Coding strategies in the otolith system differ for translational head motion vs. static orientation relative to gravity
The detection of gravito-inertial forces by the otolith system is essential for our sense of balance and accurate perception. To date, however, how this system encodes the self-motion stimuli that are experienced during everyday activities remains unknown. Here, we addressed this fundamental questio...
| Main Authors: | , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2019-06-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/45573 |
| _version_ | 1818019514142425088 |
|---|---|
| author | Mohsen Jamali Jerome Carriot Maurice J Chacron Kathleen E Cullen |
| author_facet | Mohsen Jamali Jerome Carriot Maurice J Chacron Kathleen E Cullen |
| author_sort | Mohsen Jamali |
| collection | DOAJ |
| description | The detection of gravito-inertial forces by the otolith system is essential for our sense of balance and accurate perception. To date, however, how this system encodes the self-motion stimuli that are experienced during everyday activities remains unknown. Here, we addressed this fundamental question directly by recording from single otolith afferents in monkeys during naturalistic translational self-motion and changes in static head orientation. Otolith afferents with higher intrinsic variability transmitted more information overall about translational self-motion than their regular counterparts, owing to stronger nonlinearities that enabled precise spike timing including phase locking. By contrast, more regular afferents better discriminated between different static head orientations relative to gravity. Using computational methods, we further demonstrated that coupled increases in intrinsic variability and sensitivity accounted for the observed functional differences between afferent classes. Together, our results indicate that irregular and regular otolith afferents use different strategies to encode naturalistic self-motion and static head orientation relative to gravity. |
| first_indexed | 2024-04-14T07:53:19Z |
| format | Article |
| id | doaj.art-eb2a79f62842418da507b090ae301f35 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-14T07:53:19Z |
| publishDate | 2019-06-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-eb2a79f62842418da507b090ae301f352022-12-22T02:05:08ZengeLife Sciences Publications LtdeLife2050-084X2019-06-01810.7554/eLife.45573Coding strategies in the otolith system differ for translational head motion vs. static orientation relative to gravityMohsen Jamali0https://orcid.org/0000-0002-1750-7591Jerome Carriot1Maurice J Chacron2https://orcid.org/0000-0002-3032-452XKathleen E Cullen3https://orcid.org/0000-0002-9348-0933Department of Neurosurgery, Harvard Medical School, Massachusetts General Hospital, Boston, United StatesDepartment of Physiology, McGill University, Montreal, CanadaDepartment of Physiology, McGill University, Montreal, CanadaDepartment of Biomedical Engineering, Johns Hopkins University, Baltimore, United StatesThe detection of gravito-inertial forces by the otolith system is essential for our sense of balance and accurate perception. To date, however, how this system encodes the self-motion stimuli that are experienced during everyday activities remains unknown. Here, we addressed this fundamental question directly by recording from single otolith afferents in monkeys during naturalistic translational self-motion and changes in static head orientation. Otolith afferents with higher intrinsic variability transmitted more information overall about translational self-motion than their regular counterparts, owing to stronger nonlinearities that enabled precise spike timing including phase locking. By contrast, more regular afferents better discriminated between different static head orientations relative to gravity. Using computational methods, we further demonstrated that coupled increases in intrinsic variability and sensitivity accounted for the observed functional differences between afferent classes. Together, our results indicate that irregular and regular otolith afferents use different strategies to encode naturalistic self-motion and static head orientation relative to gravity.https://elifesciences.org/articles/45573otolith afferentsself-motiontilttranslationneural codingspike timing |
| spellingShingle | Mohsen Jamali Jerome Carriot Maurice J Chacron Kathleen E Cullen Coding strategies in the otolith system differ for translational head motion vs. static orientation relative to gravity eLife otolith afferents self-motion tilt translation neural coding spike timing |
| title | Coding strategies in the otolith system differ for translational head motion vs. static orientation relative to gravity |
| title_full | Coding strategies in the otolith system differ for translational head motion vs. static orientation relative to gravity |
| title_fullStr | Coding strategies in the otolith system differ for translational head motion vs. static orientation relative to gravity |
| title_full_unstemmed | Coding strategies in the otolith system differ for translational head motion vs. static orientation relative to gravity |
| title_short | Coding strategies in the otolith system differ for translational head motion vs. static orientation relative to gravity |
| title_sort | coding strategies in the otolith system differ for translational head motion vs static orientation relative to gravity |
| topic | otolith afferents self-motion tilt translation neural coding spike timing |
| url | https://elifesciences.org/articles/45573 |
| work_keys_str_mv | AT mohsenjamali codingstrategiesintheotolithsystemdifferfortranslationalheadmotionvsstaticorientationrelativetogravity AT jeromecarriot codingstrategiesintheotolithsystemdifferfortranslationalheadmotionvsstaticorientationrelativetogravity AT mauricejchacron codingstrategiesintheotolithsystemdifferfortranslationalheadmotionvsstaticorientationrelativetogravity AT kathleenecullen codingstrategiesintheotolithsystemdifferfortranslationalheadmotionvsstaticorientationrelativetogravity |