Comodulation Enhances Signal Detection via Priming of Auditory Cortical Circuits

Abstract

Acoustic environments are composed of complex overlapping sounds that the auditory system is required to segregate into discrete perceptual objects. The functions of distinct auditory processing stations in this challenging task are poorly understood. Here we show a direct role for mouse auditory cortex in detection and segregation of acoustic information. We measured the sensitivity of auditory cortical neurons to brief tones embedded in masking noise. By altering spectrotemporal characteristics of the masker, we reveal that sensitivity to pure tone stimuli is strongly enhanced in coherently modulated broadband noise, corresponding to the psychoacoustic phenomenon comodulation masking release. Improvements in detection were largest following priming periods of noise alone, indicating that cortical segregation is enhanced over time. Transient opsin-mediated silencing of auditory cortex during the priming period almost completely abolished these improvements, suggesting that cortical processing may play a direct and significant role in detection of quiet sounds in noisy environments.SIGNIFICANCE STATEMENT Auditory systems are adept at detecting and segregating competing sound sources, but there is little direct evidence of how this process occurs in the mammalian auditory pathway. We demonstrate that coherent broadband noise enhances signal representation in auditory cortex, and that prolonged exposure to noise is necessary to produce this enhancement. Using optogenetic perturbation to selectively silence auditory cortex during early noise processing, we show that cortical processing plays a crucial role in the segregation of competing sounds.

Contributions of distinct auditory cortical inhibitory neuron types to the detection of sounds in background noise

“…Consistent with the effect of comodulation masking release (Schooneveldt and Brian Moore, 1989;Sollini and Chadderton, 2016), sensitivity to the pure tone signal was lower when the noise masker had a narrow bandwidth (0.25 octaves) compared to a broad bandwidth (white noise), despite the greater power contained within the broadband noise masker (median d = 0.797 across mice for narrowband masker, median d = 1.190 for broadband, p = 4.67 × 10 −6 , Wilcoxon signed-rank test, N = 48 mice). Hit rates and false alarm rates were both significantly higher when the masker was narrowband rather than broadband (median narrowband hit rate = 81%, median broadband hit rate = 65%, p = 3.38 × 10 −13 ; median narrowband false alarm rate = 46%, median broadband hit rate = 21%, p = 5.11 × 10 −13 ; Wilcoxon signed-rank test).…”

Spatial Processing Is Frequency Specific in Auditory Cortex But Not in the Midbrain

“…Naturally, our model does not represent the full complexity of known ILD computations. In the AC ( Kyweriga et al, 2014 , Sollini and Chadderton, 2016 ) and IC ( Li and Pollak, 2013 , Xiong et al, 2013 , Ono and Oliver, 2014 ), there is ample evidence of local inhibition and excitation shaping responses of all types and in IC and even the cochlear nucleus ( Park et al, 1997 , Sanes et al, 1998 , Burger and Pollak, 2001 , Shore et al, 2003 , Pecka et al, 2007 , Dahmen et al, 2010 , Pollak, 2012 , Yao et al, 2015 , Orton et al, 2016 ). In addition, recent evidence in the rat suggests sharpening of ILD tuning between IC and MGB ( Yao et al, 2015 ).…”

Listening in complex acoustic scenes

“…Surprisingly, the presence of continuous broadband noise has been found to improve tone discrimination for small frequency differences in mice and this behavioral improvement could be replicated by optogenetically activating parvalbumin-positive interneurons in order to make A1 tuning curves resemble those recorded in the presence of noise [ 41 • ]. Furthermore, A1 neuronal sensitivity to tones presented in noise is enhanced if coherently modulated sidebands are added to the noise masker, a condition that improves signal detection thresholds in humans [ 42 ]. Like the release from masking found for speech-in-noise recognition noise by human listeners [ 14 , 15 ], prior adaptation to the noise is required to produce substantial comodulation masking release in A1 and this was reduced by inhibiting cortical activity during the priming period [ 42 ].…”

“…Furthermore, A1 neuronal sensitivity to tones presented in noise is enhanced if coherently modulated sidebands are added to the noise masker, a condition that improves signal detection thresholds in humans [ 42 ]. Like the release from masking found for speech-in-noise recognition noise by human listeners [ 14 , 15 ], prior adaptation to the noise is required to produce substantial comodulation masking release in A1 and this was reduced by inhibiting cortical activity during the priming period [ 42 ].…”