Otoacoustic emissions but not behavioral measurements predict cochlear nerve frequency tuning in an avian vocal communication specialist
Frequency analysis by the cochlea forms a key foundation for all subsequent auditory processing. Stimulus-frequency otoacoustic emissions (SFOAEs) are a potentially powerful alternative to traditional behavioral experiments for estimating cochlear tuning without invasive testing, as is necessary in...
Saved in:
| Main Authors: | , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
eLife Sciences Publications Ltd
2025-06-01
|
| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/102911 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1849410136037130240 |
|---|---|
| author | Diana M Karosas Leslie Gonzales Yingxuan Wang Christopher Bergevin Laurel H Carney Kenneth S Henry |
| author_facet | Diana M Karosas Leslie Gonzales Yingxuan Wang Christopher Bergevin Laurel H Carney Kenneth S Henry |
| author_sort | Diana M Karosas |
| collection | DOAJ |
| description | Frequency analysis by the cochlea forms a key foundation for all subsequent auditory processing. Stimulus-frequency otoacoustic emissions (SFOAEs) are a potentially powerful alternative to traditional behavioral experiments for estimating cochlear tuning without invasive testing, as is necessary in humans. Which methods accurately predict cochlear tuning remains controversial due to only a single animal study comparing SFOAE-based, behavioral, and cochlear frequency tuning in the same species. The budgerigar (Melopsittacus undulatus) is a parakeet species with human-like behavioral sensitivity to many sounds and the capacity to mimic speech. Intriguingly, previous studies of critical bands, psychophysical tuning curves, and critical ratios in budgerigars show that behavioral tuning sharpness increases dramatically with increasing frequency from 1 to 3.5 kHz, doubling once per octave with peak tuning sharpness from 3.5 to 4 kHz. The pattern contrasts with slower monotonic growth of behavioral tuning sharpness with increasing frequency in other animals, including most avian species, suggesting a possible auditory specialization in budgerigars. We measured SFOAE-based and cochlear-afferent tuning in budgerigars, for comparison to previously reported behavioral results. SFOAE-based and cochlear-afferent tuning sharpness both increased monotonically and relatively slowly for higher frequencies, in contrast to the behavioral pattern. SFOAE-based tuning in budgerigars accurately predicted cochlear frequency tuning, and both measures aligned with typical patterns of cochlear tuning in other species. Divergent behavioral tuning in budgerigars is unlikely attributable to the periphery and could reflect specializations for central processing of masked signals. Our findings highlight the value of SFOAEs for estimating cochlear tuning and caution against direct inference of peripheral tuning from behavioral critical bands, psychophysical tuning curves, and critical ratios. |
| format | Article |
| id | doaj-art-1b8b6036ede54bb79be947f797e07fcf |
| institution | Kabale University |
| issn | 2050-084X |
| language | English |
| publishDate | 2025-06-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj-art-1b8b6036ede54bb79be947f797e07fcf2025-08-20T03:35:15ZengeLife Sciences Publications LtdeLife2050-084X2025-06-011310.7554/eLife.102911Otoacoustic emissions but not behavioral measurements predict cochlear nerve frequency tuning in an avian vocal communication specialistDiana M Karosas0Leslie Gonzales1Yingxuan Wang2Christopher Bergevin3https://orcid.org/0000-0002-4529-399XLaurel H Carney4Kenneth S Henry5https://orcid.org/0000-0003-1364-318XDepartment of Biomedical Engineering, University of Rochester, Rochester, United StatesDepartment of Neuroscience, University of Rochester, Rochester, United StatesDepartment of Biomedical Engineering, University of Rochester, Rochester, United StatesDepartment of Physics and Astronomy, York University, Toronto, CanadaDepartment of Biomedical Engineering, University of Rochester, Rochester, United States; Department of Neuroscience, University of Rochester, Rochester, United StatesDepartment of Biomedical Engineering, University of Rochester, Rochester, United States; Department of Neuroscience, University of Rochester, Rochester, United States; Department of Otolaryngology, University of Rochester, Rochester, United StatesFrequency analysis by the cochlea forms a key foundation for all subsequent auditory processing. Stimulus-frequency otoacoustic emissions (SFOAEs) are a potentially powerful alternative to traditional behavioral experiments for estimating cochlear tuning without invasive testing, as is necessary in humans. Which methods accurately predict cochlear tuning remains controversial due to only a single animal study comparing SFOAE-based, behavioral, and cochlear frequency tuning in the same species. The budgerigar (Melopsittacus undulatus) is a parakeet species with human-like behavioral sensitivity to many sounds and the capacity to mimic speech. Intriguingly, previous studies of critical bands, psychophysical tuning curves, and critical ratios in budgerigars show that behavioral tuning sharpness increases dramatically with increasing frequency from 1 to 3.5 kHz, doubling once per octave with peak tuning sharpness from 3.5 to 4 kHz. The pattern contrasts with slower monotonic growth of behavioral tuning sharpness with increasing frequency in other animals, including most avian species, suggesting a possible auditory specialization in budgerigars. We measured SFOAE-based and cochlear-afferent tuning in budgerigars, for comparison to previously reported behavioral results. SFOAE-based and cochlear-afferent tuning sharpness both increased monotonically and relatively slowly for higher frequencies, in contrast to the behavioral pattern. SFOAE-based tuning in budgerigars accurately predicted cochlear frequency tuning, and both measures aligned with typical patterns of cochlear tuning in other species. Divergent behavioral tuning in budgerigars is unlikely attributable to the periphery and could reflect specializations for central processing of masked signals. Our findings highlight the value of SFOAEs for estimating cochlear tuning and caution against direct inference of peripheral tuning from behavioral critical bands, psychophysical tuning curves, and critical ratios.https://elifesciences.org/articles/102911budgerigarotoacoustic emissionauditory-nervefrequency tuningcochlea |
| spellingShingle | Diana M Karosas Leslie Gonzales Yingxuan Wang Christopher Bergevin Laurel H Carney Kenneth S Henry Otoacoustic emissions but not behavioral measurements predict cochlear nerve frequency tuning in an avian vocal communication specialist eLife budgerigar otoacoustic emission auditory-nerve frequency tuning cochlea |
| title | Otoacoustic emissions but not behavioral measurements predict cochlear nerve frequency tuning in an avian vocal communication specialist |
| title_full | Otoacoustic emissions but not behavioral measurements predict cochlear nerve frequency tuning in an avian vocal communication specialist |
| title_fullStr | Otoacoustic emissions but not behavioral measurements predict cochlear nerve frequency tuning in an avian vocal communication specialist |
| title_full_unstemmed | Otoacoustic emissions but not behavioral measurements predict cochlear nerve frequency tuning in an avian vocal communication specialist |
| title_short | Otoacoustic emissions but not behavioral measurements predict cochlear nerve frequency tuning in an avian vocal communication specialist |
| title_sort | otoacoustic emissions but not behavioral measurements predict cochlear nerve frequency tuning in an avian vocal communication specialist |
| topic | budgerigar otoacoustic emission auditory-nerve frequency tuning cochlea |
| url | https://elifesciences.org/articles/102911 |
| work_keys_str_mv | AT dianamkarosas otoacousticemissionsbutnotbehavioralmeasurementspredictcochlearnervefrequencytuninginanavianvocalcommunicationspecialist AT lesliegonzales otoacousticemissionsbutnotbehavioralmeasurementspredictcochlearnervefrequencytuninginanavianvocalcommunicationspecialist AT yingxuanwang otoacousticemissionsbutnotbehavioralmeasurementspredictcochlearnervefrequencytuninginanavianvocalcommunicationspecialist AT christopherbergevin otoacousticemissionsbutnotbehavioralmeasurementspredictcochlearnervefrequencytuninginanavianvocalcommunicationspecialist AT laurelhcarney otoacousticemissionsbutnotbehavioralmeasurementspredictcochlearnervefrequencytuninginanavianvocalcommunicationspecialist AT kennethshenry otoacousticemissionsbutnotbehavioralmeasurementspredictcochlearnervefrequencytuninginanavianvocalcommunicationspecialist |