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

Abstract

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 Statement

Binaural 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.