Directional Plasticity Rapidly Improves 3D Vestibulo-Ocular Reflex Alignment in Monkeys Using a Multichannel Vestibular Prosthesis

Directional Plasticity Rapidly Improves 3D Vestibulo-Ocular Reflex Alignment in Monkeys Using a Multichannel Vestibular Prosthesis
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DOI:
10.1007/s10162-013-0413-0
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发表时间:
2013-12-01
影响因子:
2.4
通讯作者:
Della Santina, Charles C.
Della Santina, Charles C.
中科院分区:
医学2区
文献类型:
--
作者:
Dai, Chenkai;Fridman, Gene Y.;Della Santina, Charles C.

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双侧前庭感觉丧失可能导致残疾。我们已经证明,多通道前庭假体(MVP)可以部分恢复前庭感觉,证明了三维角前庭眼反射(3D VOR)的改善。然而,一个关键的挑战是最大限度地减少眼睛和头部旋转轴之间的不对准,这显然是由电流扩散到每个电极的目标神经分支之外引起的。我们最近报道,啮齿动物穿着MVP显着改善3D VOR对齐在MVP激活后的第一周,可能通过相同的中枢神经系统的适应机制,介导跨轴适应随着时间的推移,在正常人穿着棱镜,导致视觉场景运动的轴不同于头部旋转轴。我们假设,恒河猴将表现出类似的改善与持续假体刺激随着时间的推移。我们通过鼓室内注射庆大霉素在四只恒河猴中建立了双侧前庭缺陷。将MVP安装到颅骨,并在连续头部运动调制的假体电刺激的1周内重复测量响应于黑暗中的全身被动旋转的眼球运动。在慢性刺激的第1、3和7天测量围绕每个半规管轴的全身旋转的3D VOR反应。在开启假体之前,1 Hz、50 A度/s峰值全身旋转期间的水平VOR增益< 0.1,这远远低于正常值(0.94 A +/- 0.12)。在刺激第1天,VOR增益为0.4-0.8,但观察到的眼球运动的轴与头部旋转对准不良(未对准范围类似于30-40 A度)。在正常昼夜光照下连续运动调制假体刺激7天后,观察到轴不对准的实质性改善。所有动物、所有三个旋转轴、所有正弦频率(0.05-5 Hz)和高加速度瞬时旋转均观察到类似改善。VOR不对称性变化没有达到统计学显著性,尽管随着时间的推移,它们确实有轻微改善的趋势。先前的研究已经表明,当一个具有正常视皮层的受试者看到异常的视觉场景运动时,方向可塑性减少了错位。我们的研究结果表明,匡威也是正确的:在正常的观看条件下接受定向错误的前庭感觉的个人迅速适应恢复对齐良好的3D VOR。考虑到VOR生理学在灵长类物种中的相似性,使用MVP治疗双侧前庭缺陷的人类可能会出现类似的效果。
Bilateral loss of vestibular sensation can be disabling. We have shown that a multichannel vestibular prosthesis (MVP) can partly restore vestibular sensation as evidenced by improvements in the 3-dimensional angular vestibulo-ocular reflex (3D VOR). However, a key challenge is to minimize misalignment between the axes of eye and head rotation, which is apparently caused by current spread beyond each electrode's targeted nerve branch. We recently reported that rodents wearing a MVP markedly improve 3D VOR alignment during the first week after MVP activation, probably through the same central nervous system adaptive mechanisms that mediate cross-axis adaptation over time in normal individuals wearing prisms that cause visual scene movement about an axis different than the axis of head rotation. We hypothesized that rhesus monkeys would exhibit similar improvements with continuous prosthetic stimulation over time. We created bilateral vestibular deficiency in four rhesus monkeys via intratympanic injection of gentamicin. A MVP was mounted to the cranium, and eye movements in response to whole-body passive rotation in darkness were measured repeatedly over 1 week of continuous head motion-modulated prosthetic electrical stimulation. 3D VOR responses to whole-body rotations about each semicircular canal axis were measured on days 1, 3, and 7 of chronic stimulation. Horizontal VOR gain during 1 Hz, 50 A degrees/s peak whole-body rotations before the prosthesis was turned on was < 0.1, which is profoundly below normal (0.94 A +/- 0.12). On stimulation day 1, VOR gain was 0.4-0.8, but the axis of observed eye movements aligned poorly with head rotation (misalignment range similar to 30-40 A degrees). Substantial improvement of axis misalignment was observed after 7 days of continuous motion-modulated prosthetic stimulation under normal diurnal lighting. Similar improvements were noted for all animals, all three axes of rotation tested, for all sinusoidal frequencies tested (0.05-5 Hz), and for high-acceleration transient rotations. VOR asymmetry changes did not reach statistical significance, although they did trend toward slight improvement over time. Prior studies had already shown that directional plasticity reduces misalignment when a subject with normal labyrinths views abnormal visual scene movement. Our results show that the converse is also true: individuals receiving misoriented vestibular sensation under normal viewing conditions rapidly adapt to restore a well-aligned 3D VOR. Considering the similarity of VOR physiology across primate species, similar effects are likely to occur in humans using a MVP to treat bilateral vestibular deficiency.