Functional Development of Principal Neurons in the Anteroventral Cochlear Nucleus Extends Beyond Hearing Onset

Abstract

Sound information is transduced into graded receptor potential by cochlear hair cells and encoded as discrete action potentials of auditory nerve fibers. In the cochlear nucleus, auditory nerve fibers convey this information through morphologically distinct synaptic terminals onto bushy cells (BCs) and stellate cells (SCs) for processing of different sound features. With expanding use of transgenic mouse models, it is increasingly important to understand the in vivo functional development of these neurons in mice. We characterized the maturation of spontaneous and acoustically evoked activity in BCs and SCs by acquiring single-unit juxtacellular recordings between hearing onset (P12) and young adulthood (P30) of anesthetized CBA/J mice. In both cell types, hearing sensitivity and characteristic frequency (CF) range are mostly adult-like by P14, consistent with rapid maturation of the auditory periphery. In BCs, however, some physiological features like maximal firing rate, dynamic range, temporal response properties, recovery from post-stimulus depression, first spike latency (FSL) and encoding of sinusoid amplitude modulation undergo further maturation up to P18. In SCs, the development of excitatory responses is even more prolonged, indicated by a gradual increase in spontaneous and maximum firing rates up to P30. In the same cell type, broadly tuned acoustically evoked inhibition is immediately effective at hearing onset, covering the low- and high-frequency flanks of the excitatory response area. Together, these data suggest that maturation of auditory processing in the parallel ascending BC and SC streams engages distinct mechanisms at the first central synapses that may differently depend on the early auditory experience.

Deletion of BDNF in Pax2 Lineage-Derived Interneuron Precursors in the Hindbrain Hampers the Proportion of Excitation/Inhibition, Learning, and Behavior

“…Juxtacellular single-unit recordings were performed in adult controls and in Bdnf Pax 2 KOs. The experimental protocol for such recordings was described previously ( Müller et al, 2019 ). Animals were intraperitoneally anesthetized with a mixture of ketamine hydrochloride (0.1 mg/g bodyweight; Ketamin-Ratiopharm, Ratiopharm) and xylazine hydrochloride (5 μg/g bodyweight; Rompun, Bayer).…”

Post-natal development of the envelope following response to amplitude modulated sounds in the bat Phyllostomus discolor

“…The above-described development-dependent changes can be contributed to maturational processes of the cochlea (Johnson et al, 2005) and the ascending auditory pathway (e.g. increasing number of action potentials (AP) in stellate cells or decreasing AP duration in bushy cells (Müller et al, 2019)). Additionally, the myelination of axons and maturation of mechanisms underlying synaptic transmission also add to said changes (Brenowitz and Trussell, 2001;Müller et al, 2019;Prado-Gutierrez et al, 2012;Shu Hui Wu and Oertel, 1987;Venkataraman and Bartlett, 2013).…”

“…increasing number of action potentials (AP) in stellate cells or decreasing AP duration in bushy cells (Müller et al, 2019)). Additionally, the myelination of axons and maturation of mechanisms underlying synaptic transmission also add to said changes (Brenowitz and Trussell, 2001;Müller et al, 2019;Prado-Gutierrez et al, 2012;Shu Hui Wu and Oertel, 1987;Venkataraman and Bartlett, 2013). In cats, the onset of myelination occurred at p5 and reached a rate of 70% by p10 (Ryugo et al, 2006).…”

“…The post-natal development of processing of temporal modulations has been already investigated in several mammalian species, e.g. gerbils (Heil et al, 1995;Khurana et al, 2012), mice (Müller et al, 2019), harbour porpoises (Linnenschmidt et al, 2013) and in humans (Draganova et al, 2018;Rance et al, 2006;Walker et al, 2019). However, data for bats are lacking so far.…”

Two types of somatic spines provide sites for intercellular signaling during calyx of Held growth and maturation

“…Previous studies have shown many of the morphological stages of CH formation occur largely during the first week of life and ahead of the onset of hearing in mice (Hoffpauir et al, 2006;Holcomb et al, 2013;Kandler & Friauf, 1993;Taschenberger et al, 2002). However, auditory neurons continue to undergo changes to intrinsic and synaptic properties until the system nears maturity as early as P30 in both brainstem nuclei (Müller et al, 2019) as well as within the auditory cortex (Carrasco et al, 2013). We next examined the prevalence of type 1 spines and spine mats across principal neurons of the MNTB at early postnatal ages (P3, 4, 6, 9) in relation to young adult mice (P30).…”