Model-based analysis and design of nerve cuff electrodes for restoring bladder function by selective stimulation of the pudendal nerve

OBJECTIVE Electrical stimulation of the pudendal nerve (PN) is being developed as a means to restore bladder function in persons with spinal cord injury. A single nerve cuff electrode placed on the proximal PN trunk may enable selective stimulation of distinct fascicles to maintain continence or evoke micturition. The objective of this study was to design a nerve cuff that enabled selective stimulation of the PN. APPROACH We evaluated the performance of both flat interface nerve electrode (FINE) cuff and round cuff designs, with a range of FINE cuff heights and number of contacts, as well as multiple contact orientations. This analysis was performed using a computational model, in which the nerve and fascicle cross-sectional positions from five human PN trunks were systematically reshaped within the nerve cuff. These cross-sections were used to create finite element models, with electric potentials calculated and applied to a cable model of a myelinated axon to evaluate stimulation selectivity for different PN targets. Subsequently, the model was coupled to a genetic algorithm (GA) to identify solutions that used multiple contact activation to maximize selectivity and minimize total stimulation voltage. MAIN RESULTS Simulations did not identify any significant differences in selectivity between FINE and round cuffs, although the latter required smaller stimulation voltages for target activation due to preserved localization of targeted fascicle groups. Further, it was found that a ten contact nerve cuff generated sufficient selectivity for all PN targets, with the degree of selectivity dependent on the relative position of the target within the nerve. The GA identified solutions that increased fitness by 0.7-45.5% over single contact activation by decreasing stimulation of non-targeted fascicles. SIGNIFICANCE This study suggests that using an optimal nerve cuff design and multiple contact activation could enable selective stimulation of the human PN trunk for restoration of bladder function.

[1]  W B Shingleton,et al.  The development of urologic complications in relationship to bladder pressure in spinal cord injured patients. , 1993, The Journal of the American Paraplegia Society.

[2]  Dominique M. Durand,et al.  MODELING OF MAMMALIAN MYELINATED NERVE FOR FUNCTIONAL NEUROMUSCULAR STIMULATION. , 1987 .

[3]  W. Grill,et al.  Quantification of recruitment properties of multiple contact cuff electrodes. , 1996, IEEE transactions on rehabilitation engineering : a publication of the IEEE Engineering in Medicine and Biology Society.

[4]  Ronald J. Triolo,et al.  Probabilistic modeling of selective stimulation of the human sciatic nerve with a flat interface nerve electrode , 2012, 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[5]  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.

[6]  D. Durand,et al.  Chronic Response of the Rat Sciatic Nerve to the Flat Interface Nerve Electrode , 2003, Annals of Biomedical Engineering.

[7]  Nicholas T. Carnevale,et al.  The NEURON Simulation Environment , 1997, Neural Computation.

[8]  Warren M Grill,et al.  Energy-efficient waveform shapes for neural stimulation revealed with a genetic algorithm , 2010, Journal of neural engineering.

[9]  Daniel K. Leventhal,et al.  Subfascicle Stimulation Selectivity with the Flat Interface Nerve Electrode , 2003, Annals of Biomedical Engineering.

[10]  W. Grill,et al.  Selective control of muscle activation with a multipolar nerve cuff electrode , 1993, IEEE Transactions on Biomedical Engineering.

[11]  J. B. Ranck,et al.  Specific impedance of rabbit cerebral cortex. , 1963, Experimental neurology.

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

[13]  M. Schiefer,et al.  Fascicular Perineurium Thickness, Size, and Position Affect Model Predictions of Neural Excitation , 2008, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[14]  R. Triolo,et al.  A Model of Selective Activation of the Femoral Nerve With a Flat Interface Nerve Electrode for a Lower Extremity Neuroprosthesis , 2008, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[15]  G. Creasey,et al.  Detrusor and blood pressure responses to dorsal penile nerve stimulation during hyperreflexic contraction of the bladder in patients with cervical cord injury. , 2003, Archives of physical medicine and rehabilitation.

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

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

[18]  M. Chancellor,et al.  Urodynamics of spinal cord injury. , 1996, The Urologic clinics of North America.

[19]  Dominique M. Durand,et al.  Selectivity of multiple-contact nerve cuff electrodes: a simulation analysis , 2001, IEEE Transactions on Biomedical Engineering.

[20]  G. Ayala,et al.  Bladder inhibition with functional electrical stimulation. , 1975, Urology.

[21]  Dominique M. Durand,et al.  Chronic measurement of the stimulation selectivity of the flat interface nerve electrode , 2004, IEEE Transactions on Biomedical Engineering.

[22]  Warren M. Grill,et al.  Fascicular anatomy and surgical access of the human pudendal nerve , 2005, World Journal of Urology.

[23]  M D Craggs,et al.  Emerging clinical applications of electrical stimulation: opportunities for restoration of function. , 2001, Journal of rehabilitation research and development.

[24]  J. B. Ranck,et al.  THE SPECIFIC IMPEDANCE OF THE DORSAL COLUMNS OF CAT: AN INISOTROPIC MEDIUM. , 1965, Experimental neurology.

[25]  D. Durand,et al.  Functionally selective peripheral nerve stimulation with a flat interface nerve electrode , 2002, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[26]  J T Mortimer,et al.  Neural and connective tissue response to long-term implantation of multiple contact nerve cuff electrodes. , 2000, Journal of biomedical materials research.

[27]  W. Grill,et al.  Electrical properties of implant encapsulation tissue , 2006, Annals of Biomedical Engineering.

[28]  M. Keith,et al.  Stimulation Stability and Selectivity of Chronically Implanted Multicontact Nerve Cuff Electrodes in the Human Upper Extremity , 2009, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[29]  R. Saxod,et al.  The density of myelinated fibres is related to the fascicle diameter in human superficial peroneal nerve Statistical study of 41 normal samples , 1985, Journal of the Neurological Sciences.

[30]  L. Geddes,et al.  The specific resistance of biological material—A compendium of data for the biomedical engineer and physiologist , 1967, Medical and biological engineering.

[31]  S. Rapoport,et al.  AC impedance of the perineurium of the frog sciatic nerve. , 1984, Biophysical journal.

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

[33]  Dustin Tyler,et al.  Optimizing nerve cuff stimulation of targeted regions through use of genetic algorithms , 2011, 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

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

[35]  J. Walter,et al.  Management of incontinent SCI patients with penile stimulation: preliminary results. , 1994, The Journal of the American Paraplegia Society.

[36]  Warren M. Grill,et al.  Sensitivity analysis of a model of mammalian neural membrane , 1998, Biological Cybernetics.

[37]  Changfeng Tai,et al.  Plasticity of urinary bladder reflexes evoked by stimulation of pudendal afferent nerves after chronic spinal cord injury in cats , 2011, Experimental Neurology.

[38]  J. Mortimer,et al.  Selective and independent activation of four motor fascicles using a four contact nerve-cuff electrode , 2004, IEEE Transactions on Neural Systems and Rehabilitation Engineering.