A multichannel semicircular canal neural prosthesis using electrical stimulation to restore 3-d vestibular sensation

Abstract

Bilateral loss of vestibular sensation can be disabling. Those afflicted suffer illusory visual field movement during head movements, chronic disequilibrium and postural instability due to failure of vestibulo-ocular and vestibulo-spinal reflexes. A neural prosthesis that emulates the normal transduction of head rotation by semicircular canals could significantly improve quality of life for these patients. Like the three semicircular canals in a normal ear, such a device should at least transduce three orthogonal (or linearly separable) components of head rotation into activity on corresponding ampullary branches of the vestibular nerve. We describe the design, circuit performance and in vivo application of a head-mounted, semi-implantable multichannel vestibular prosthesis that encodes head movement in three dimensions as pulse-frequency-modulated electrical stimulation of three or more ampullary nerves. In chinchillas treated with intratympanic gentamicin to ablate vestibular sensation bilaterally, prosthetic stimuli elicited a partly compensatory angular vestibulo-ocular reflex in multiple planes. Minimizing misalignment between the axis of eye and head rotation, apparently caused by current spread beyond each electrode's targeted nerve branch, emerged as a key challenge. Increasing stimulation selectivity via improvements in electrode design, surgical technique and stimulus protocol will likely be required to restore AVOR function over the full range of normal behavior.

Figures

Figure 1

Head coordinate system used for head and eye rotation data. When the animal is positioned in a holder that pitches the occlusal plane 50° nose down, the Z plane (approximating the horizontal SCCs) is Earth-horizontal, the Y (pitch) plane is midsagittal, the X (roll) plane is perpendicular to the Y and Z planes, the intersection of the X and Z planes is along the interaural axis, and the origin of the coordinate system is centered on the Earth-vertical axis of the motor that rotates the animal. The X, Y and Z axis positive tips are anterior, left and superior, respectively. We approximated the positive left-anterior/right-posterior (LARP) axis normal to the LARP plane as (X,Y,Z)=(1,−1,0), and the right-anterior/left-posterior (RALP) axis as (X,Y,Z)=(1,1,0). Right-hand-rule rotations about an axis’ positive tip (dashed arrows) are positive polarity. Solid arrows show sense of head rotations that excite the left labyrinth’s SCCs while inhibiting the coplanar right SCCs.

Figure 2

Conceptual diagram of prosthesis circuitry. Three mutually orthogonal gyro sensors aligned with the horizontal, anterior and posterior semicircular canals of the left labyrinth measure head rotation about the head axes shown (dashed lines with open arrows). Head rotation in the sense shown by black arrows “excites” a higher pulse rate on the corresponding gyro’s channel. Gyro signals are digitized within the MSP430 microcontroller’s analog-digital converter module, then optionally filtered and/or transformed via a coordinate system rotation to account for misalignment of gyros with SCCs. Resulting signals set the frequency modulation of biphasic pulses according to a sigmoid operating curve (Figure 3). A 3-channel digital-analog converter sets command current for a shared current source, which switches between pairs of electrodes to generate the cathodic phase of a pulse and then a charge-recovery anodic phase with oppositely directly current through the same electrode pair. All parameters may be set through a JTAG programming interface or RS-232 serial interface with the device in situ.

Figure 3

Prosthesis pulse rate versus head velocity operating characteristic curves defined by Equation 1 with resting rate 100 pulse/s, max rate 350 pulse/s, and compression factor C of 1, 2, 5, or 10.

Figure 4

Prosthesis circuitry. Arrows = gyro rate sensors, two of which are on boards perpendicular to the mother board. Scale = cm.

Figure 5

(A) Pulse rates on each of 3 electrode channels (LH = left horizontal SCC, LA = left anterior, LP = left posterior) encoding components of 3 different 2 Hz, 50 deg/s rotations of the device on the animal’s head about each axis. (B) Biphasic stimulus current delivered via one pair of the electrodes immersed in 0.9% NaCl during 240 μA/phase pulses of 50, 120 and 200 μs/phase, with cathodic-to-anodic intrapulse interval set to 10% of the duration of each phase.

Figure 6

(Column 1) Mean head rotation and eye rotations of a normal chinchilla (ch090303) during 2 Hz, 50°/s head rotations without vision, in horizontal (top), LARP (middle) and RALP (bottom) planes. This animal’s gains were higher than average. For all panels, a sinusoid indicating the grand mean response of all 5 normal animals to 2 Hz, 50°/s head rotation in the appropriate plane (thin dotted line) is shown for comparison; number of cycles pooled is listed; standard deviation of each trace at each time point is < 5°/s, head or eye traces are inverted as required to facilitate visual comparison; the sense of head rotation is listed in each panel. (Column 2) Responses under same testing conditions for chinchilla treated bilaterally with gentamicin and then implanted with electrodes in the 3 left SCC’s (ch050506B), with prosthetic stimulation off. (Column 3) Responses of ch050506B to same head rotations, 3.5 hrs after activation of the multichannel prosthesis (parameters in text). (Column 4) Responses of ch072106 5 days hrs after activation. (Column 5) Responses of ch071405 3 days hrs after activation.

Figure 7

Mean gain (top) and phase lead (bottom) of eye versus the ideal response (−1 × head velocity) for the horizontal component of 3D angular AVOR for 5 normal chinchillas during 50°/s peak horizontal passive head rotation in darkness (circles) and for 3 bilaterally gentamicin-treated chinchillas during prosthetic stimulation encoding 50°/s horizontal passive head rotations (triangles). Error bars denote ±1SD. Only 1 animal yielded data for electrical stimulation at 15 Hz. The prosthetic stimulation responses have a shallower slope of gain versus frequency (nearly 0.5 on a log-log plot) and an upward shift in phase lead compared to normal. Gains for bilaterally-gentamicin-treated animals without prosthetic stimulation were below the physiologic and measurement noise of the recording system.

Figure 8

(A & B) Horizontal components of left and right eye rotational velocity for the same chinchilla as Figure 1, Columns 2 and 3 (ch050506B), during 2Hz 50°/s peak sinusoidal horizontal head rotations without (A, t<55.7 sec) and then with (A, t>55.7 sec) prosthetic electrical stimulation pulse-frequency-modulated by horizontal head velocity. Only the left horizontal SCC electrodes were activated. Stimulus parameters: cathodic-first biphasic pulses, bipolar electrode pair in the left horizontal SCC ampulla, 150 μA/phase, 200 μs/phase, fpeak 300 pulse/s, fbaseline 100, C=5. Head rotation without electrical stimulation elicited no AVOR. Onset of electrical stimulation produced brisk, asymmetric horizontal nystagmus. (B) Slow phase nystagmus is already more symmetric in direction <20 sec after onset, tracking horizontal head velocity with a mean gain for the each eye similar to the mean response for normal animals (dashed gray line). (C) Mean±1SD cycle-by-cycle average for horizontal, LARP and RALP components for both eyes over the 17 cycles beginning at t=67 of the trial shown in A & B.

Figure 8

(A & B) Horizontal components of left and right eye rotational velocity for the same chinchilla as Figure 1, Columns 2 and 3 (ch050506B), during 2Hz 50°/s peak sinusoidal horizontal head rotations without (A, t<55.7 sec) and then with (A, t>55.7 sec) prosthetic electrical stimulation pulse-frequency-modulated by horizontal head velocity. Only the left horizontal SCC electrodes were activated. Stimulus parameters: cathodic-first biphasic pulses, bipolar electrode pair in the left horizontal SCC ampulla, 150 μA/phase, 200 μs/phase, fpeak 300 pulse/s, fbaseline 100, C=5. Head rotation without electrical stimulation elicited no AVOR. Onset of electrical stimulation produced brisk, asymmetric horizontal nystagmus. (B) Slow phase nystagmus is already more symmetric in direction <20 sec after onset, tracking horizontal head velocity with a mean gain for the each eye similar to the mean response for normal animals (dashed gray line). (C) Mean±1SD cycle-by-cycle average for horizontal, LARP and RALP components for both eyes over the 17 cycles beginning at t=67 of the trial shown in A & B.

Figure 9

AVOR responses during a 2 Hz, 50°/s RALP head rotation of ch050506B encoded by prosthetic stimulation delivered by a monopolar electrode in the LP SCC ampulla with respect to a distant reference. For each panel, stimulus current is labeled; all other parameters were kept constant (fbaseline 100, fpeak 350, C=5, 200 us/phase, cathodic first). In each, the ordinate axis and inverted head velocity trace have been scaled to enhance visibility all components of the response. Barely visible at 50 μA, the response at 100 μA includes conjugate RALP rotations similar to normal chinchilla responses, except for a horizontal component that could indicate horizontal SCC ampulla or otolith nerve stimulation. At 250 μA, the LP response has grown to over 150°/s peak velocity, but the spurious horizontal component nearly equals it.