| Human speech and animal communication sounds contain rapid time-varying amplitude and spectral information. The accurate processing of sound temporal information by auditory system is crucial to human speech perception and other species-specific communication. Previous studies have shown that the encoding of sound envelope rise-fall time and sound gap duration undergoes a progressive postnatal development and refinement. During postnatal development, the function of auditory cortex undergoes environmental and experience-dependent plasticity; environmental noise exposure impairs the cortical processing of sound frequency, level, and spatial information; in contrast, environmental enrichment can enhance the cortical plasticity and rescue the degraded processing of sound frequency information. However, how postnatal environment affects cortical processing of sound temporal information is not fully understood. The aim of the present study was to determine whether postnatal noise exposure impairs neural temporal processing in the auditory cortex, and if so, whether environmental enrichment can rescue this degraded neural temporal acuity. To answer these questions, we used electrophysiological method and extracellular single-cell recording technique to study the effects of various postnatal environments on neural encoding of sound envelope rise-fall time and sound gap durations in the auditory cortex of Sprague-Dawley rats. The results are as follows:1. The effects of postnatal noise exposure on neural processing of sound envelope rise-fall time in the rat auditory cortexThe study was conducted in 22 rats in control group (CON group) that reared in normal environment during postnatal day (P) 1-77,21 rats in critical period noise exposure group (CPN group) that were exposed in 70 dB SPL white noise environment during P10-P31 and reared in normal environment during P1-P8, and P32-P77, and 20 rats in adult noise exposure group (AN group) that were reared in normal environment during P1-P56 and exposed to 70 dB SPL white noise environment during P57-P77. All of the rats were used to do physiological recording after P77. We determined the dependence of neural response strength and first spike latency on sound rise-fall time across sound levels in the rat primary auditory cortex (Al). Statistically analysis showed that, at a given sound level and rise-fall time, the average neural response strength and normalized neural response strength of Al neurons in CPN group were significantly lower than those in both CON group and AN group, and the average first spike latencies and latency differences of Al neurons in CPN group were significantly longer than those in both CON group and AN group. Whereas the average response strength did not differ significantly between the CON group and the AN group, the Al neurons in AN group showed longer first spike latencies compared to those in CON group. The slopes of average latency change across rise-fall time were greater in CPN group than those in CON group and AN group. These results indicated that postnatal moderate-level noise exposure impaired the cortical neural processing of sound envelope rise-fall time, and that the effect of noise exposure was greater during the critical period of postnatal hearing development than that during adulthood.2. The effects of postnatal noise exposure at young age and in adulthood on the cortical neural processing of sound gap duration in adulthoodWe used 23 rats in CON group,48 rats in CPN group, and 28 rats in AN group in this study. We determined the response strength and response latency of A1 neurons to pairs of noise bursts (white noise), and we compared the minimum thresholds, response latencies, and the neural gap detection thresholds among the three groups. We found that, compared with the minimum thresholds of A1 neurons in the CON group, moderate-level noise exposure significantly elevated the minimum thresholds of Al neurons in the CPN group but not in the AN group. In contrast, noise exposure increased the response latencies of Al neurons in both CPN group and AN group, but the noise exposure had greater effects on the response latencies of Al neurons in the CPN group than in the AN group. Moreover, moderate-level noise exposure to juvenile rats induced much higher neural gap detection thresholds in adulthood than the same noise exposure to adult rats. These results demonstrated that postnatal noise exposure degraded the auditory neural temporal resolution in the rat auditory cortex, and the effects of noise exposure in juvenile rats were greater than those in adult rats.3. Environmental enrichment rescued the poor auditory temporal resolution in Al induced by early noise exposureTo determine whether postnatal environmental enrichment (EE group) have impacts on the auditory temporal resolution in normally developing rats, we reared rats in the environmental enrichment during P10-P56, and in normal environment during P1-P9, and P57-P77. We found that the neural gap detection thresholds, the minimum thresholds, and the response latencies of A1 neurons in this EE group were not significantly different from those in the CON group. We then tested whether EE can rescue the degraded auditory temporal resolution induced by noise exposure at young age, and we reared rats that were exposed to 70 dB SPL white noise during P10-31 and the environmental enrichment during P31-P56 (CPN+EE group). We found that the neural gap detection thresholds in this CPN+EE group were much lower than those in CPN group, but were still higher than that in CON group. These data demonstrated that, in our experimental conditions, EE indeed rescue the impaired neural temporal resolution of A1 units induced by early noise exposure; However, EE did not fully restore the impaired neural gap detection thresholds to the control level. Next, we determined the contribution of the acoustic component in the EE in rescuing the noise-induced degraded neural temporal resolution, and we reared the early noise-exposed rats in standard cages during P31-P56 but with the same tone stimuli exposure used in the EE conditions (CPN+Tone group). The neural gap detection thresholds in this CPN+Tone group were much higher than those in CPN+EE group, and were lower than those in CPN group. These data indicated that the use of environmental enrichment was more effective in rescuing the impaired auditory temporal resolution than the use of tone exposure alone.In summary, postnatal noise exposure during the critical period of hearing development impairs the auditory cortical processing of sound envelope rise-fall time and sound gap duration, and environmental enrichment can rescue the degraded auditory neural temporal resolution in Al induced by postnatal early noise exposure. These results provide new evidences to help us to understand the postnatal environmental-dependent auditory functional plasticity, and provide experimental and theoretic evidences for rescuing the deficit in auditory temporal information processing in the central auditory system. |
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