Selectivity of afferent microstimulation at the DRG using epineural and penetrating electrode arrays

Abstract

Objective: We have shown previously that microstimulation of the lumbar dorsal root ganglia (L5-L7 DRG) using penetrating microelectrodes, selectively recruits distal branches of the sciatic and femoral nerves in an acute preparation. However, a variety of challenges limit the clinical translatability of DRG microstimulation via penetrating electrodes. For clinical translation of a DRG somatosensory neural interface, electrodes placed on the epineural surface of the DRG may be a viable path forward. The goal of this study was to evaluate the recruitment properties of epineural electrodes and compare their performance with that of penetrating electrodes. Here, we compare the number of selectively recruited distal nerve branches and the threshold stimulus intensities between penetrating and epineural electrode arrays.

Approach: Antidromically propagating action potentials were recorded from multiple distal branches of the femoral and sciatic nerves in response to epineural stimulation on 11 ganglia in four cats to quantify the selectivity of DRG stimulation. Compound action potentials (CAPs) were recorded using nerve cuff electrodes implanted around up to nine distal branches of the femoral and sciatic nerve trunks. We also tested stimulation selectivity with penetrating microelectrode arrays implanted into ten ganglia in four cats. A binary search was carried out to identify the minimum stimulus intensity that evoked a response at any of the distal cuffs, as well as whether the threshold response selectively occurred in only a single distal nerve branch.

Main results: Stimulation evoked activity in just a single peripheral nerve through 67% of epineural electrodes (35/52) and through 79% of the penetrating microelectrodes (240/308). The recruitment threshold (median = 9.67 nC/phase) and dynamic range of epineural stimulation (median = 1.01 nC/phase) were significantly higher than penetrating stimulation (0.90 nC/phase and 0.36 nC/phase, respectively). However, the pattern of peripheral nerves recruited for each DRG were similar for stimulation through epineural and penetrating electrodes.

Significance: Despite higher recruitment thresholds, epineural stimulation provides comparable selectivity and superior dynamic range to penetrating electrodes. These results suggest that it may be possible to achieve a highly selective neural interface with the DRG without penetrating the epineurium.

Figure 1.

(A) Placement of Ripple stimulation electrodes on the epineurium of the L5 and L6 DRG (left) along with a representation of the 2 epineural electrode designs and images of 32-channel UEA and FMAs (right). (B) Schematic of nerve cuff location in the left hindlimb. (C) Nerve cuffs and book electrodes implanted on the sciatic trunk and distal branches. (D) Summary of nerves instrumented and DRG stimulation electrodes used across 6 acute experiments. Hatching represents instances where a nerve was not instrumented or a DRG stimulation electrode was not used. (E) Example stimulation triggered average ENG recorded from the sciatic nerve and its common peroneal (middle) and tibial (bottom) branches.

Figure 2.

Count of nerves coactivated at threshold per DRG for stimulation via (A) epineural and (B) penetrating electrodes. Dashed line indicates division between femoral and sciatic nerve branches. Rows represent the nerves recruited and columns represent the nerves coactivated at threshold.

Figure 3.

(A) Counts of selectively recruited nerves for stimulation via epineural and penetrating electrodes at each DRG. (B) Counts for selective recruitment, non-selective recruitment and coactivation of agonists at threshold. Counts for selective recruitment were obtained by adding the counts at each DRG for each nerve in (A). Nerves in the same innervation path (e.g. tibial and distal tibial) were allowed to be coactivated while still being considered selective; however, only activation of the distal most nerve was counted to highlight differential recruitment of proximal branches.

Figure 4.

(A) Distribution of selective recruitment thresholds for stimulation via epineural (median = 9.67 nC/phase) and penetrating (median = 0.905 nC/phase) electrodes. B) Distribution of dynamic range for selective recruitment for epineural (median = 1.01 nC/phase) and penetrating (median = 0.36 nC/phase) stimulation. Dashed lines show median for each plot.

Figure 5.

Comparison of stimulation charge injected and the CV of the nerve cuff response recorded across all stimulation amplitudes (blue) and at recruitment threshold (orange) for stimulation via (A) epineural and (B) penetrating electrodes at the lumbar DRG. CV values were discretized due to sampling frequency limitations of the recording setup. The vertical grey bars indicate the range of CVs corresponding to group I, Aβ and II afferents.