Activation and inhibition of the micturition reflex by penile afferents in the cat

Abstract

Woock JP, Yoo PB, Grill WM. Activation and inhibition of the micturition reflex by penile afferents in the cat. Am J Physiol Regul Integr Comp Physiol 294: R1880-R1889, 2008. First published April 23, 2008 doi:10.1152/ajpregu.00029.2008.-Coordination of the urinary bladder and the external urethral sphincter is controlled by descending projections from the pons and is also subject to modulation by segmental afferents. We quantified the effects on the micturition reflex of sensory inputs from genital afferents traveling in the penile component of the somatic pudendal nerve by electrical stimulation of the dorsal nerve of the penis (DNP) in ␣-chloralose anesthetized male cats. Depending on the frequency of stimulation (range, 1-40 Hz), activation of penile afferents either inhibited contractions of the bladder and promoted urine storage or activated the bladder and produced micturition. Stimulation of the DNP at 5-10 Hz inhibited distension-evoked contractions and increased the maximum bladder capacity before incontinence. Conversely, stimulation at 33 and 40 Hz augmented distension-evoked contractions. When the bladder was filled above a threshold volume (70% of the volume necessary for distension-evoked contractions), stimulation at 20 -40 Hz activated de novo the micturition reflex and elicited detrusor contractions that increased voiding efficiency compared with distension-evoked voiding. Electrical stimulation of the DNP with a cuff electrode or percutaneous wire electrode produced similar results. The ability to evoke detrusor contractions by activation of the DNP was preserved following acute spinal cord transection. These results demonstrate a clear role of genital afferents in modulating the micturition reflex and suggest the DNP as a potential target for functional restoration of bladder control using electrical stimulation. electrical stimulation; spinal cord injury; dorsal nerve of the penis; frequency dependence RECIPROCAL COORDINATION of the urinary bladder and the external urethral sphincter (EUS) to maintain continence and produce micturition is controlled by the pontine micturition center (2, 3, 24). The spinobulbospinal micturition reflex is also subject to modulation by peripheral afferent activity (29, 30) that can influence voiding efficiency (41). The objective of the present study was to quantify the effects of genital afferents traveling in the penile component of the somatic pudendal nerve on the micturition reflex in the cat.Activation of pudendal afferent nerve fibers can engage spinal (5) and spinobulbospinal (2, 3) reflexes that are integral to the regulation of bladder function. Fluid flow through the urethra activates pudendal afferents (56), and this flow-driven activation can elicit detrusor contractions and facilitate micturition (2, 44, 48). Furthermore, electrical stimulation of pudendal urethral afferents in the cat (5, 49) and human (21) elicits detrusor contraction, and these responses are preserved following decerebration and acute and chronic spinal cord transection (SCT;...

A spinal GABAergic mechanism is necessary for bladder inhibition by pudendal afferent stimulation

“…Stimulation at 1T and 2T produced significant bladder inhibition, but was less robust, consistent with results of other studies (53). The nomenclature used here for threshold and stimulation amplitude (1T ϭ BCR reflex EMG threshold) should be distinguished from other studies, where 1T is determined as the threshold to evoke inhibition and would, in general, represent a higher amplitude.…”

“…Electrodes were composed of single platinum contacts embedded within silicone cuffs, and pulse generators (Pulsar 6bp, FHC) were used to deliver stimulation (0.1-ms cathodic stimulus pulses, for 20 -30 s) between the cuffs and subcutaneous 20-G needles. Both the PN and DNP were stimulated at 10 Hz, a frequency previously shown to produce strong bladder inhibition in cats (53). The stimulation amplitude was one (1T), two (2T), or three (3T) times the threshold (T) that produced a bulbocavernosus reflex (BCR) EMG response in the EAS with 1-Hz stimulation.…”

Convergence and cross talk in urogenital neural circuitries

“…This finding is consistent with clinical neuromodulation studies showing that conditional and continuous DNP stimulation significantly increases bladder capacity (Kirkham et al 2001). The stimulus parameters to evoke the response are also consistent with animal studies showing that low-frequency DNP stimulation inhibits bladder contractions (Su et al 2012a;Woock et al 2008). Studies in adult cats also indicate that optimal inhibition of bladder contractions has a wider effective range of frequencies and amplitudes via DNP stimulation than other targets (pudendal, S 1 ) (Snellings and Grill 2012).…”

“…The study results demonstrate significant overlap in the neurostimulation parameters (amplitudes and frequencies) both for producing an increase in the interval of voiding during filling and for evoking or altering neuronal responses of MRF neurons in the rostral medulla, a site known to be involved in the control of sexual function (Marson and McKenna 1990). Previous studies examining neurostimulation for altering urinary physiology have demonstrated a U-shaped inhibitory curve with maximal effects at frequencies near 10 Hz (Snellings and Grill 2012;Su et al 2012aSu et al , 2012bWoock et al 2008). Interestingly, the present results with neurostimulation effects on MRF neuronal responses showed a plateau, or sigmoidal, effect with respect to frequency.…”

Mechanisms of reflex bladder activation by pudendal afferents

“…Further, abolition of stimulationevoked bladder contractions following administration of hexamethonium bromide confirmed that contractions were generated by pelvic efferent activation via the pelvic ganglion. These findings indicate that pudendal afferent stimulation evokes bladder contractions through convergence with pelvic afferents to increase pelvic efferent activity.cat; micturition; parasympathetic; sympathetic DEPENDING ON THE STIMULATION frequency, electrical stimulation of pudendal afferents evokes spinal reflexes that either inhibit the bladder and promote continence or excite the bladder and cause micturition in both cats (5,6,41,45,49) and persons with spinal cord injury (48). Previous results suggest that bladder inhibition by pudendal afferent stimulation arises from activation of hypogastric efferents and subsequent synaptic and ganglionic inhibition of parasympathetic efferents (8, 30), but the mechanisms of bladder excitation by pudendal afferent stimulation are not known.…”