Cochlear efferent feedback balances interaural sensitivity

Abstract

Neurons in the lateral superior olive (LSO) compute sound location based on differences in interaural intensity, coded in ascending signals from the two cochleas. Unilateral destruction of the neuronal feedback from the LSO to the cochlea, the lateral olivocochlear efferents, disrupted the normal interaural correlation in response amplitudes to sounds of equal intensity. Thus, lateral olivocochlear feedback maintains the binaural balance in neural excitability required for accurate localization of sounds in space.

Figure 1

Assessment and interpretation of brainstem lesions. Schematics illustrate the central origins (a) and peripheral projections (b) of the medial and lateral components of the olivocochlear (OC) efferent system. Micrographs of an acetylcholinesterase-stained brainstem section ipsilateral (d) and contralateral (c) to a neurotoxin injection show the successful targeting of the LSO in one case and the corresponding selective loss of cholinergic immunostaining in the inner hair cell (IHC) area ipsilateral to the injection (e versus f). A schematic (g) illustrates the binaural circuitry driving the principal cells of the LSO: auditory nerve fibers (1) project to cochlear nucleus bushy cells (2), which send excitatory projections to the ipsilateral LSO (4) and inhibitory projections to the contralateral LSO via an interneuron (3) in the MNTB. Similar inputs to the nearby LOC somata (5) are hypothesized to account for the results in the present study. All procedures were approved by the Institutional Animal Care and Use Committee of the Massachusetts Eye and Ear Infirmary.

Figure 2

Unilateral cochlear de-efferentation disrupts interaural balance in neural excitability. Selective destruction of the LOC efferent system enhances mean cochlear neural response amplitudes (ABR) ipsilaterally and reduces them contralaterally (a) without affecting hair-cell based DPOAEs (b)or mean cochlear thresholds, as seen by either ABR (c) or DPOAE (d) measures. Comparing neural amplitudes between the two ears reveals that the normal binaural balance of excitability seen with an intact LOC (e) is disrupted when the LOC is destroyed (f). a–d show mean data (±s.e.m.) for different groups: symbol key in a applies to these 4 panels. Data in a and b are for stimuli at 22.6 kHz. e,f show data from individual cases (gray) and mean data for each group (black); each point is the mean interaural difference in ABR amplitude (expressed as the percent by which ipsilateral amplitudes exceed contralateral amplitudes) averaged, for one frequency, over the highest four levels presented (50–80 dB SPL). All ABR amplitudes reflect the peak-to-peak value of Wave 1, the summed activity of auditory nerve fibers.