Altered neural encoding of vowels in noise does not affect behavioral vowel discrimination in gerbils with age-related hearing loss
IntroductionUnderstanding speech in a noisy environment, as opposed to speech in quiet, becomes increasingly more difficult with increasing age. Using the quiet-aged gerbil, we studied the effects of aging on speech-in-noise processing. Specifically, behavioral vowel discrimination and the encoding...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2023-11-01
|
| Series: | Frontiers in Neuroscience |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fnins.2023.1238941/full |
| _version_ | 1827762667783192576 |
|---|---|
| author | Amarins N. Heeringa Carolin Jüchter Rainer Beutelmann Georg M. Klump Christine Köppl |
| author_facet | Amarins N. Heeringa Carolin Jüchter Rainer Beutelmann Georg M. Klump Christine Köppl |
| author_sort | Amarins N. Heeringa |
| collection | DOAJ |
| description | IntroductionUnderstanding speech in a noisy environment, as opposed to speech in quiet, becomes increasingly more difficult with increasing age. Using the quiet-aged gerbil, we studied the effects of aging on speech-in-noise processing. Specifically, behavioral vowel discrimination and the encoding of these vowels by single auditory-nerve fibers were compared, to elucidate some of the underlying mechanisms of age-related speech-in-noise perception deficits.MethodsYoung-adult and quiet-aged Mongolian gerbils, of either sex, were trained to discriminate a deviant naturally-spoken vowel in a sequence of vowel standards against a speech-like background noise. In addition, we recorded responses from single auditory-nerve fibers of young-adult and quiet-aged gerbils while presenting the same speech stimuli.ResultsBehavioral vowel discrimination was not significantly affected by aging. For both young-adult and quiet-aged gerbils, the behavioral discrimination between /eː/ and /iː/ was more difficult to make than /eː/ vs. /aː/ or /iː/ vs. /aː/, as evidenced by longer response times and lower d’ values. In young-adults, spike timing-based vowel discrimination agreed with the behavioral vowel discrimination, while in quiet-aged gerbils it did not. Paradoxically, discrimination between vowels based on temporal responses was enhanced in aged gerbils for all vowel comparisons. Representation schemes, based on the spectrum of the inter-spike interval histogram, revealed stronger encoding of both the fundamental and the lower formant frequencies in fibers of quiet-aged gerbils, but no qualitative changes in vowel encoding. Elevated thresholds in combination with a fixed stimulus level, i.e., lower sensation levels of the stimuli for old individuals, can explain the enhanced temporal coding of the vowels in noise.DiscussionThese results suggest that the altered auditory-nerve discrimination metrics in old gerbils may mask age-related deterioration in the central (auditory) system to the extent that behavioral vowel discrimination matches that of the young adults. |
| first_indexed | 2024-03-11T10:33:50Z |
| format | Article |
| id | doaj.art-b2b3ed2e14174b16aeef369364552f62 |
| institution | Directory Open Access Journal |
| issn | 1662-453X |
| language | English |
| last_indexed | 2024-03-11T10:33:50Z |
| publishDate | 2023-11-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neuroscience |
| spelling | doaj.art-b2b3ed2e14174b16aeef369364552f622023-11-14T11:44:39ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2023-11-011710.3389/fnins.2023.12389411238941Altered neural encoding of vowels in noise does not affect behavioral vowel discrimination in gerbils with age-related hearing lossAmarins N. HeeringaCarolin JüchterRainer BeutelmannGeorg M. KlumpChristine KöpplIntroductionUnderstanding speech in a noisy environment, as opposed to speech in quiet, becomes increasingly more difficult with increasing age. Using the quiet-aged gerbil, we studied the effects of aging on speech-in-noise processing. Specifically, behavioral vowel discrimination and the encoding of these vowels by single auditory-nerve fibers were compared, to elucidate some of the underlying mechanisms of age-related speech-in-noise perception deficits.MethodsYoung-adult and quiet-aged Mongolian gerbils, of either sex, were trained to discriminate a deviant naturally-spoken vowel in a sequence of vowel standards against a speech-like background noise. In addition, we recorded responses from single auditory-nerve fibers of young-adult and quiet-aged gerbils while presenting the same speech stimuli.ResultsBehavioral vowel discrimination was not significantly affected by aging. For both young-adult and quiet-aged gerbils, the behavioral discrimination between /eː/ and /iː/ was more difficult to make than /eː/ vs. /aː/ or /iː/ vs. /aː/, as evidenced by longer response times and lower d’ values. In young-adults, spike timing-based vowel discrimination agreed with the behavioral vowel discrimination, while in quiet-aged gerbils it did not. Paradoxically, discrimination between vowels based on temporal responses was enhanced in aged gerbils for all vowel comparisons. Representation schemes, based on the spectrum of the inter-spike interval histogram, revealed stronger encoding of both the fundamental and the lower formant frequencies in fibers of quiet-aged gerbils, but no qualitative changes in vowel encoding. Elevated thresholds in combination with a fixed stimulus level, i.e., lower sensation levels of the stimuli for old individuals, can explain the enhanced temporal coding of the vowels in noise.DiscussionThese results suggest that the altered auditory-nerve discrimination metrics in old gerbils may mask age-related deterioration in the central (auditory) system to the extent that behavioral vowel discrimination matches that of the young adults.https://www.frontiersin.org/articles/10.3389/fnins.2023.1238941/fullpresbycusisconsonant-vowel-consonant logatomesMongolian gerbilspeech-in-noise perceptiontemporal coding |
| spellingShingle | Amarins N. Heeringa Carolin Jüchter Rainer Beutelmann Georg M. Klump Christine Köppl Altered neural encoding of vowels in noise does not affect behavioral vowel discrimination in gerbils with age-related hearing loss Frontiers in Neuroscience presbycusis consonant-vowel-consonant logatomes Mongolian gerbil speech-in-noise perception temporal coding |
| title | Altered neural encoding of vowels in noise does not affect behavioral vowel discrimination in gerbils with age-related hearing loss |
| title_full | Altered neural encoding of vowels in noise does not affect behavioral vowel discrimination in gerbils with age-related hearing loss |
| title_fullStr | Altered neural encoding of vowels in noise does not affect behavioral vowel discrimination in gerbils with age-related hearing loss |
| title_full_unstemmed | Altered neural encoding of vowels in noise does not affect behavioral vowel discrimination in gerbils with age-related hearing loss |
| title_short | Altered neural encoding of vowels in noise does not affect behavioral vowel discrimination in gerbils with age-related hearing loss |
| title_sort | altered neural encoding of vowels in noise does not affect behavioral vowel discrimination in gerbils with age related hearing loss |
| topic | presbycusis consonant-vowel-consonant logatomes Mongolian gerbil speech-in-noise perception temporal coding |
| url | https://www.frontiersin.org/articles/10.3389/fnins.2023.1238941/full |
| work_keys_str_mv | AT amarinsnheeringa alteredneuralencodingofvowelsinnoisedoesnotaffectbehavioralvoweldiscriminationingerbilswithagerelatedhearingloss AT carolinjuchter alteredneuralencodingofvowelsinnoisedoesnotaffectbehavioralvoweldiscriminationingerbilswithagerelatedhearingloss AT rainerbeutelmann alteredneuralencodingofvowelsinnoisedoesnotaffectbehavioralvoweldiscriminationingerbilswithagerelatedhearingloss AT georgmklump alteredneuralencodingofvowelsinnoisedoesnotaffectbehavioralvoweldiscriminationingerbilswithagerelatedhearingloss AT christinekoppl alteredneuralencodingofvowelsinnoisedoesnotaffectbehavioralvoweldiscriminationingerbilswithagerelatedhearingloss |