Department of Biomedical Engineering, Johns Hopkins University School of Medicine; Baltimore, Maryland, United States of America.
Kavli Neuroscience Discovery Institute, Johns Hopkins University; Baltimore, Maryland, United States of America.
PLoS Biol. 2022 Sep 14;20(9):e3001798. doi: 10.1371/journal.pbio.3001798. eCollection 2022 Sep.
Sensory pathways provide complex and multifaceted information to the brain. Recent advances have created new opportunities for applying our understanding of the brain to sensory prothesis development. Yet complex sensor physiology, limited numbers of electrodes, and nonspecific stimulation have proven to be a challenge for many sensory systems. In contrast, the vestibular system is uniquely suited for prosthesis development. Its peripheral anatomy allows site-specific stimulation of 3 separate sensory organs that encode distinct directions of head motion. Accordingly, here, we investigated whether implementing natural encoding strategies improves vestibular prosthesis performance. The eye movements produced by the vestibulo-ocular reflex (VOR), which plays an essential role in maintaining visual stability, were measured to quantify performance. Overall, implementing the natural tuning dynamics of vestibular afferents produced more temporally accurate VOR eye movements. Exploration of the parameter space further revealed that more dynamic tunings were not beneficial due to saturation and unnatural phase advances. Trends were comparable for stimulation encoding virtual versus physical head rotations, with gains enhanced in the latter case. Finally, using computational methods, we found that the same simple model explained the eye movements evoked by sinusoidal and transient stimulation and that a stimulation efficacy substantially less than 100% could account for our results. Taken together, our results establish that prosthesis encodings that incorporate naturalistic afferent dynamics and account for activation efficacy are well suited for restoration of gaze stability. More generally, these results emphasize the benefits of leveraging the brain's endogenous coding strategies in prosthesis development to improve functional outcomes.
感觉通路为大脑提供复杂多样的信息。最近的进展为我们将对大脑的理解应用于感官假体开发创造了新的机会。然而，复杂的传感器生理学、电极数量有限和非特异性刺激已被证明是许多感觉系统的挑战。相比之下，前庭系统非常适合假体开发。其外围解剖结构允许对编码头部运动不同方向的 3 个独立感觉器官进行特定部位的刺激。因此，在这里，我们研究了实施自然编码策略是否能提高前庭假体的性能。通过测量前庭眼反射（VOR）产生的眼球运动来量化性能，VOR 在维持视觉稳定性方面起着至关重要的作用。总的来说，实施前庭传入的自然调谐动力学产生了更准确的 VOR 眼球运动。对参数空间的进一步探索表明，由于饱和和不自然的相位超前，更动态的调谐没有好处。刺激编码虚拟与物理头部旋转的趋势相当，在后一种情况下增益增强。最后，使用计算方法，我们发现相同的简单模型可以解释正弦和瞬态刺激引起的眼球运动，并且刺激效率远低于 100%可以解释我们的结果。总之，我们的结果表明，将包含自然传入动力学并考虑到激活效率的假体编码用于恢复凝视稳定性是合适的。更广泛地说，这些结果强调了在假体开发中利用大脑内源性编码策略来提高功能结果的好处。
