TY - JOUR
T1 - Cross-axis adaptation improves 3D vestibulo-ocular reflex alignment during chronic stimulation via a head-mounted multichannel vestibular prosthesis
AU - Dai, Chenkai
AU - Fridman, Gene Y.
AU - Chiang, Bryce
AU - Davidovics, Natan S.
AU - Melvin, Thuy Anh
AU - Cullen, Kathleen E.
AU - Della Santina, Charles C.
N1 - Funding Information:
Acknowledgments We thank Lani Swarthout for assistance with animal care. This work was funded by NIH NIDCD grants R01DC009255, K08DC6216, R01DC2390, and 5F32DC009917. CDS, GYF, and BC are inventors on pending and awarded patents relevant to prosthesis technology, and CDS holds an equity interest in Labyrinth Devices LLC.
PY - 2011/5
Y1 - 2011/5
N2 - By sensing three-dimensional (3D) head rotation and electrically stimulating the three ampullary branches of a vestibular nerve to encode head angular velocity, a multichannel vestibular prosthesis (MVP) can restore vestibular sensation to individuals disabled by loss of vestibular hair cell function. However, current spread to afferent fibers innervating non-targeted canals and otolith end organs can distort the vestibular nerve activation pattern, causing misalignment between the perceived and actual axis of head rotation. We hypothesized that over time, central neural mechanisms can adapt to correct this misalignment. To test this, we rendered five chinchillas vestibular deficient via bilateral gentamicin treatment and unilaterally implanted them with a head-mounted MVP. Comparison of 3D angular vestibulo-ocular reflex (aVOR) responses during 2 Hz, 50°/s peak horizontal sinusoidal head rotations in darkness on the first, third, and seventh days of continual MVP use revealed that eye responses about the intended axis remained stable (at about 70% of the normal gain) while misalignment improved significantly by the end of 1 week of prosthetic stimulation. A comparable time course of improvement was also observed for head rotations about the other two semicircular canal axes and at every stimulus frequency examined (0.2-5 Hz). In addition, the extent of disconjugacy between the two eyes progressively improved during the same time window. These results indicate that the central nervous system rapidly adapts to multichannel prosthetic vestibular stimulation to markedly improve 3D aVOR alignment within the first week after activation. Similar adaptive improvements are likely to occur in other species, including humans.
AB - By sensing three-dimensional (3D) head rotation and electrically stimulating the three ampullary branches of a vestibular nerve to encode head angular velocity, a multichannel vestibular prosthesis (MVP) can restore vestibular sensation to individuals disabled by loss of vestibular hair cell function. However, current spread to afferent fibers innervating non-targeted canals and otolith end organs can distort the vestibular nerve activation pattern, causing misalignment between the perceived and actual axis of head rotation. We hypothesized that over time, central neural mechanisms can adapt to correct this misalignment. To test this, we rendered five chinchillas vestibular deficient via bilateral gentamicin treatment and unilaterally implanted them with a head-mounted MVP. Comparison of 3D angular vestibulo-ocular reflex (aVOR) responses during 2 Hz, 50°/s peak horizontal sinusoidal head rotations in darkness on the first, third, and seventh days of continual MVP use revealed that eye responses about the intended axis remained stable (at about 70% of the normal gain) while misalignment improved significantly by the end of 1 week of prosthetic stimulation. A comparable time course of improvement was also observed for head rotations about the other two semicircular canal axes and at every stimulus frequency examined (0.2-5 Hz). In addition, the extent of disconjugacy between the two eyes progressively improved during the same time window. These results indicate that the central nervous system rapidly adapts to multichannel prosthetic vestibular stimulation to markedly improve 3D aVOR alignment within the first week after activation. Similar adaptive improvements are likely to occur in other species, including humans.
KW - Adaptation
KW - Areflexia
KW - Bilateral vestibular deficiency
KW - Electrical stimulation
KW - Vestibular implant
KW - Vestibular nerve
KW - Vestibular prosthesis
KW - Vestibulo-ocular reflex, VOR, labyrinth
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U2 - 10.1007/s00221-011-2591-5
DO - 10.1007/s00221-011-2591-5
M3 - Article
C2 - 21374081
AN - SCOPUS:79954862929
VL - 210
SP - 595
EP - 606
JO - Experimental Brain Research
JF - Experimental Brain Research
SN - 0014-4819
IS - 3-4
ER -