Abstract
Spatial hearing allows animals to rapidly detect and localize auditory events in the surrounding environment. The auditory brainstem plays a central role in processing and extracting binaural spatial cues through microsecond-precise binaural integration, especially for detecting interaural time differences (ITDs) of low-frequency sounds at the medial superior olive (MSO). A series of mechanisms exist in the underlying neural circuits for preserving accurate action potential timing across multiple fibers, synapses and nuclei along this pathway. One of these is the myelination of afferent fibers that ensures reliable and temporally precise action potential propagation in the axon. There are several reports of fine-tuned myelination patterns in the MSO circuit, but how specifically myelination influences the precision of sound localization remains incompletely understood. Here we present a spiking neural network (SNN) model of the Mongolian gerbil auditory brainstem with myelinated axons to investigate whether different axon myelination thicknesses alter the sound localization process. Our model demonstrates that axon myelin thickness along the contralateral pathways can substantially modulate ITD detection. Furthermore, optimal ITD sensitivity is reached when the MSO receives contralateral inhibition via thicker myelinated axons compared to contralateral excitation, a result that is consistent with previously reported experimental observations. Our results suggest specific roles of axon myelination for extracting temporal dynamics in ITD decoding, especially in the pathway of the contralateral inhibition.
Highlights
In the mammalian brain, the precise temporal information encoded in action potentials and trains of action potentials is one major mechanism contributing to accurate neural integration and information processing
High-frequency sounds are localized in the LSO by calculating the interaural level difference (ILD; Boudreau and Tsuchitani, 1968), while low-frequency sounds are localized in the medial superior olive (MSO) by calculating the interaural time difference (ITD; Goldberg and Brown, 1969)
The myelination thickness and the synaptic conductance were modeled in detail and compared with pure tone and natural sound stimulation regarding ITD coding accuracy and minimum temporal discrimination. Based on this spiking neural network (SNN) model and our decoding analysis, we found that the axon myelination patterns of both contralateral excitatory and inhibitory pathways can significantly modulate ITD decoding
Summary
The precise temporal information encoded in action potentials and trains of action potentials is one major mechanism contributing to accurate neural integration and information processing. For different species with different head sizes, the relationship between ITD and corresponding spatial angle varies, but for most species and most spatial angles, ITDs are one to two orders of magnitude shorter than the duration of an action potential To operate at such temporal precision, several neural mechanisms along the afferent pathways have been described, including kinetically fast ion channels, large and electrically compact synapses, tuning of cochlear, synaptic, post-synaptic, and transmission delays (reviewed in Trussell, 1999; Grothe, 2003; Tollin and Yin, 2009; Grothe et al, 2010). Some of these mechanisms remain plastic during an individual’s lifetime, allowing for a recalibration of the network, for example in response to hearing loss. The various inputs to MSO neurons show different axon myelination patterns, which precisely preserve and actively control the timing of action potentials propagated in these afferents, thereby controlling the sound localization process at MSO neurons
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