Primordial Rhythmic Bursting in Embryonic Cochlear Ganglion Cells

Abstract

This study examined the nature of spontaneous discharge patterns in cochlear ganglion cells in embryonic day 13 (E13) to early E17 chicken embryos (stages 39-43). Neural recordings were made with glass micropipettes. No sound-driven activity was seen for the youngest embryos (maximum intensity 107 dB sound pressure level). Ganglion cells were labeled with biotinylated dextran amine in four embryos. In two animals, primary afferents projected to hair cells in the middle region along the length of the basilar papilla in which, in one cell, the terminals occupied a neural transverse position and, in the other, a more abneural location. Statoacoustic ganglion cells showing no spontaneous activity were seen for the first time in the chicken. The proportion of "silent" cells was largest at the youngest stages (stage 39, 67%). In active cells, mean spontaneous discharge rates [9.4 +/- 10.4 spikes (Sp)/sec; n = 44] were lower than rates for older embryos (19 +/- 17 Sp/sec) (Jones and Jones, 2000). Embryos at stages 39-41 evidenced even lower rates (4.2 +/- 5.0 Sp/sec). The most salient feature of spontaneous activity for stages 39-43 was a bursting discharge pattern in >75% of active neurons (33 of 44). Moreover, in 55% of these cells, there was a clear, slow, rhythmic bursting pattern. The proportion of cells showing rhythmic bursting was greatest at the youngest stages (39-42) and decreased to <30% at stage 43. Rate of bursting ranged from 1 to 54 bursts per minute. The presence of rhythmic bursting in cochlear ganglion cells at E13-E17 provides an explanation for the existence of such patterns in central auditory relays. The bursting patterns may serve as a patterning signal for central synaptic refinements in the auditory system during development.

Early Postnatal Development of Spontaneous and Acoustically Evoked Discharge Activity of Principal Cells of the Medial Nucleus of the Trapezoid Body: AnIn VivoStudy in Mice

“…It is defined as the ratio of SD of interspike intervals (ISIs) and mean ISI (CV ϭ SD ISI /mean ISI ). Discharge patterns that follow a near Poisson-distributed process show CV values close to 1 and are found in mature sensory neurons (Walsh et al, 1972;Jones and Jones, 2000;Jones et al, 2001Jones et al, , 2007. Bursting patterns lead to CV values Ͼ1 (Jones and Jones, 2000;Jones et al, 2007).…”

“…The CV serves as a measure for regularity of spike discharges (Young et al, 1988;Jones and Jones, 2000;Jones et al, 2001Jones et al, , 2007. It is defined as the ratio of SD of interspike intervals (ISIs) and mean ISI (CV ϭ SD ISI /mean ISI ).…”

Unilateral cochlear ablation before hearing onset disrupts the maintenance of dorsal nucleus of the lateral lemniscus projection patterns in the rat inferior colliculus

“…As for the retina, cochlear activity begins quite early in development (Jhaveri et al, 1991;Lippe, 1994Lippe, ,1995Lin and Chen, 2000;Jones et al, 2001). The intrinsic bursting characterizing that activity may well have important implications for regulation of developing afferent projections in IC.…”

Time course of embryonic midbrain and thalamic auditory connection development in mice as revealed by carbocyanine dye tracing

“…Whereas recent data show that topographically distinct connections between the cochlea and cochlear nuclei can develop grossly normal even in the absence of hair cells (Xiang et al, 2003), the specific role of proper stimulation or the potential existence of spontaneous activity in the embryonic auditory system of mammals (Jones et al, 2001) requires further exploration beyond the already existing data (Gabriele et al, 2000b;Leake et al, 2002). Most importantly, it needs to be established how neonatal plasticity after the removal of a specific set of hair cells using high energy sound bursts can affect the cortical tonotopic representation.…”

“…The grossly normal formation of these connections is apparently specified by genes at the onset. Spontaneous activity, shown to play major roles in other systems such as the visual system (Rauschecker, 2002), seems to be of little importance here as no spontaneous activity has been reported thus far in such young embryonic mice (Jones et al, 2001). We are now using some of the mouse models with genetic alteration specifically of the periphery such as loss of hair cells or alteration of peripheral and central sensory neuron projections Xiang et al, 2003) to investigate how the central organization will be affected by these changes.…”