Distribution of bladder afferent activity across the sacral roots in sheep shows marked individual variation: implications for neuroprosthesis design.

Objective: Implantable sacral anterior root stimulators enable bladder emptying after spinal cord injury but do not prevent reflex incontinence. A closed-loop neuroprosthesis that detects and inhibits reflex bladder contractions could address this, but first, reliable detection of bladder fullness from the sacral roots. Further, the distribution of afferent bladder activity between sacral roots, and the relationship between efferent and afferent activity within each root, remains unclear and must be clarified to guide implant design. Methods: Electrode books were implanted on the S1-S3 extra-dural sacral roots bilaterally in six terminally anesthetized sheep. Afferent electroneurogram (ENG) was recorded concurrently from all implanted roots during filling cystometries and correlated with bladder pressure. Each root was individually electrically stimulated and the bladder pressure response recorded. Post-mortem morphometric analysis determined fiber size distribution in each root. Results: Overall, S2 ENG activity showed the highest correlation with bladder pressure, and electrical stimulation of S2 and S3 produced the greatest increases in bladder pressure. Fiber size distribution did not correlate with either ENG activity or bladder pressure response. Significant variation was identified between individual sheep, but notably, in four of six sheep, a single sacral root had both the highest ENG correlation to bladder pressure and the greatest bladder response to stimulation. Significance: This study demonstrates reliable recording of bladder afferents from sacral roots using clinically applicable electrodes. It provides the first systematic recording of bladder ENG concurrently across three pairs of sacral roots in multiple animals, and the first characterization of signal distribution between roots. Significant individual variation is identified, impacting the design of future implantable sacral neuroprostheses for bladder control.