Noise trauma induced plastic changes in brain regions outside the classical auditory pathway

Abstract

The effects of intense noise exposure on the classical auditory pathway have been extensively investigated; however, little is known about the effects of noise-induced hearing loss on non-classical auditory areas in the brain such as the lateral amygdala (LA) and striatum (Str). To address this issue, we compared the noise-induced changes in spontaneous and tone-evoked responses from multiunit clusters (MUC) in the LA and Str with those seen in auditory cortex (AC) in rats. High-frequency octave band noise (10-20 kHz) and narrow band noise (16-20 kHz) induced permanent threshold shifts at high-frequencies within and above the noise band but not at low frequencies. While the noise trauma significantly elevated spontaneous discharge rate (SR) in the AC, SRs in the LA and Str were only slightly increased across all frequencies. The high-frequency noise trauma affected tone-evoked firing rates in frequency and time-dependent manner and the changes appeared to be related to the severity of noise trauma. In the LA, tone-evoked firing rates were reduced at the high-frequencies (trauma area) whereas firing rates were enhanced at the low-frequencies or at the edge-frequency dependent on severity of hearing loss at the high frequencies. The firing rate temporal profile changed from a broad plateau to one sharp, delayed peak. In the AC, tone-evoked firing rates were depressed at high frequencies and enhanced at the low frequencies while the firing rate temporal profiles became substantially broader. In contrast, firing rates in the Str were generally decreased and firing rate temporal profiles become more phasic and less prolonged. The altered firing rate and pattern at low frequencies induced by high-frequency hearing loss could have perceptual consequences. The tone-evoked hyperactivity in low-frequency MUC could manifest as hyperacusis whereas the discharge pattern changes could affect temporal resolution and integration.

Keywords: amygdala; hyperacusis; neural plasticity; noise trauma; striatum; tinnitus.

Figure 1

Blue open bars and black filled bars show the dB SPL measured in one-third octave bands for the 10–20 kHz OBN and 16–20 kHz NBN. The dashed line and hatched area show the background noise in the colony.

Figure 2

Mean (±SEM) ABR threshold shifts as a function of frequency induced by (A) the OBN and (C) the NBN. Mean (±SEM) OHC and IHC loss in the group exposed to the OBN noise (B) and the NBN (D). Red horizontal bars show location of the noise bands. The arrows sh ow the high-frequency edge of the noise band.

Figure 3

Representative responses from MUC in the primary AC, Str and LA. (A): Peristimulus time histograms (PSTH) of a MUC recorded in the AC in response to 18.3 kHz tone bursts presented at 100 dB SPL; note short-latency, sharp onset response. (B): PSTH of a MUC in the Str to 18.3 kHz tone bursts presented at 100 dB SPL; note short-latency, sharp onset response. (C1): PSTH of a MUC in the LA to 3.5 kHz tone bursts presented at 100 dB SPL; not early and late response components. (C2) PSTH of a MUC in the LA in response to 18.3 kHz tone bursts presented at 100 dB SPL; note broad, late response. Horizontal bars show location of 50 ms tone burst stimulation. The approximate locations of the three recording sites are shown in the coronal schematic (D).

Figure 4

Examples of frequency receptive field of MUC in the AC (A), Str (B), and LA (C). Each panel shows the frequency (x axis, 10 frequencies, 1–42 kHz) vs intensity (y axis, 0–100 dB, 20 dB steps) matrix of MUC PSTHs for the AC (A), Str (B), and LA (C). The line in each plot outlines the tuning curve of the MUC with approximate CF shown below. X-axis of PSTH is 200 ms; y-axis is 500 spikes/s for A and B and 150 spikes/s for C; Stimulus duration is 50 ms.

Figure 5

(A) Overall group mean (±SEM) SR in the AC, LA and Str of control rats and rats exposed to the OBN or NBN (see inset). In the AC, the mean SR of all neurons in the OBN group and the NBN group were significantly greater than the control group. In the LA, the mean SR of all MUC in the OBN group was significantly greater than the control group. In the Str, mean SR in the OBN and NBN groups were significantly greater than the control groups. (B) The AC-MUC were separated into low-CF (≤8 kHz) and high-CF (≥12 kHz) groups. The mean SR of high-CF MUC were significantly greater than the control group in both the OBN and NBN groups, but for the low-CF MUC the significance was only observed in the NBN group. (C) The LA-MUC were separated into low-CF (≤8 kHz) and high-CF (≥12 kHz) groups. The mean SR of low-CF MUC in the OBN group was significantly greater than the control group, but all other noise-exposed LA-MUC did not show significant difference from the control. * p<0.05; *** p<0.001, see text for details.

Figure 6

(A): Population PSTH frequency-intensity matrix for LA MUC in the control group (n = 103, blue line) and the OBN group (n = 140, red line). Tone burst (50 ms) frequencies and intensities indicated on abscissa and ordinate. Red-up arrowhead and black-down arrowhead point to the approximate frequency-intensity regions where there were large increase (hyperactivity) and decrease (hypoactivity) in firing rate in the OBN group compared to the control group. (B): Population PSTH responses in the control group (blue line) and OBN group (red line) to 1 kHz tone bursts (50 ms) presented at 100, 80, and 60 dB SPL. Red-up arrowheads show the region of the PSTH where there was a large increase (hyperactivity) in firing rate in the OBN group compared to the control group. (C) Population PSTH responses in the control group (blue line) and OBN group (red line) to 12.1 kHz tone bursts (50 ms) presented at 100, 80, and 60 dB SPL. Black-down arrowheads show regions of PSTH where there was a large decrease in spike rate in the OBN-group. (D): Population PSTH responses in the control group (blue line) and OBN group (red line) in response to an 8 kHz (edge frequency) tone burst (50 ms) presented at 100, 80, and 60 dB SPL. Black-down arrowheads show regions were there was a large decrease in spike rate. PSTH: 500 ms x-axis; 60 spikes/s y-axis. Significant changes in PSTH profiles: **p<0.01; ***p<0.001; see text for details.

Figure 7

(A) PSTH frequency-intensity matrix for LA MUC in the control group (n = 103, blue line) and the NBN group (n = 183, red line). Tone burst (50 ms) frequencies and intensities indicated on abscissa and ordinate. Red-up arrowhead and black-down arrowhead point to the approximate frequency-intensity regions where there were large increases (hyperactivity) and decreases (hypoactivity) in firing rate in the NBN group compared to the control group. (B): Population PSTH responses in the control group (blue line) and NBN group (red line) to 1 kHz tone bursts (50 ms) presented at 100, 80, and 60 dB SPL. Red-up arrowheads show the region of the PSTH where there was a large increase (hyperactivity) in firing rate in the NBN group compared to the control group. (C) Population PSTH responses in the control group (blue line) and NBN group (red line) to 18.3 kHz tone bursts (50 ms) presented at 100, 80, and 60 dB SPL. Black-down arrowheads show regions of PSTH where there was a large decrease in spike rate in the NBN group. (D) Population PSTH responses in the control group (blue line) and NBN group (red line) in response to a 12.1 kHz (edge-frequency) tone burst (50 ms) presented at 100, 80, and 60 dB SPL. Red arrowhead shows region of PSTH where there was an increase in spike rate in the NBN group. PSTH: 500 ms x-axis; 60 spikes/s y-axis. Significant changes in PSTH profiles: **p<0.01; ***p<0.001; see text for details.

Figure 8

(A): Population PSTH (500 ms) of LA MUC in control group (blue line, n=103) and NBN exposed rats (red line, n=88) with 30 dB of PTS in the noise band (16–20 kHz); data shown for 80 dB SPL tone bursts (50 ms) presented at 1.0, 12.1 and 18.3 kHz. Note large increase in firing rate at 1 kHz (red-up arrowhead) and large reduction at 18.3 kHz (black-down arrowhead), but no change at 12.1 kHz (edge frequency). (B) Population PSTH (500 ms) of LA MUC in the control group (blue line, n=103) and NBN exposed rats (red line, n=95) with 16 dB of PTS in the noise band (16–20 kHz); data shown for tone bursts (50 ms) presented at 1.0, 12.1 and 18.3 kHz at 80 dB SPL. No change in PSTH at 1.0 kHz, slight enhancement at 12.1 kHz (edge frequency), and slight reduction at 18.3 kHz. Significant changes in PSTH profiles: *p<0.05; ***p<0.001; see text for details.

Figure 9

(A): Population PSTH frequency-intensity matrix for AC MUC in the control group (n = 548, blue line) and the OBN group (n = 224, red line) Tone burst (50 ms) frequencies and intensities indicated on abscissa and ordinate. Red-up arrowhead and black-down arrowhead point to the approximate frequency-intensity regions where there were large increase (hyperacti vity) and decrease (hypoactivity) in firing rate in the OBN group compared to the control group. (B): Population PSTH responses in the control group (blue line) and OBN group (red line) to 1 kHz tone bursts (50 ms) presented at 100, 80, and 60 dB SPL. Red-up arrowheads show the region of the PSTH where there was a large increase (hyperactivity) in firing rate in the OBN group compared to the control group. (C) Population PSTH responses in the control group (blue line) and OBN group (red line) to 12.1 kHz tone bursts (50 ms) presented at 100, 80, and 60 dB SPL. Black-down arrowheads show regions of PSTH where there was a large decrease in spike rate in the OBN-group. (D): Population PSTH responses in the control group (blue line) and OBN group (red line) in response to an 8 kHz (edge frequency) tone burst (50 ms) presented at 100, 80, and 60 dB SPL. Black-down arrowheads show regions where there was a large decrease in spike rate. PSTH: 200 ms x-axis; 250 spikes/s y-axis. Significant changes in PSTH profiles: ***p<0.001; see text for details.

Figure 10

(A): Frequency-intensity matrix showing population PSTHs (200 ms duration, ordinate; 250 spikes/s) of AC MUC in the control group (blue line, n=548) and NBN group (red line, n=236); data obtained with 50 ms tone bursts (1 to 42. kHz, 0–100 dB SPL, 20-dB steps). Red-up arrowhead shows low-frequency regions where firing rates and response duration increased; black-down arrowhead shows high-frequency region where spike rate decreased. (B) Population PSTHs to 1.0 kHz tone bursts (50 ms) presented at 100, 80, and 60 dB SPL; note significant increase in response duration and mean discharge rates in 100 ms duration (red-up arrowheads); (C): Population PSTHs (200 ms, 250 spikes/s) to 18.3 kHz tone bursts presented at 100, 80 and 60 dB SPL showing reduction in spike rate during the stimulus (black-down arrowheads) followed by late response (red up arrows). (D) Population PSTHs (200 ms; 250 spikes/s) to 12.1 kHz tone bursts (edge frequency) at 100, 80, and 60 dB SPL. Note significant increase in response duration and mean discharge rate (red up arrowheads) and increased late component (red up arrows). Significant changes in PSTH profiles: ***p<0.001; see text for details.

Figure 11

(A): Frequency-intensity matrix of population PSTHs (100 ms duration, ordinate 200 spikes/s) of Str MUC in the control group (blue line, n=95) and the OBN group (red line, n=261). Note reduction firing rate and response duration in high-frequency, high-intensity PSTH in the OBN group. (B) Frequency-intensity matrix of population PSTHs (100 ms duration; ordinate 200 spikes/s) in Str MUC of the control group (blue line, n=95) and the NBN group (red line, n=226). Note reduction in spike rate and decrease in response duration in the NBN group compared to the control group.

Figure 12

Schematic describing the relation between the degree of high-frequency hearing loss (severe, moderate and minor) and changes in suprathreshold population response profiles in the low-frequency, edge-frequency and high-frequency regions. (A) In cases of severe high-frequency hearing loss, low-frequency regions become extremely hyperactive, the edge-frequency becomes mildly hypoactive and the high-frequency region become very hypoactive. (B) In cases of moderate high-frequency hearing loss, low-frequency regions become mildly hyperactive, little change occurs at the edge-frequency region and the high-frequency region becomes moderately hypoactive. (C) In cases of minor high-frequency hearing loss, the low-frequency region shows no change at suprathreshold intensities; the edge-frequency becomes mildly hyperactive and the high-frequency region is mildly hypoactive.