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Assessing temporal responsiveness of primary stimulated neurons in auditory brainstem and cochlear implant users

Azadpour, Mahan; Shapiro, William H; Roland, J Thomas; Svirsky, Mario A
The reasons why clinical outcomes with auditory brainstem implants (ABIs) are generally poorer than with cochlear implants (CIs) are still somewhat elusive. Prior work has focused on differences in processing of spectral information due to possibly poorer tonotopic representation and higher channel interaction with ABIs than with CIs. In contrast, this study examines the hypothesis that a potential contributing reason for poor speech perception in ABI users may be the relative lack of temporal responsiveness of the primary neurons that are stimulated by the ABI. The cochlear nucleus, the site of ABI stimulation, consists of different neuron types, most of which have much more complex responses than the auditory nerve neurons stimulated by a CI. Temporal responsiveness of primary stimulated neurons was assessed in a group of ABI and CI users by measuring recovery of electrically evoked compound action potentials (ECAPs) from single-pulse forward masking. Slower ECAP recovery tended to be associated with poorer hearing outcomes in both groups. ABI subjects with the longest recovery time had no speech understanding or even no hearing sensation with their ABI device; speech perception for the one CI outlier with long ECAP recovery time was well below average. To the extent that ECAP recovery measures reveal temporal properties of the primary neurons that receive direct stimulation form neural prosthesis devices, they may provide a physiological underpinning for clinical outcomes of auditory implants. ECAP recovery measures may be used to determine which portions of the cochlear nucleus to stimulate, and possibly allow us to enhance the stimulation paradigms.
PMID: 33434815
ISSN: 1878-5891
CID: 4746742

Individual Differences in Mothers' Spontaneous Infant-Directed Speech Predict Language Attainment in Children With Cochlear Implants

Dilley, Laura; Lehet, Matthew; Wieland, Elizabeth A; Arjmandi, Meisam K; Kondaurova, Maria; Wang, Yuanyuan; Reed, Jessa; Svirsky, Mario; Houston, Derek; Bergeson, Tonya
Purpose Differences across language environments of prelingually deaf children who receive cochlear implants (CIs) may affect language acquisition; yet, whether mothers show individual differences in how they modify infant-directed (ID) compared with adult-directed (AD) speech has seldom been studied. This study assessed individual differences in how mothers realized speech modifications in ID register and whether these predicted differences in language outcomes for children with CIs. Method Participants were 36 dyads of mothers and their children aged 0;8-2;5 (years;months) at the time of CI implantation. Mothers' spontaneous speech was recorded in a lab setting in ID or AD conditions before ~15 months postimplantation. Mothers' speech samples were characterized for acoustic-phonetic and lexical properties established as canonical indices of ID speech to typically hearing infants, such as vowel space area differences, fundamental frequency variability, and speech rate. Children with CIs completed longitudinal administrations of one or more standardized language assessment instruments at variable intervals from 6 months to 9.5 years postimplantation. Standardized scores on assessments administered longitudinally were used to calculate linear regressions, which gave rise to predicted language scores for children at 2 years postimplantation and language growth over 2-year intervals. Results Mothers showed individual differences in how they modified speech in ID versus AD registers. Crucially, these individual differences significantly predicted differences in estimated language outcomes at 2 years postimplantation in children with CIs. Maternal speech variation in lexical quantity and vowel space area differences across ID and AD registers most frequently predicted estimates of language attainment in children with CIs, whereas prosodic differences played a minor role. Conclusion Results support that caregiver language behaviors play a substantial role in explaining variability in language attainment in children receiving CIs. Supplemental Material https://doi.org/10.23641/asha.12560147.
PMCID:7838839
PMID: 32603621
ISSN: 1558-9102
CID: 5043752

Speech Perception Changes in the Acoustically Aided, Nonimplanted Ear after Cochlear Implantation: A Multicenter Study

Svirsky, Mario A; Neuman, Arlene C; Neukam, Jonathan D; Lavender, Annette; Miller, Margaret K; Aaron, Ksenia A; Skarzynski, Piotr H; Cywka, Katarzyna B; Skarzynski, Henryk; Truy, Eric; Seldran, Fabien; Hermann, Ruben; Govaerts, Paul; De Ceulaer, Geert; Bergeron, Francois; Hotton, Matthieu; Moran, Michelle; Dowell, Richard C; Goffi-Gomez, Maria Valeria Schmidt; Magalhães, Ana Tereza de Matos; Santarelli, Rosamaria; Scimemi, Pietro
In recent years there has been an increasing percentage of cochlear implant (CI) users who have usable residual hearing in the contralateral, nonimplanted ear, typically aided by acoustic amplification. This raises the issue of the extent to which the signal presented through the cochlear implant may influence how listeners process information in the acoustically stimulated ear. This multicenter retrospective study examined pre- to postoperative changes in speech perception in the nonimplanted ear, the implanted ear, and both together. Results in the latter two conditions showed the expected increases, but speech perception in the nonimplanted ear showed a modest yet meaningful decrease that could not be completely explained by changes in unaided thresholds, hearing aid malfunction, or several other demographic variables. Decreases in speech perception in the nonimplanted ear were more likely in individuals who had better levels of speech perception in the implanted ear, and in those who had better speech perception in the implanted than in the nonimplanted ear. This raises the possibility that, in some cases, bimodal listeners may rely on the higher quality signal provided by the implant and may disregard or even neglect the input provided by the nonimplanted ear.
PMID: 32517138
ISSN: 2077-0383
CID: 4478212

Music Is More Enjoyable With Two Ears, Even If One of Them Receives a Degraded Signal Provided By a Cochlear Implant

Landsberger, David M; Vermeire, Katrien; Stupak, Natalia; Lavender, Annette; Neukam, Jonathan; Van de Heyning, Paul; Svirsky, Mario A
OBJECTIVES/OBJECTIVE:Cochlear implants (CIs) restore speech perception in quiet but they also eliminate or distort many acoustic cues that are important for music enjoyment. Unfortunately, quantifying music enjoyment by CI users has been difficult because comparisons must rely on their recollection of music before they lost their hearing. Here, we aimed to assess music enjoyment in CI users using a readily interpretable reference based on acoustic hearing. The comparison was done by testing "single-sided deafness" (SSD) patients who have normal hearing (NH) in one ear and a CI in the other ear. The study also aimed to assess binaural musical enjoyment, with the reference being the experience of hearing with a single NH ear. Three experiments assessed the effect of adding different kinds of input to the second ear: electrical, vocoded, or unmodified. DESIGN/METHODS:In experiment 1, music enjoyment in SSD-CI users was investigated using a modified version of the MUSHRA (MUltiple Stimuli with Hidden Reference and Anchor) method. Listeners rated their enjoyment of song segments on a scale of 0 to 200, where 100 represented the enjoyment obtained from a song segment presented to the NH ear, 0 represented a highly degraded version of the same song segment presented to the same ear, and 200 represented enjoyment subjectively rated as twice as good as the 100 reference. Stimuli consisted of acoustic only, electric only, acoustic and electric, as well as other conditions with low pass filtered acoustic stimuli. Acoustic stimulation was provided by headphone to the NH ear and electric stimulation was provided by direct audio input to the subject's speech processor. In experiment 2, the task was repeated using NH listeners who received vocoded stimuli instead of electric stimuli. Experiment 3 tested the effect of adding the same unmodified song segment to the second ear, also in NH listeners. RESULTS:Music presented through the CI only was very unpleasant, with an average rating of 20. Surprisingly, the combination of the unpleasant CI signal in one ear with acoustic stimulation in the other ear was rated more enjoyable (mean = 123) than acoustic processing alone. Presentation of the same monaural musical signal to both ears in NH listeners resulted with even greater enhancement of the experience compared with presentation to a single ear (mean = 159). Repeating the experiment using a vocoder to one ear of NH listeners resulted in interference rather than enhancement. CONCLUSIONS:Music enjoyment from electric stimulation is extremely poor relative to a readily interpretable NH baseline for CI-SSD listeners. However, the combination of this unenjoyable signal presented through a CI and an unmodified acoustic signal presented to a NH (or near-NH) contralateral ear results in enhanced music enjoyment with respect to the acoustic signal alone. Remarkably, this two-ear enhancement experienced by CI-SSD listeners represents a substantial fraction of the two-ear enhancement seen in NH listeners. This unexpected benefit of electroacoustic auditory stimulation will have to be considered in theoretical accounts of music enjoyment and may facilitate the quest to enhance music enjoyment in CI users.
PMID: 31469701
ISSN: 1538-4667
CID: 4054672

Editorial: Preregistration and Open Science Practices in Hearing Science and Audiology: The Time Has Come [Editorial]

Svirsky, Mario A
PMID: 31880675
ISSN: 1538-4667
CID: 4250882

Auditory cortical plasticity in cochlear implant users

Glennon, Erin; Svirsky, Mario A; Froemke, Robert C
Cochlear implants are one of the most successful neuroprosthetic devices that have been developed to date. Profoundly deaf patients can achieve speech perception after complete loss of sensory input. Despite the improvements many patients experience, there is still a large degree of outcome variability. It has been proposed that central plasticity may be a major factor in the different levels of benefit that patients experience. However, the neural mechanisms of how plasticity impacts cochlear implant learning and the degree of plasticity's influence remain unknown. Here, we review the human and animal research on three of the main ways that central plasticity affects cochlear implant outcomes.
PMID: 31864104
ISSN: 1873-6882
CID: 4250432

The Effect of Hearing Aid Bandwidth and Configuration of Hearing Loss on Bimodal Speech Recognition in Cochlear Implant Users

Neuman, Arlene C; Zeman, Annette; Neukam, Jonathan; Wang, Binhuan; Svirsky, Mario A
OBJECTIVES/OBJECTIVE:(1) To determine the effect of hearing aid (HA) bandwidth on bimodal speech perception in a group of unilateral cochlear implant (CI) patients with diverse degrees and configurations of hearing loss in the nonimplanted ear, (2) to determine whether there are demographic and audiometric characteristics that would help to determine the appropriate HA bandwidth for a bimodal patient. DESIGN/METHODS:Participants were 33 experienced bimodal device users with postlingual hearing loss. Twenty three of them had better speech perception with the CI than the HA (CI>HA group) and 10 had better speech perception with the HA than the CI (HA>CI group). Word recognition in sentences (AzBio sentences at +10 dB signal to noise ratio presented at 0° azimuth) and in isolation [CNC (consonant-nucleus-consonant) words] was measured in unimodal conditions [CI alone or HAWB, which indicates HA alone in the wideband (WB) condition] and in bimodal conditions (BMWB, BM2k, BM1k, and BM500) as the bandwidth of an actual HA was reduced from WB to 2 kHz, 1 kHz, and 500 Hz. Linear mixed-effect modeling was used to quantify the relationship between speech recognition and listening condition and to assess how audiometric or demographic covariates might influence this relationship in each group. RESULTS:For the CI>HA group, AzBio scores were significantly higher (on average) in all bimodal conditions than in the best unimodal condition (CI alone) and were highest at the BMWB condition. For CNC scores, on the other hand, there was no significant improvement over the CI-alone condition in any of the bimodal conditions. The opposite pattern was observed in the HA>CI group. CNC word scores were significantly higher in the BM2k and BMWB conditions than in the best unimodal condition (HAWB), but none of the bimodal conditions were significantly better than the best unimodal condition for AzBio sentences (and some of the restricted bandwidth conditions were actually worse). Demographic covariates did not interact significantly with bimodal outcomes, but some of the audiometric variables did. For CI>HA participants with a flatter audiometric configuration and better mid-frequency hearing, bimodal AzBio scores were significantly higher than the CI-alone score with the WB setting (BMWB) but not with other bandwidths. In contrast, CI>HA participants with more steeply sloping hearing loss and poorer mid-frequency thresholds (≥82.5 dB) had significantly higher bimodal AzBio scores in all bimodal conditions, and the BMWB did not differ significantly from the restricted bandwidth conditions. HA>CI participants with mild low-frequency hearing loss showed the highest levels of bimodal improvement over the best unimodal condition on CNC words. They were also less affected by HA bandwidth reduction compared with HA>CI participants with poorer low-frequency thresholds. CONCLUSIONS:The pattern of bimodal performance as a function of the HA bandwidth was found to be consistent with the degree and configuration of hearing loss for both patients with CI>HA performance and for those with HA>CI performance. Our results support fitting the HA for all bimodal patients with the widest bandwidth consistent with effective audibility.
PMID: 30067559
ISSN: 1538-4667
CID: 3217482

Locus coeruleus activation accelerates perceptual learning

Glennon, Erin; Carcea, Ioana; Martins, Ana Raquel O; Multani, Jasmin; Shehu, Ina; Svirsky, Mario A; Froemke, Robert C
Neural representations of the external world are constructed and updated in a manner that depends on behavioral context. For neocortical networks, this contextual information is relayed by a diverse range of neuromodulatory systems, which govern attention and signal the value of internal state variables such as arousal, motivation, and stress. Neuromodulators enable cortical circuits to differentially process specific stimuli and modify synaptic strengths in order to maintain short- or long-term memory traces of significant perceptual events and behavioral episodes. One of the most important subcortical neuromodulatory systems for attention and arousal is the noradrenergic locus coeruleus. Here we report that the noradrenergic system can enhance behavior in rats performing a self-initiated auditory recognition task, and optogenetic stimulation of noradrenergic locus coeruleus neurons accelerated the rate at which trained rats began correctly responding to a change in reward contingency. Animals successively progressed through distinct behavioral epochs, including periods of perseverance and exploration that occurred much more rapidly when animals received locus coeruleus stimulation. In parallel, we made recordings from primary auditory cortex and found that pairing tones with locus coeruleus stimulation led to a similar set of changes to cortical tuning profiles. Thus both behavioral and neural responses go through phases of adjustment for exploring and exploiting environmental reward contingencies. Furthermore, behavioral engagement does not necessarily recruit optimal locus coeruleus activity.
PMID: 29859972
ISSN: 1872-6240
CID: 3144272

Duration of unilateral auditory deprivation is associated with reduced speech perception after cochlear implantation: A single-sided deafness study

Cohen, Samuel M; Svirsky, Mario A
OBJECTIVE:Examine the relationship between duration of unilateral deafness and speech perception outcomes after cochlear implantation in adults with single-sided deafness. METHODS:A systematic review of PubMed articles containing individual speech perception and duration of deafness data from single-sided deaf adults. Studies were selected for detailed review and duration of deafness and speech perception outcomes were extracted, with speech scores reported as percent correct. A linear regression as a function of study and length of deafness was performed. RESULTS:A statistically significant negative effect of duration of unilateral deafness on speech perception was found, but there was substantial uncertainty regarding the strength of the effect. DISCUSSION/CONCLUSIONS:Existing data make it difficult to either support or reject a hard 5- or 10-year unilateral auditory deprivation limit on cochlear implant (CI) candidacy for patients with single-sided deafness. This is because the totality of available data are consistent with a very small effect, perhaps negligible in practical terms, and just as consistent with a very large effect. Regardless of effect size, the present results have important basic implications. They suggest that unilateral sound deprivation may have a deleterious effect on auditory processing even though more central parts of the auditory system have continued to receive input from a contralateral normal ear. CONCLUSIONS:Speech perception scores in SSD patients are negatively correlated with duration of deafness, but the limited amount of data from cochlear implant users with long-term single-sided deafness leads to substantial uncertainly, which in turn precludes any strong clinical recommendations. Further study of SSD CI users with long-term deafness will be necessary to generate evidence-based guidelines for implantation criteria in this population.
PMCID:6335158
PMID: 30486762
ISSN: 1754-7628
CID: 3594642

Comparison of Skull Radiograph and Computed Tomography Measurements of Cochlear Implant Insertion Angles

Gallant, Sara; Friedmann, David R; Hagiwara, Mari; Roland, J Thomas; Svirsky, Mario A; Jethanamest, Daniel
BACKGROUND:Measurement of the angular depth of insertion (aDOI) of cochlear implant electrode arrays has numerous clinical and research applications. Plain-film radiographs are easily obtained intraoperatively and have been described as a means to calculate aDOI. CT imaging with 3D reformatting can also be used for this measurement, but is less conveniently obtained and requires higher radiation doses, a particular concern in pediatrics. The extent to which plain-film and 3D CT image-based measurements are representative of the true position of the electrode within the cochlea is unknown. METHODS:Cochlear implantation was performed on 10 cadaveric temporal bones. Five bones were implanted with perimodiolar electrodes (Contour Advance TM, Cochlear, Sydney, Australia) and five were implanted with lateral wall electrodes (Slim Straight, Cochlear). The insertion depths of the electrodes were varied. Each bone was imaged with a radiograph and CT. aDOI was measured for each bone in each imaging modality by a neurotologist and a neuroradiologist. To obtain a 'gold standard' estimate of aDOI, the implanted temporal bones were embedded in an epoxy resin and methodically sectioned at 100 μm intervals; histologic images were captured at each interval. A 3D stack of the images was compounded, and a MATLAB script used to calculate aDOI of the most apical electrode. Measurements in the three modalities (radiograph, CT, and histology) were then compared. RESULTS:The average aDOI across all bones was similar for all modalities: 423° for radiographs, 425° for CT scans, and 427° for histology, indicating that neither imaging modality resulted in large systematic errors. Using the histology-measured angles as a reference, the average error for CT-based measures (regardless of whether the error was in the positive or negative direction) was 12°, and that for radiograph-based measures was 15°. This small difference (12 vs 15° error) was not statistically significant. CONCLUSION/CONCLUSIONS:Based on this cadaveric temporal bone model, both radiographs and CTs can provide reasonably accurate aDOI measurements. In this small sample, and as expected, the CT-based estimates were more accurate than the radiograph-based measurements. However, the difference was small and not statistically significant. Thus, the use of plain radiographs to calculate aDOI seems judicious whenever it is desired to prevent unnecessary radiation exposure and expense.
PMID: 30741910
ISSN: 1537-4505
CID: 3656032