Microsecond interaural time difference discrimination restored by cochlear implants after neonatal deafness

Roßkothen-Kuhl, Nicole; Buck, Alexa N; Li, Kongyan; Schnupp, Jan W. H.

doi:10.7554/elife.59300

Cited by 27 publications

(36 citation statements)

References 94 publications

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“…Previous studies on bilateral CI users with prelingual or early onset deafness suggest an important role of early auditory input in the establishment of ITD sensitivity ( Litovsky et al, 2010 , 2012 ; Salloum et al, 2010 ). Patients with early auditory deprivation showed no measurable sensitivity to ITDs on the lateralization task, whereas recent studies in rats have shown a comparable behavioral ITD sensitivity between animals with NH and those who were ND and received bilateral CIs ( K. Li et al, 2019 ; Rosskothen-Kuhl et al, 2021 ). It should be noted that Rosskothen-Kuhl and colleagues, fully inserted the animal electrode array into the middle turn through a cochleostomy and not into the basal turn via the round window, as performed in human studies.…”

Section: Discussionmentioning

confidence: 81%

Neonatal Deafening Selectively Degrades the Sensitivity to Interaural Time Differences of Electrical Stimuli in Low-Frequency Pathways in Rats

Sunwoo

2023

eNeuro

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We examined the effect of neonatal deafening on frequency-specific pathways for processing of interaural time differences (ITDs) in cochlear-implant stimuli. Animal studies have demonstrated differences in neural ITD sensitivity in the inferior colliculus (IC) depending on the intracochlear location of intra-cochlear stimulating electrodes. We used neonatally deafened (ND) rats of both sexes and recorded the responses of single neurons in the IC to electrical stimuli with ITDs delivered to the apical or basal cochlea and compared them with acutely deafened (AD) rats of both sexes with normal hearing during development. We found that neonatal deafness significantly impacted the ITD sensitivity and the ITD tuning patterns restricted to apically driven IC neurons. In ND rats, the ITD sensitivity of apically driven neurons is reduced to values similar to basally driven neurons. The prevalence of ITD-sensitive apical neurons with a peak-shaped ITD tuning curve, which may reflect predominant input from the medial superior olivary complex, in ND rats was diminished compared with that in AD rats (67%, AD vs. 40%, ND). Conversely, monotonic-type responses rarely occurred in AD rats (14%) but were approximately equally as prevalent as peak-type tuning curves in ND rats (42%). Nevertheless, in ND rats, the ITD at the maximum slope of the ITD tuning curve was still more concentrated within the physiological ITD range in apically driven than in basally driven neurons. These results indicate that the development of high ITD sensitivity processed by low-frequency pathways depends on normal auditory experience and associated biases in ITD tuning strategies.Significance StatementBinaural neurons in the inferior colliculus (IC) are sensitive to interaural time differences (ITDs) with a high resolution when electrical pulse trains are presented through a low-frequency pathway compared to a high-frequency pathway. However, despite the potential importance of intracochlear stimulating sites in improving ITD sensitivity, it is unclear whether these functionally segregated pathways can be preserved following early auditory deprivation. Here, we show that site-specific ITD circuitry from the cochlea to the IC can be partly developed without auditory experience in neonatally deafened animals. This finding may support the importance of selective electrical stimulation of the apical region of the cochlea for achieving improved sensitivity to ITDs in bilateral cochlear implant users, even after early auditory deprivation.

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Section: Discussionmentioning

confidence: 81%

Neonatal Deafening Selectively Degrades the Sensitivity to Interaural Time Differences of Electrical Stimuli in Low-Frequency Pathways in Rats

Sunwoo

2023

eNeuro

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“…Another notable conclusion of the model's prediction about improved resolution at small ITDs is that it potentially provides a mechanistic explanation for the recent reports of highly precise ITD sensitivity both on the level of midbrain coding (Buck et al, 2021) and perceptual resolution (Rosskothen-Kuhl et al, 2021) in bilaterally implanted rats. Since these animals have smaller inter-ear-distances compared to human subjects, the predicted region of increased LSO ITD coding capacity would 10.3389/fnins.2022.1021541 cover a large fraction of the available ITDs in rats, and hence provide an advantageous effect on spatial resolution for almost the entire frontal field.…”

Section: Discussionmentioning

confidence: 90%

Temporal hyper-precision of brainstem neurons alters spatial sensitivity of binaural auditory processing with cochlear implants

Müller

Dietz

et al. 2023

Front. Neurosci.

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The ability to localize a sound source in complex environments is essential for communication and navigation. Spatial hearing relies predominantly on the comparison of differences in the arrival time of sound between the two ears, the interaural time differences (ITDs). Hearing impairments are highly detrimental to sound localization. While cochlear implants (CIs) have been successful in restoring many crucial hearing capabilities, sound localization via ITD detection with bilateral CIs remains poor. The underlying reasons are not well understood. Neuronally, ITD sensitivity is generated by coincidence detection between excitatory and inhibitory inputs from the two ears performed by specialized brainstem neurons. Due to the lack of electrophysiological brainstem recordings during CI stimulation, it is unclear to what extent the apparent deficits are caused by the binaural comparator neurons or arise already on the input level. Here, we use a bottom-up approach to compare response features between electric and acoustic stimulation in an animal model of CI hearing. Conducting extracellular single neuron recordings in gerbils, we find severe hyper-precision and moderate hyper-entrainment of both the excitatory and inhibitory brainstem inputs to the binaural comparator neurons during electrical pulse-train stimulation. This finding establishes conclusively that the binaural processing stage must cope with highly altered input statistics during CI stimulation. To estimate the consequences of these effects on ITD sensitivity, we used a computational model of the auditory brainstem. After tuning the model parameters to match its response properties to our physiological data during either stimulation type, the model predicted that ITD sensitivity to electrical pulses is maintained even for the hyper-precise inputs. However, the model exhibits severely altered spatial sensitivity during electrical stimulation compared to acoustic: while resolution of ITDs near midline was increased, more lateralized adjacent source locations became inseparable. These results directly resemble recent findings in rodent and human CI listeners. Notably, decreasing the phase-locking precision of inputs during electrical stimulation recovered a wider range of separable ITDs. Together, our findings suggest that a central problem underlying the diminished ITD sensitivity in CI users might be the temporal hyper-precision of inputs to the binaural comparator stage induced by electrical stimulation.

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“…In contrast, three studies in rats have shown a similar sensitivity in tuning between animals with NH and those who were early-deafened and received CI stimulation [ 95 – 97 ]. Supportive of their assertion that tuning was similar, many neurons recorded from the inferior colliculus in these rats were significantly tuned to ITDs, in contrast to previous studies with rabbits [ 88 ].…”

Section: Discussionmentioning

confidence: 99%

“…Recent experiments in rabbits support the idea that consistent BiCI stimulation can restore ITD sensitivity [ 98 ]. It should be noted that because few animals participated in the study by Rosskothen-Kuhl and colleagues, the lack of effect (i.e., no significant difference in ITD tuning between NH and late-implanted groups) in one study could have been driven by the variability in rats with NH [ 95 ].…”

Section: Discussionmentioning

confidence: 99%

Sound source localization patterns and bilateral cochlear implants: Age at onset of deafness effects

et al. 2022

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The ability to determine a sound’s location is critical in everyday life. However, sound source localization is severely compromised for patients with hearing loss who receive bilateral cochlear implants (BiCIs). Several patient factors relate to poorer performance in listeners with BiCIs, associated with auditory deprivation, experience, and age. Critically, characteristic errors are made by patients with BiCIs (e.g., medial responses at lateral target locations), and the relationship between patient factors and the type of errors made by patients has seldom been investigated across individuals. In the present study, several different types of analysis were used to understand localization errors and their relationship with patient-dependent factors (selected based on their robustness of prediction). Binaural hearing experience is required for developing accurate localization skills, auditory deprivation is associated with degradation of the auditory periphery, and aging leads to poorer temporal resolution. Therefore, it was hypothesized that earlier onsets of deafness would be associated with poorer localization acuity and longer periods without BiCI stimulation or older age would lead to greater amounts of variability in localization responses. A novel machine learning approach was introduced to characterize the types of errors made by listeners with BiCIs, making them simple to interpret and generalizable to everyday experience. Sound localization performance was measured in 48 listeners with BiCIs using pink noise trains presented in free-field. Our results suggest that older age at testing and earlier onset of deafness are associated with greater average error, particularly for sound sources near the center of the head, consistent with previous research. The machine learning analysis revealed that variability of localization responses tended to be greater for individuals with earlier compared to later onsets of deafness. These results suggest that early bilateral hearing is essential for best sound source localization outcomes in listeners with BiCIs.

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Microsecond interaural time difference discrimination restored by cochlear implants after neonatal deafness

Cited by 27 publications

References 94 publications

Neonatal Deafening Selectively Degrades the Sensitivity to Interaural Time Differences of Electrical Stimuli in Low-Frequency Pathways in Rats

Neonatal Deafening Selectively Degrades the Sensitivity to Interaural Time Differences of Electrical Stimuli in Low-Frequency Pathways in Rats

Temporal hyper-precision of brainstem neurons alters spatial sensitivity of binaural auditory processing with cochlear implants

Sound source localization patterns and bilateral cochlear implants: Age at onset of deafness effects

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