Noise-Sensitive But More Precise Subcortical Representations Coexist with Robust Cortical Encoding of Natural Vocalizations

Abstract

Humans and animals maintain accurate sound discrimination in the presence of loud sources of background noise. It is commonly assumed that this ability relies on the robustness of auditory cortex responses. However, only a few attempts have been made to characterize neural discrimination of communication sounds masked by noise at each stage of the auditory system and to quantify the noise effects on the neuronal discrimination in terms of alterations in amplitude modulations. Here, we measured neural discrimination between communication sounds masked by a vocalization-shaped stationary noise from multiunit responses recorded in the cochlear nucleus, inferior colliculus, auditory thalamus, and primary and secondary auditory cortex at several signal-to-noise ratios (SNRs) in anesthetized male or female guinea pigs. Masking noise decreased sound discrimination of neuronal populations in each auditory structure, but collicular and thalamic populations showed better performance than cortical populations at each SNR. In contrast, in each auditory structure, discrimination by neuronal populations was slightly decreased when tone-vocoded vocalizations were tested. These results shed new light on the specific contributions of subcortical structures to robust sound encoding, and suggest that the distortion of slow amplitude modulation cues conveyed by communication sounds is one of the factors constraining the neuronal discrimination in subcortical and cortical levels.

Neuronal selectivity to complex vocalization features emerges in the superficial layers of primary auditory cortex

“…When we computed the average MI in 100 ms time bins (50 ms slide; see Materials and methods) of the population of A1 L4 neurons as has been done in most earlier studies [49][50][51][52], we found low information levels throughout the response duration (Fig 8A, yellow) that were not significantly different (two-sided t test with FDR correction at each time point) from population MI present in the vMGB population (Fig 8A , blue). However, consistent with a recent result showing decreasing information content in the ascending auditory pathway of anesthetized GPs [53], we found significantly lower MI levels in the A1 L2/3 population (Fig 8A , red). We confirmed that this result held over a wide range of window sizes used for analysis (S1 Fig and data in Supporting information file S9 Data).…”

A complex feature-based representation of vocalizations emerges in the superficial layers of primary auditory cortex

“…8A, blue). However, consistent with a recent result showing decreasing information content in the ascending auditory pathway of anesthetized GPs [53], we found significantly lower MI levels in the A1 L2/3 population (Fig. 8A, red).…”

Natural Statistics as Inference Principles of Auditory Tuning in Biological and Artificial Midbrain Networks

“…These results suggest that the optimal representation of call statistics likely plays a role in facilitating the identification of different sound classes even in presence of noise. Similarly, a study with guinea pigs has shown the robust discrimination in the responses to communication sounds ( Souffi et al, 2020 ). Such hypothesis aligns with earlier reports ( Chechik et al, 2006 ) but remains to be validated in the IC of the big brown bat.…”