Enriched acoustic environment after noise trauma reduces hearing loss and prevents cortical map reorganization

Abstract

Exposure to sound of sufficient duration and level causes permanent damage to the peripheral auditory system, which results in the reorganization of the cortical tonotopic map. The changes are such that neurons with pre-exposure tuning to frequencies in the hearing loss range now become tuned to frequencies near the near-normal lower boundary of the hearing loss range, which thus becomes over represented. However, cats exposed to a traumatizing noise and immediately thereafter placed for a few weeks in an enriched acoustic environment presented a much-restricted hearing loss compared with similarly exposed cats that were placed for the same time in a quiet environment. The enriched environment spectrally matched the expected hearing loss range and was approximately 40 dB above the level of the expected hearing loss. The hearing loss in the quiet environment-reared cats ranged from 6 to 32 kHz with the largest loss (on average, 40 dB) ranging from 24 to 32 kHz. In contrast, the hearing loss in the enriched-environment cats was restricted to 6-8 kHz at a level of, on average, 35 dB and with 16-32 kHz having normal thresholds. Despite the remaining hearing loss for the enriched-environment cats in the 6-8 kHz range, plastic tonotopic map changes in primary auditory cortex could no longer be demonstrated, suggesting that the enriched acoustic environment prevents this reorganization. This finding has implications for the treatment of hearing disorders, such as tinnitus, that have been linked to cortical tonotopic map reorganization.

Figure 1.

Averaged ABR threshold shifts across the three groups. The threshold shifts in group 1 cats, group 2 cats, and control cats, represented by open circles, filled triangles, and gray filled circles, respectively. A negative shift is considered equal to the amount of hearing loss. Vertical bars indicate the SEM.

Figure 2.

Compound CF maps in AI in control cats (A), group 1 cats (B), and group 2 cats (C). The center of each polygon, constructed using the tessellation method (MatLab), corresponds to the coordinates of a recording site in auditory cortex along the anteroposterior axis (abscises) and the ventrodorsal axis (ordinates). The tip of the posterior ecto-Sylvian sulcus was taken as the (0,0) coordinate. The CF is represented by color; cold colors (blue-like) represent low CF, and hot colors (red-like) represent high CF as indicated by the color bar.

Figure 3.

CF of AI neurons according to the location of the recording site along the anteroposterior axis relative to the CF = 8 kHz location in each cat (a), thresholds at CF according to the location of the recording site along the anteroposterior axis relative to CF = 8 kHz in each cat (b), and thresholds at CF as a function of CF (c). group 1 cats, group 2 cats, and control cats are represented by open circles, filled triangles, and filled gray circles, respectively. Lines represent locally weighted regression curves (solid gray lines, control; thin black lines, group 2; thick black lines, group 1).

Figure 4.

Comparison between two cats having similar hearing loss but different posttrauma exposure and a control (normal hearing) cat. a, ABR threshold shifts. b, CF of AI neurons according to the location of the recording site along the anteroposterior axis. The group 2 cat, group 1-type cat, and the control cat are represented by filled triangles, open squares, and filled gray circles, respectively.