Neural Adaptation at Stimulus Onset and Speed of Neural Processing as Critical Contributors to Speech Comprehension Independent of Hearing Threshold or Age

Author:

Schirmer Jakob1,Wolpert Stephan1,Dapper Konrad12,Rühle Moritz1,Wertz Jakob1,Wouters Marjoleen3ORCID,Eldh Therese1,Bader Katharina1ORCID,Singer Wibke1,Gaudrain Etienne45ORCID,Başkent Deniz5ORCID,Verhulst Sarah3,Braun Christoph67,Rüttiger Lukas1,Munk Matthias H. J.28ORCID,Dalhoff Ernst1,Knipper Marlies1

Affiliation:

1. Department of Otolaryngology, Head and Neck Surgery, University of Tübingen, Elfriede-Aulhorn-Str. 5, 72076 Tübingen, Germany

2. Department of Biology, Technical University Darmstadt, 64287 Darmstadt, Germany

3. Department of Information Technology, Ghent University, Technologiepark 126, 9052 Zwijnaarde, Belgium

4. Lyon Neuroscience Research Center, Centre National de la Recherche Scientifique UMR5292, Inserm U1028, Université Lyon 1, Centre Hospitalier Le Vinatier-Bâtiment 462–Neurocampus, 95 Boulevard Pinel, 69675 Bron CEDEX, France

5. Department of Otorhinolaryngology, University Medical Center Groningen (UMCG), Hanzeplein 1, BB21, 9700 RB Groningen, The Netherlands

6. Magnetoencephalography-Centre and Hertie Institute for Clinical Brain Research, University of Tübingen, Otfried-Müller-Straße 27, 72076 Tübingen, Germany

7. Center for Mind and Brain Research, University of Trento, Palazzo Fedrigotti-corso Bettini 31, 38068 Rovereto, Italy

8. Department of Psychiatry & Psychotherapy, University of Tübingen, Calwerstraße 14, 72076 Tübingen, Germany

Abstract

Background: It is assumed that speech comprehension deficits in background noise are caused by age-related or acquired hearing loss. Methods: We examined young, middle-aged, and older individuals with and without hearing threshold loss using pure-tone (PT) audiometry, short-pulsed distortion-product otoacoustic emissions (pDPOAEs), auditory brainstem responses (ABRs), auditory steady-state responses (ASSRs), speech comprehension (OLSA), and syllable discrimination in quiet and noise. Results: A noticeable decline of hearing sensitivity in extended high-frequency regions and its influence on low-frequency-induced ABRs was striking. When testing for differences in OLSA thresholds normalized for PT thresholds (PTTs), marked differences in speech comprehension ability exist not only in noise, but also in quiet, and they exist throughout the whole age range investigated. Listeners with poor speech comprehension in quiet exhibited a relatively lower pDPOAE and, thus, cochlear amplifier performance independent of PTT, smaller and delayed ABRs, and lower performance in vowel-phoneme discrimination below phase-locking limits (/o/-/u/). When OLSA was tested in noise, listeners with poor speech comprehension independent of PTT had larger pDPOAEs and, thus, cochlear amplifier performance, larger ASSR amplitudes, and higher uncomfortable loudness levels, all linked with lower performance of vowel-phoneme discrimination above the phase-locking limit (/i/-/y/). Conslusions: This study indicates that listening in noise in humans has a sizable disadvantage in envelope coding when basilar-membrane compression is compromised. Clearly, and in contrast to previous assumptions, both good and poor speech comprehension can exist independently of differences in PTTs and age, a phenomenon that urgently requires improved techniques to diagnose sound processing at stimulus onset in the clinical routine.

Funder

Deutsche Forschungsgemeinschaft DFG

DFG

Publisher

MDPI AG

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