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Midbrain-Level Neural Correlates of Behavioral Tone-in-Noise Detection: Dependence on Energy and Envelope Cues
Journal of Neuroscience ( IF 4.4 ) Pub Date : 2021-08-25 , DOI: 10.1523/jneurosci.3103-20.2021
Yingxuan Wang , Kristina S. Abrams , Laurel H. Carney , Kenneth S. Henry

Hearing in noise is a problem often assumed to depend on encoding of energy level by channels tuned to target frequencies, but few studies have tested this hypothesis. The present study examined neural correlates of behavioral tone-in-noise (TIN) detection in budgerigars (Melopsittacus undulatus, either sex), a parakeet species with human-like behavioral sensitivity to many simple and complex sounds. Behavioral sensitivity to tones in band-limited noise was assessed using operant-conditioning procedures. Neural recordings were made in awake animals from midbrain-level neurons in the inferior colliculus, the first processing stage of the ascending auditory pathway with pronounced rate-based encoding of stimulus amplitude modulation. Budgerigar TIN detection thresholds were similar to human thresholds across the full range of frequencies (0.5–4 kHz) and noise levels (45–85 dB SPL) tested. Also as in humans, thresholds were minimally affected by a challenging roving-level condition with random variation in background-noise level. Many midbrain neurons showed a decreasing response rate as TIN signal-to-noise ratio (SNR) was increased by elevating the tone level, a pattern attributable to amplitude-modulation tuning in these cells and the fact that higher SNR tone-plus-noise stimuli have flatter amplitude envelopes. TIN thresholds of individual neurons were as sensitive as behavioral thresholds under most conditions, perhaps surprisingly even when the unit's characteristic frequency was tuned an octave or more away from the test frequency. A model that combined responses of two cell types enhanced TIN sensitivity in the roving-level condition. These results highlight the importance of midbrain-level envelope encoding and off-frequency neural channels for hearing in noise.

SIGNIFICANCE STATEMENT Detection of target sounds in noise is often assumed to depend on energy-level encoding by neural processing channels tuned to the target frequency. In contrast, we found that tone-in-noise sensitivity in budgerigars was often greatest in midbrain neurons not tuned to the test frequency, underscoring the potential importance of off-frequency channels for perception. Furthermore, the results highlight the importance of envelope processing for hearing in noise, especially under challenging conditions with random variation in background noise level over time.



中文翻译:

行为音调噪声检测的中脑级神经关联:对能量和包络线索的依赖

噪音中的听力是一个问题,通常被认为取决于调谐到目标频率的频道对能量水平的编码,但很少有研究验证这一假设。本研究检查了虎皮鹦鹉(Melopsittacus undulatus,无论是性别),一种长尾小鹦鹉物种,对许多简单和复杂的声音具有类似人类的行为敏感性。使用操作条件程序评估对带限噪声中的音调的行为敏感性。神经记录是在清醒动物的下丘中脑水平神经元中进行的,这是上行听觉通路的第一个处理阶段,具有明显的基于速率的刺激幅度调制编码。虎皮鹦鹉 TIN 检测阈值在测试的整个频率范围 (0.5–4 kHz) 和噪声水平 (45–85 dB SPL) 中与人类阈值相似。与人类一样,阈值受具有挑战性的流动水平条件的影响最小,背景噪声水平随机变化。随着 TIN 信噪比 (SNR) 通过提高音调水平而增加,许多中脑神经元显示出响应率下降,这种模式归因于这些细胞中的幅度调制调谐以及更高 SNR 音调加噪声刺激的事实具有更平坦的幅度包络。在大多数情况下,单个神经元的 TIN 阈值与行为阈值一样敏感,即使当单元的特征频率与测试频率相差一个八度或更多时,这可能令人惊讶。结合两种细胞类型响应的模型增强了流动水平条件下的 TIN 敏感性。这些结果突出了中脑级包络编码和离频神经通道在噪声中听力的重要性。归因于这些单元中的幅度调制调谐的模式以及更高 SNR 音调加噪声刺激具有更平坦的幅度包络的事实。在大多数情况下,单个神经元的 TIN 阈值与行为阈值一样敏感,即使当单元的特征频率与测试频率相差一个八度或更多时,这可能令人惊讶。结合两种细胞类型响应的模型增强了流动水平条件下的 TIN 敏感性。这些结果突出了中脑级包络编码和离频神经通道在噪声中听力的重要性。归因于这些单元中的幅度调制调谐的模式以及更高 SNR 音调加噪声刺激具有更平坦的幅度包络的事实。在大多数情况下,单个神经元的 TIN 阈值与行为阈值一样敏感,即使当单元的特征频率与测试频率相差一个八度或更多时,这可能令人惊讶。结合两种细胞类型响应的模型增强了流动水平条件下的 TIN 敏感性。这些结果突出了中脑级包络编码和离频神经通道在噪声中听力的重要性。s 特征频率被调谐到一个八度音程或更多远离测试频率。结合两种细胞类型响应的模型增强了流动水平条件下的 TIN 敏感性。这些结果突出了中脑级包络编码和离频神经通道在噪声中听力的重要性。s 特征频率被调谐到一个八度音程或更多远离测试频率。结合两种细胞类型响应的模型增强了流动水平条件下的 TIN 敏感性。这些结果突出了中脑级包络编码和离频神经通道在噪声中听力的重要性。

意义陈述噪声中目标声音的检测通常被假定依赖于通过调谐到目标频率的神经处理通道进行的能量水平编码。相比之下,我们发现虎皮鹦鹉的音调敏感性通常在未调整到测试频率的中脑神经元中最大,这强调了非频率通道对感知的潜在重要性。此外,结果强调了包络处理对噪声听力的重要性,尤其是在背景噪声水平随时间随机变化的挑战性条件下。

更新日期:2021-08-26
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