Evidence of activity-dependent plasticity in the dorsal cochlear nucleus, in vivo, induced by brief sound exposure

Abstract

The purpose of the present study was to investigate the immediate effects of acute exposure to intense sound on spontaneous and stimulus-driven activity in the dorsal cochlear nucleus (DCN). We examined the levels of multi- and single-unit spontaneous activity before and immediately following brief exposure (2 min) to tones at levels of either 109 or 85 dB SPL. Exposure frequency was selected to either correspond to the units' best frequency (BF) or fall within the borders of its inhibitory side band. The results demonstrate that these exposure conditions caused significant alterations in spontaneous activity and responses to BF tones. The induced changes have a fast onset (minutes) and are persistent for durations of at least 20 min. The directions of the change were found to depend on the frequency of exposure relative to BF. Transient decreases followed by more sustained increases in spontaneous activity were induced when the exposure frequency was at or near the units' BF, while sustained decreases of activity resulted when the exposure frequency fell inside the inhibitory side band. Follow-up studies at the single unit level revealed that the observed activity changes were found on unit types having properties which have previously been found to represent fusiform cells. The changes in spontaneous activity occurred despite only minor changes in response thresholds. Noteworthy changes also occurred in the strength of responses to BF tones, although these changes tended to be in the direction opposite those of the spontaneous rate changes. We discuss the possible role of activity-dependent plasticity as a mechanism underlying the rapid emergence of increased spontaneous activity after tone exposure and suggest that these changes may represent a neural correlate of acute noise-induced tinnitus.

Keywords: Acute noise-induced tinnitus; Dorsal cochlear nucleus; Hyperactivity; Long-term potentiation.

Copyright © 2016 Elsevier B.V. All rights reserved.

Figures

Figure 1

Effect of an acute 10 kHz tone exposure on multiunit surface activity in the middle frequency region of the DCN. (a) Transverse view of the DCN showing the location of the recording electrode in the m.f. (mid-frequency: 8–12 kHz) region of the DCN. l.f., low frequency. h.f., high frequency. (b) Spontaneous activity recorded from the 9 kHz locus during an extended period of silence. Dashed line indicates baseline activity. (c–d) Tuning curves and spontaneous activity recorded from the 9 kHz locus of a single animal before and after a 2 minute exposure to a 10 kHz (109 db SPL) tone. (e) Mean spontaneous activity of 5 animals recorded in region m.f. before and after a two minute exposure to a 10 kHz tone at 109 dB SPL. (f) Averaged mean threshold shifts at BF in the five animals that were included in (e).

Figure 2

Effect of an acute 10 kHz tone exposure on multiunit surface activity in the low (3–8 kHz) and high (12–30 kHz) frequency regions of the DCN. (a) Transverse view of the DCN showing the locations of the three frequency regions (l.f., m.f., h.f.) and the differences in their underlying circuit connections with the cochlea. (b–c) Spontaneous activity recorded at the 16 kHz and 5 kHz loci, respectively. Inset in (c), comparison between DCN surface activity recorded at l.f. and m.f. in the same animal. (d) Normalized mean spontaneous activity of 4 animals recorded at l.f. before and after exposure to a 10 kHz tone (109 dB SPL). (e) Comparison of changes in mean multiunit spontaneous activity in the mid- and low-frequency regions of the DCN. Exposure tone was the same as that used for Fig. 1 data (10 kHz, 109 dB SPL, 2 minutes). (f) Tuning curves measured in the same 4 animals represented in (d) before (upper row) and after exposure (lower row). CC, cartwheel cell; FC, fusiform cell; GC, granule cell; Gi, giant cell; VC, vertical cell.

Figure 3

Intensity dependence of the long-lasting enhancement of multiunit spontaneous activity recorded in the m.f. region of the DCN following a 2 minute exposure to a 10 kHz tone. (a) Time course of activity changes recorded before and following tone exposure at a level of 85 dB SPL. Dashed line indicates baseline activity before sound exposure. (b) Comparison of the ratios of post-exposure to pre-exposure activity obtained following exposure to a tone at 109 and 85 dB SPL. Asterisks indicate p < 0.05, Mann-Whitney U test.

Figure 4

Effect of tone exposure on single unit spontaneous activity when the frequency of the exposure tone (10 kHz) was at or near the unit’s BF (9 kHz). (a) Demonstration of a persistent increase of SFR in a neuron with the properties of fusiform cells. The unit displayed a typical type III frequency response map (a1) and a chopper PST histogram pattern (a2). In panel a3, it can be seen that spontaneous activity in the same cell represented in a1 and a2 increased after a 2 minute exposure to the BF tone (109 dB SPL). (b) Normalized mean spontaneous activity recorded in 8 type III units, showing the persistent increase of SFR following exposure to a two minute BF tone (109 dB SPL). Black dots represent the normalized mean spontaneous activity from 8 units and grey dots represent points where data was available for only 3 of the 8 units. (c) Comparison of long-term activity changes observed in multiunit and single unit recordings. Dashed line in a3 and b indicates baseline activity before sound exposure.

Figure 5

Effect of tone exposure on single unit spontaneous activity when the frequency of the exposure tone (10 kHz) fell within the unit’s inhibitory side band. (a) Response maps for each of 8 type III units, showing the tuned excitatory areas and their flanking inhibitory side bands (areas in which spontaneous activity was absent). (b) Normalized time course of mean spontaneous activity change averaged across the 8 type III units shown in panel a. Tone exposure duration and intensity were two minutes and 109 dB SPL, respectively. c) Differences of the long-term activity changes following the tone exposure to different frequencies. Dashed lines in b and c indicate baseline activity before and after sound exposure.

Figure 6

Effect of tone exposure on stimulus-elicited responses of type III units based on comparisons of RIFs collected at BF before and after tone exposure. (a) Tuning curves measured from a unit (#1) before and after exposure to a BF tone (8 kHz, 109 dB SPL, 2 minutes). (b) PSTH collected in the same unit as that in (a). (c) RIFs at BF in 4 type III units (#1–4). The post-exposure RIF curves showed lower maxima than the pre-exposure curves except that collected in unit #4. (d) Response maps from a unit with a type III response (#6) before and after exposure to an 11 kHz tone (109 dB SPL, 2 minute), which fell into the unit’s inhibitory side band (BF = 7 kHz). (e) PST histogram collected from the same unit as in (d). (f) RIFs collected at BF from 7 units with type III response maps (#5–11). The post-exposure RIF curve showed higher maxima than the pre-exposure curve except that collected from unit #8.