Adaptation of Binaural Processing in the Adult Brainstem Induced by Ambient Noise

Abstract

Interaural differences in stimulus intensity and timing are major cues for sound localization. In mammals, these cues are first processed in the lateral and medial superior olive by interaction of excitatory and inhibitory synaptic inputs from ipsi-and contralateral cochlear nucleus neurons. To preserve sound localization acuity following changes in the acoustic environment, the processing of these binaural cues needs neuronal adaptation. Recent studies have shown that binaural sensitivity adapts to stimulation history within milliseconds, but the actual extent of binaural adaptation is unknown. In the current study, we investigated long-term effects on binaural sensitivity using extracellular in vivo recordings from single neurons in the dorsal nucleus of the lateral lemniscus that inherit their binaural properties directly from the lateral and medial superior olives. In contrast to most previous studies, we used a noninvasive approach to influence this processing. Adult gerbils were exposed for 2 weeks to moderate noise with no stable binaural cue. We found monaural response properties to be unaffected by this measure. However, neuronal sensitivity to binaural cues was reversibly altered for a few days. Computational models of sensitivity to interaural time and level differences suggest that upregulation of inhibition in the superior olivary complex can explain the electrophysiological data.

Congenital and Prolonged Adult-Onset Deafness Cause Distinct Degradations in Neural ITD Coding with Bilateral Cochlear Implants

“…The reorganization in neural ITD maps in barn owls is greatly reduced if exposure to prisms occurs after about 200 days postnatal (Brainard and Knudsen 1998), although even in adult animals, map reorganization can be induced by allowing owls to hunt for prey while wearing the prisms (Bergan et al 2005). Exposing adult gerbils to omnidirectional noise appears to alter the distribution of best ITDs in DNLL (Siveke et al 2012), but the shifts are in the opposite direction (away from the midline) from those observed in both noise-exposed juvenile gerbils and our long-term adult-deafened cats, and there is no broadening of the best ITD distribution in adult gerbils. Unlike our deafening protocol, omnidirectional noise may not completely mask environmental ITD cues.…”

“…Importantly, the altered ITD tuning induced by abnormal sensory inputs is reversed after animals are returned to a normal environment (Brainard and Knudsen 1998;Siveke et al 2012), suggesting that appropriate experience with bilateral CIs might also restore normal ITD tuning in deaf animals.…”

“…Although the 6-month duration of deafness in these cats is shorter than the periods of deprivation typically experienced by CI users, this period is biologically significant in cats, which become sexually mature at~7 months of age (Scott 1970). The maintenance of a high number of ITD-sensitive neurons in long-term adult-deafened cats, along with the general reversibility of changes in coding of binaural cues induced by abnormal sensory experience regardless of age (Brainard and Knudsen 1998;Kacelnik et al 2006;Siveke et al 2012), suggests that the degradation in ITD coding resulting from long-term auditory deprivation in adults may be reversible by appropriate binaural stimulation.…”

Cortical and Subcortical Substrates of Cranial Nerve Function

“…These cues are first processed in the lateral and medial superior olive by interaction of excitatory and inhibitory synaptic inputs from ipsi-and contralateral cochlear nucleus neurons. 144 The superior olivary complex is therefore involved in binaural processing and is sensitive to differences in the timing of sounds at the 2 ears. The superior olivary complex is also involved in an initial assessment of the intensity differences of the sounds being received from the 2 sides.…”

Some observations about cochlear implants: challenges and future directions

“…However, many bilateral CI patients often receive their second CI sequentially often after long time intervals between surgeries. This is not an optimal strategy because there is substantial evidence documenting a narrow sensitive period for the development of binaural hearing [115][116][117][118][119][120][121], although the binaural system shows some degree of plasticity into adulthood and sensitivity to these cues may improve with experience [122][123][124]. A common misconception in the media is that "if one CI is good, then two must be better. "…”