Abstract
Plasticity of myelination represents a mechanism to tune the flow of information by balancing functional requirements with metabolic and spatial constraints. The auditory system is heavily myelinated and operates at the upper limits of action potential generation frequency and speed observed in the mammalian CNS. This study aimed to characterize the development of myelin within the trapezoid body, a central auditory fiber tract, and determine the influence sensory experience has on this process in mice of both sexes. We find that in vitro conduction speed doubles following hearing onset and the ability to support high-frequency firing increases concurrently. Also in this time, the diameter of trapezoid body axons and the thickness of myelin double, reaching mature-like thickness between 25 and 35 d of age. Earplugs were used to induce ∼50 dB elevation in auditory thresholds. If introduced at hearing onset, trapezoid body fibers developed thinner axons and myelin than age-matched controls. If plugged during adulthood, the thickest trapezoid body fibers also showed a decrease in myelin. These data demonstrate the need for sensory activity in both development and maintenance of myelin and have important implications in the study of myelin plasticity and how this could relate to sensorineural hearing loss following peripheral impairment.SIGNIFICANCE STATEMENT The auditory system has many mechanisms to maximize the dynamic range of its afferent fibers, which operate at the physiological limit of action potential generation, precision, and speed. In this study we demonstrate for the first time that changes in peripheral activity modifies the thickness of myelin in sensory neurons, not only in development but also in mature animals. The current study suggests that changes in CNS myelination occur as a downstream mechanism following peripheral deficit. Given the required submillisecond temporal precision for binaural auditory processing, reduced myelination might augment sensorineural hearing impairment.
Highlights
Transmission of signals through the nervous system is determined by the number of action potentials (APs), their temporal precision, and the speed of propagation
We investigate in mice whether axonal diameter, myelin thickness, transmitted firing rates, and conduction speed in the trapezoid body (TB) fibers are coregulated during development and whether sound-evoked activity is essential to their maturation
Conduction speed of TB fibers increases rapidly within the first week of hearing and peaks ϳP18 A key feature of TB fibers in the mammalian brainstem is the transmission of auditory information with high firing rates
Summary
Transmission of signals through the nervous system is determined by the number of action potentials (APs), their temporal precision, and the speed of propagation. Some classes of auditory brainstem neurons, for example, the globular bushy cells (GBCs). Of the ventral cochlear nucleus (VCN), are capable of generating instantaneous rates in excess of 1000 Hz (Taberner and Liberman, 2005; Kopp-Scheinpflug et al, 2008a,b; Sonntag et al, 2009; Typlt et al, 2012). GBCs provide excitatory input to the principal neurons of the medial nucleus of the trapezoid body (MNTB) via a giant axosomatic synapse known as the calyx of Held (Held, 1893). Calyx synapses and MNTB principal neurons express a specialized complement of voltage and ligand-gated ion channels to allow AP generation at very high frequencies (Johnston et al, 2010; Kopp-Scheinpflug et al, 2011). GBC axons constitute part of the trapezoid body (TB), a large decussating fiber tract. TB fibers support high firing rates and their diameter and myelination allow adjustment of conduction speed to ensure that binaural auditory inputs coincide at superior olivary structures. GBC axons in gerbils are uniquely tuned according to their tonotopic termination site (Ford et al, 2015)
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