Is cochlear synapse loss an origin of low-frequency hearing loss associated with endolymphatic hydrops?

Valenzuela, Carla V.; Lee, Choongheon; Mispagel, Abby; Bhattacharyya, Atri; Lefler, Shannon M.; Payne, Shelby; Goodman, Shawn S.; Ortmann, Amanda; Buchman, Craig A.; Rutherford, Mark A.; Lichtenhan, Jeffery T.

doi:10.1016/j.heares.2020.108099

Cited by 15 publications

(17 citation statements)

References 35 publications

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“…OAEs provide noninvasive, frequency-specific objective measures of cochlear mechanical sensitivity 11 , 12 . These hearing-threshold and OAE results are similar to those we reported previously from other guinea pigs with endolymphatic hydrops 8 , 9 . It is interesting that similar OAE results were obtained from a patient with Ménière’s disease 12 .…”

Section: Resultssupporting

confidence: 91%

“…We created an animal model of endolymphatic hydrops by ablating the endolymphatic sac 7 . At 30 days after the operation, operated ears had normal hearing thresholds at high frequencies and a hearing loss at low frequencies 8 , 9 , a pattern found in early-stage Ménière’s disease 3 . By using a cochlear perfusion technique that enables assessment of tonotopicity 10 , 11 , we show, for the first time, abnormal cochlear frequency-place maps in ears that developed normally but have been changed by a disease process (endolymphatic hydrops).…”

Section: Introductionmentioning

confidence: 89%

“…Animal preparation methods on have been detailed in our previous publications 7 – 9 , 29 , and here we provide essential information. Guinea pigs were sedated with intraperitoneal injection of 100 mg/kg Inactin hydrate (i.e., thiobutabarbital sodium).…”

Section: Methodsmentioning

confidence: 99%

“…Method details for neural measurements have been described 8 , 9 , 11 . Briefly, neural measurements (e.g.…”

Section: Methodsmentioning

confidence: 99%

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Altered mapping of sound frequency to cochlear place in ears with endolymphatic hydrops provide insight into the pitch anomaly of diplacusis

Guinan

Lefler

Buchman

et al. 2021

Sci Rep

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A fundamental property of mammalian hearing is the conversion of sound pressure into a frequency-specific place of maximum vibration along the cochlear length, thereby creating a tonotopic map. The tonotopic map makes possible systematic frequency tuning across auditory-nerve fibers, which enables the brain to use pitch to separate sounds from different environmental sources and process the speech and music that connects us to people and the world. Sometimes a tone has a different pitch in the left and right ears, a perceptual anomaly known as diplacusis. Diplacusis has been attributed to a change in the cochlear frequency-place map, but the hypothesized abnormal cochlear map has never been demonstrated. Here we assess cochlear frequency-place maps in guinea-pig ears with experimentally-induced endolymphatic hydrops, a hallmark of Ménière’s disease. Our findings are consistent with the hypothesis that diplacusis is due to an altered cochlear map. Map changes can lead to altered pitch, but the size of the pitch change is also affected by neural synchrony. Our data show that the cochlear frequency-place map is not fixed but can be altered by endolymphatic hydrops. Map changes should be considered in assessing hearing pathologies and treatments.

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Section: Resultssupporting

confidence: 91%

Section: Introductionmentioning

confidence: 89%

Section: Methodsmentioning

confidence: 99%

“…Method details for neural measurements have been described 8 , 9 , 11 . Briefly, neural measurements (e.g.…”

Section: Methodsmentioning

confidence: 99%

See 2 more Smart Citations

Altered mapping of sound frequency to cochlear place in ears with endolymphatic hydrops provide insight into the pitch anomaly of diplacusis

Guinan

Lefler

Buchman

et al. 2021

Sci Rep

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“…Here we show recruitment in auditory-nerve measurements from two guinea pig models: (1) guinea-pig ears that underwent surgery to ablate the endolymphatic sac, a procedure that induces endolymphatic hydrops that can be seen histologically at 30 postoperative days and that causes low-frequency hearing threshold elevation soon after the ablation (12)(13)(14), and (2) naïve (i.e., never operated on) animals that underwent cochlear perfusions of 13 mM 2-Hydroxypropyl-Beta-Cyclodextrin (HPBCD) in artificial perilymph. HPBCD can be used to treat Niemann-Pick type C disease, Alzheimer's disease, and atherosclerosis, but causes hearing loss [(15) p. 1,017].…”

Section: Introductionmentioning

confidence: 99%

Measurements From Ears With Endolymphatic Hydrops and 2-Hydroxypropyl-Beta-Cyclodextrin Provide Evidence That Loudness Recruitment Can Have a Cochlear Origin

et al. 2021

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Background: Loudness recruitment is commonly experienced by patients with putative endolymphatic hydrops. Loudness recruitment is abnormal loudness growth with high-level sounds being perceived as having normal loudness even though hearing thresholds are elevated. The traditional interpretation of recruitment is that cochlear amplification has been reduced. Since the cochlear amplifier acts primarily at low sound levels, an ear with elevated thresholds from reduced cochlear amplification can have normal processing at high sound levels. In humans, recruitment can be studied using perceptual loudness but in animals physiological measurements are used. Recruitment in animal auditory-nerve responses has never been unequivocally demonstrated because the animals used had damage to sensory and neural cells, not solely a reduction of cochlear amplification. Investigators have thus looked for, and found, evidence of recruitment in the auditory central nervous system (CNS). While studies on CNS recruitment are informative, they cannot rule out the traditional interpretation of recruitment originating in the cochlea.Design: We used techniques that could assess hearing function throughout entire frequency- and dynamic-range of hearing. Measurements were made from two animal models: guinea-pig ears with endolymphatic-sac-ablation surgery to produce endolymphatic hydrops, and naïve guinea-pig ears with cochlear perfusions of 13 mM 2-Hydroxypropyl-Beta-Cyclodextrin (HPBCD) in artificial perilymph. Endolymphatic sac ablation caused low-frequency loss. Animals treated with HPBCD had hearing loss at all frequencies. None of these animals had loss of hair cells or synapses on auditory nerve fibers.Results: In ears with endolymphatic hydrops and those perfused with HPBCD, auditory-nerve based measurements at low frequencies showed recruitment compared to controls. Recruitment was not found at high frequencies (> 4 kHz) where hearing thresholds were normal in ears with endolymphatic hydrops and elevated in ears treated with HPBCD.Conclusions: We found compelling evidence of recruitment in auditory-nerve data. Such clear evidence has never been shown before. Our findings suggest that, in patients suspected of having endolymphatic hydrops, loudness recruitment may be a good indication that the associated low-frequency hearing loss originates from a reduction of cochlear amplification, and that measurements of recruitment could be used in differential diagnosis and treatment monitoring of Ménière's disease.

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The Origin Along the Cochlea of Otoacoustic Emissions Evoked by Mid-Frequency Tone Pips

Goodman,

Lefler,

Lee

et al. 2024

JARO

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Is cochlear synapse loss an origin of low-frequency hearing loss associated with endolymphatic hydrops?

Cited by 15 publications

References 35 publications

Altered mapping of sound frequency to cochlear place in ears with endolymphatic hydrops provide insight into the pitch anomaly of diplacusis

Altered mapping of sound frequency to cochlear place in ears with endolymphatic hydrops provide insight into the pitch anomaly of diplacusis

Measurements From Ears With Endolymphatic Hydrops and 2-Hydroxypropyl-Beta-Cyclodextrin Provide Evidence That Loudness Recruitment Can Have a Cochlear Origin

The Origin Along the Cochlea of Otoacoustic Emissions Evoked by Mid-Frequency Tone Pips

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