monitored searching for its rhythmic activation during the ejaculatory response. At this moment, MATERIALS AND METHODS the stimulation protocol was finished. Animals Sexually experienced male Wistar rats averaging 300–350 g body weight Drugs were used. Animals were housed by groups (four rats per cage) under an Urethane hydrochloride was purchased from Sigma Chemical (St Louis, inverted light/darkness cycle 12:12 h, at 22 1C, and with free access to food MO, USA) and dissolved in distilled water. and water. The Local Committee of Ethics on Animal Experimentation approved all experimental procedures, which followed the regulations established in the Mexican official norm for the use and care of laboratory Data analysis animals ‘NOM-062-ZOO-1999’. EMG activity was recorded differentially, amplified and filtered (1000 Â , 0.1–1 kHz bandpass) in a Poliview Data Acquisition System (Grass). The parameters recorded in the muscular trains during ejaculatory responses Groups were: latency to the appearance of the motor response and the number Animals were divided into four groups (N ¼ 4, each). Group 1 was utilised and frequency of EMG bursts. All numerical values were expressed as to record the EMG activity of the Bsp muscle, elicited by the mechanical means±s.e.m. Mean values were calculated for each individual animal and stimulation of the urethra expressed as the RMPE, and served as the paired comparisons between the control group and each of the control group. Animals in groups 2–4 were employed to register the experimental groups were conducted by means of the Mann–Whitney probable expression of the RMPE in the Cm (G2), Ilps (G3) and Pbc (G4) U-test. A Po0.05 was considered to be statistically significant. The Stat muscles in response to the mechanical stimulation of the urethra. program (SigmaStat 3.5, Jandell Scientific Corp., San Raphael, CA, USA) was used for all statistical analyses. Sexual behaviour observations To provide sexual experience, male rats received five sexual behaviour RESULTS tests with receptive females. Female receptivity was induced by the sequential subcutaneous administration of oestradiol valerianate (4 mg per The ejaculatory motor pattern of spinal cord-transected male rats rat, s.c.) followed 44 h later by progesterone (2 mg per animal, s.c.). evoked by urethral stimulation and registered
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