Frequency-dependent selection of alternative spinal pathways with common periodic sensory input

Jilge, B.; Minassian, Karen; Rattay, Frank; Dimitrijevič, Milan R.

doi:10.1007/s00422-004-0511-5

Cited by 36 publications

(33 citation statements)

References 28 publications

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“…This pathway would result in the inhi- bition of the inhibitory primary afferent depolarization in addition to driving further activation of the micturition reflex pathway associated with bladder afferents. This mechanism of frequency-dependent pathway activation is similar to that proposed for differential motor responses evoked by different frequencies of epidural spinal cord stimulation (25). Another potential mechanism for the observed frequency dependence is a synaptic mechanism described previously in the hippocampus (38).…”

Section: Discussionsupporting

confidence: 82%

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

Woock

Yoo²,

Grill³

2008

American Journal of Physiology-Regulatory, Integrative and Comp

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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;...

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Section: Discussionsupporting

confidence: 82%

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

Woock

Yoo²,

Grill³

2008

American Journal of Physiology-Regulatory, Integrative and Comp

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“…Indeed, they may either recruit distinct types of interneurons 20 or add previously 'silent' frequency-dependent spinal pathways to the ongoing locomotor pattern. 21 Our data here reported may spur further studies on these findings also for the spinal locomotor networks.…”

Section: Frequency Of Incoming Inputs Is More Important Than Intensitysupporting

confidence: 59%

Staggered multi-site low-frequency electrostimulation effectively induces locomotor patterns in the isolated rat spinal cord

et al. 2015

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Study design: Experimental animal study. Objectives: Epidural stimulation has been used to activate locomotor patterns after spinal injury and typically employs synchronous trains of high-frequency stimuli delivered directly to the dorsal cord, thereby recruiting multiple afferent nerve roots. Here we investigate how spinal locomotor networks integrate multi-site afferent input and address whether frequency coding is more important than amplitude to activate locomotor patterns. Setting: Italy and Belgium. Methods: To investigate the importance of input intensity and frequency in eliciting locomotor activity, we used isolated neonatal rat spinal cords to record episodes of fictive locomotion (FL) induced by electrical stimulation of single and multiple dorsal roots (DRs), employing different stimulating protocols. Results: FL was efficiently induced through staggered delivery (delays 0.5 to 2 s) of low-frequency pulse trains (0.33 and 0.67 Hz) to three DRs at intensities sufficient to activate ventral root reflexes. Delivery of the same trains to a single DR or synchronously to multiple DRs remained ineffective. Multi-site staggered trains were more efficient than randomized pulse delivery. Weak trains simultaneously delivered to DRs failed to elicit FL. Locomotor rhythm resetting occurred with single pulses applied to various distant DRs. Conclusion: Electrical stimulation recruited spinal networks that generate locomotor programs when pulses were delivered to multiple sites at low frequency. This finding might help devising new protocols to optimize the increasingly more common use of epidural implantable arrays to treat spinal dysfunctions.

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“…The model structure was based upon established neuroanatomical connections and inspired by a prior model of frequency-dependent selection of spinal locomotor reflexes (Jilge et al 2004), as the lower urinary tract reflexes evoked by pudendal afferent stimulation similarly depend on the frequency of afferent activation (Boggs et al 2006). Our model of the neural network that mediates the spinal pudendo-vesical reflex replicated the effects of pudendal afferent stimulation frequency and pattern on bladder pressure measured experimentally and enabled dissection of the underlying mechanisms.…”

Section: Introductionmentioning

confidence: 99%

Modeling the spinal pudendo-vesical reflex for bladder control by pudendal afferent stimulation

McGee

Grill

2016

J Comput Neurosci

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Electrical stimulation of the pudendal nerve (PN) is a promising approach to restore continence and micturition following bladder dysfunction resulting from neurological disease or injury. Although the pudendo-vesical reflex and its physiological properties are well established, there is limited understanding of the specific neural mechanisms that mediate this reflex. We sought to develop a computational model of the spinal neural network that governs the reflex bladder response to PN stimulation. We implemented and validated a neural network architecture based on previous neuroanatomical and electrophysiological studies. Using synaptically-connected integrate and fire model neurons, we created a network model with realistic spiking behavior. The model produced expected sacral parasympathetic nucleus (SPN) neuron firing rates from prescribed neural inputs and predicted bladder activation and inhibition with different frequencies of pudendal afferent stimulation. In addition, the model matched experimental results from previous studies of temporal patterns of pudendal afferent stimulation and selective pharmacological blockade of inhibitory neurons. The frequency- and pattern-dependent effects of pudendal afferent stimulation were determined by changes in firing rate of spinal interneurons, suggesting that neural network interactions at the lumbosacral level can mediate the bladder response to different frequencies or temporal patterns of pudendal afferent stimulation. Further, the anatomical structure of excitatory and inhibitory interneurons in the network model was necessary and sufficient to reproduce the critical features of the pudendo-vesical reflex, and this model may prove useful to guide development of novel, more effective electrical stimulation techniques for bladder control.

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Frequency-dependent selection of alternative spinal pathways with common periodic sensory input

Cited by 36 publications

References 28 publications

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

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

Staggered multi-site low-frequency electrostimulation effectively induces locomotor patterns in the isolated rat spinal cord

Modeling the spinal pudendo-vesical reflex for bladder control by pudendal afferent stimulation

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