Finite element modeling and in vivo analysis of electrode configurations for selective stimulation of pudendal afferent fibers

BackgroundIntraurethral electrical stimulation (IES) of pudendal afferent nerve fibers can evoke both excitatory and inhibitory bladder reflexes in cats. These pudendovesical reflexes are a potential substrate for restoring bladder function in persons with spinal cord injury or other neurological disorders. However, the complex distribution of pudendal afferent fibers along the lower urinary tract presents a challenge when trying to determine the optimal geometry and position of IES electrodes for evoking these reflexes. This study aimed to determine the optimal intraurethral electrode configuration(s) and locations for selectively activating targeted pudendal afferents to aid future preclinical and clinical investigations.MethodsA finite element model (FEM) of the male cat urethra and surrounding structures was generated to simulate IES with a variety of electrode configurations and locations. The activating functions (AFs) along pudendal afferent branches innervating the cat urethra were determined. Additionally, the thresholds for activation of pudendal afferent branches were measured in α-chloralose anesthetized cats.ResultsMaximum AFs evoked by intraurethral stimulation in the FEM and in vivo threshold intensities were dependent on stimulation location and electrode configuration.ConclusionsA ring electrode configuration is ideal for IES. Stimulation near the urethral meatus or prostate can activate the pudendal afferent fibers at the lowest intensities, and allowed selective activation of the dorsal penile nerve or cranial sensory nerve, respectively. Electrode location was a more important factor than electrode configuration for determining stimulation threshold intensity and nerve selectivity.

[1]  D. Durand,et al.  Modeling the effects of electric fields on nerve fibers: Determination of excitation thresholds , 1992, IEEE Transactions on Biomedical Engineering.

[2]  Warren M Grill,et al.  Computational modeling of epidural cortical stimulation , 2008, Journal of neural engineering.

[3]  W. Grill,et al.  Somatic innervation of the feline lower urinary tract , 2008, Brain Research.

[4]  Warren M Grill,et al.  Conditional and continuous electrical stimulation increase cystometric capacity in persons with spinal cord injury , 2009, Neurourology and urodynamics.

[5]  W. Grill,et al.  Intraurethral stimulation evokes bladder responses via 2 distinct reflex pathways. , 2009, The Journal of urology.

[6]  J S Walter,et al.  Bladder inhibition by penile nerve stimulation in spinal cord injury patients. , 1992, The Journal of urology.

[7]  Warren M. Grill,et al.  Bladder activation by selective stimulation of pudendal nerve afferents in the cat , 2008, Experimental Neurology.

[8]  Xuefeng F. Wei,et al.  Current density distributions, field distributions and impedance analysis of segmented deep brain stimulation electrodes , 2005, Journal of neural engineering.

[9]  Warren M Grill,et al.  Minimally‐invasive electrical stimulation of the pudendal nerve: A pre‐clinical study for neural control of the lower urinary tract , 2007, Neurourology and urodynamics.

[10]  W. D. Martin,et al.  Innervation of feline perineal musculature , 1974, The Anatomical record.

[11]  Warren M Grill,et al.  Activation and inhibition of the micturition reflex by penile afferents in the cat. , 2008, American journal of physiology. Regulatory, integrative and comparative physiology.

[12]  G. Timm,et al.  Sensory innervation of the mammalian urethra. , 1973, Investigative urology.

[13]  Intraurethral stimulation for reflex bladder activation depends on stimulation pattern and location , 2009, Neurourology and urodynamics.

[14]  W. Bradley,et al.  Innervation of the human glans penis. , 1999, The Journal of urology.

[15]  W. Grill,et al.  Functional anatomy of the male feline urethra: morphological and physiological correlations. , 1999, The Journal of urology.

[16]  William C. de Groat,et al.  Histological and Electrical Properties of Rat Dorsal Root Ganglion Neurons Innervating the Lower Urinary Tract , 2003, The Journal of Neuroscience.

[17]  Claire C. Yang,et al.  Peripheral distribution of the human dorsal nerve of the penis. , 1998, The Journal of urology.

[18]  Claire C. Yang,et al.  Innervation of the human anterior urethra by the dorsal nerve of the penis , 1998, Muscle & nerve.

[19]  R. Phillips,et al.  New, simple approach for maximal pudendal nerve exposure , 2000, Diseases of the colon and rectum.

[20]  P. Mahakkanukrauh,et al.  Anatomical study of the pudendal nerve adjacent to the sacrospinous ligament , 2005, Clinical anatomy.

[21]  G. Gebhart,et al.  Characterization of mechanosensitive pelvic nerve afferent fibers innervating the colon of the rat. , 1994, Journal of neurophysiology.

[22]  J. Tjandra,et al.  Anatomy of the pudendal nerve and its terminal branches: a cadaver study , 2004, ANZ journal of surgery.

[23]  F. Rattay Analysis of models for extracellular fiber stimulation , 1989, IEEE Transactions on Biomedical Engineering.

[24]  Warren M Grill,et al.  Dorsal genital nerve stimulation for the treatment of overactive bladder symptoms , 2008, Neurourology and urodynamics.

[25]  Calculation of magnetic field-induced current densities for humans from EAS countertop activation/deactivation devices that use ferromagnetic cores. , 2005, Physics in medicine and biology.

[26]  M. Craggs,et al.  The acute effects of continuous and conditional neuromodulation on the bladder in spinal cord injury , 2001, Spinal Cord.

[27]  Warren M Grill,et al.  A urethral afferent mediated excitatory bladder reflex exists in humans , 2004, Neuroscience Letters.

[28]  Warren M Grill,et al.  Pudendal nerve stimulation evokes reflex bladder contractions in persons with chronic spinal cord injury , 2007, Neurourology and urodynamics.

[29]  W. Bradley,et al.  Neuroanatomy of the penile portion of the human dorsal nerve of the penis. , 1998, British journal of urology.

[30]  O P Gandhi,et al.  Currents induced in anatomic models of the human for uniform and nonuniform power frequency magnetic fields. , 2001, Bioelectromagnetics.

[31]  P. Stark,et al.  Monopolar and bipolar stimulation of the brain. , 1962, The American journal of physiology.

[32]  T. Lue,et al.  Clinical significance of sacral and pudendal nerve anatomy. , 1988, The Journal of urology.