A prosthesis utilizing natural vestibular encoding strategies improves sensorimotor performance in monkeys.
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 prov...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2022-09-01
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| Series: | PLoS Biology |
| Online Access: | https://doi.org/10.1371/journal.pbio.3001798 |
| _version_ | 1811181994427547648 |
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| author | Kantapon Pum Wiboonsaksakul Dale C Roberts Charles C Della Santina Kathleen E Cullen |
| author_facet | Kantapon Pum Wiboonsaksakul Dale C Roberts Charles C Della Santina Kathleen E Cullen |
| author_sort | Kantapon Pum Wiboonsaksakul |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-11T09:24:28Z |
| format | Article |
| id | doaj.art-3630fd5a23e64be980e36dfec8ffdfaa |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-04-11T09:24:28Z |
| publishDate | 2022-09-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-3630fd5a23e64be980e36dfec8ffdfaa2022-12-22T04:32:03ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852022-09-01209e300179810.1371/journal.pbio.3001798A prosthesis utilizing natural vestibular encoding strategies improves sensorimotor performance in monkeys.Kantapon Pum WiboonsaksakulDale C RobertsCharles C Della SantinaKathleen E CullenSensory 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.https://doi.org/10.1371/journal.pbio.3001798 |
| spellingShingle | Kantapon Pum Wiboonsaksakul Dale C Roberts Charles C Della Santina Kathleen E Cullen A prosthesis utilizing natural vestibular encoding strategies improves sensorimotor performance in monkeys. PLoS Biology |
| title | A prosthesis utilizing natural vestibular encoding strategies improves sensorimotor performance in monkeys. |
| title_full | A prosthesis utilizing natural vestibular encoding strategies improves sensorimotor performance in monkeys. |
| title_fullStr | A prosthesis utilizing natural vestibular encoding strategies improves sensorimotor performance in monkeys. |
| title_full_unstemmed | A prosthesis utilizing natural vestibular encoding strategies improves sensorimotor performance in monkeys. |
| title_short | A prosthesis utilizing natural vestibular encoding strategies improves sensorimotor performance in monkeys. |
| title_sort | prosthesis utilizing natural vestibular encoding strategies improves sensorimotor performance in monkeys |
| url | https://doi.org/10.1371/journal.pbio.3001798 |
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