Changes in neuronal representations of consonants in the ascending auditory system and their role in speech recognition

Abstract

A fundamental task of the ascending auditory system is to produce representations that facilitate the 11 recognition of complex sounds. This is particularly challenging in the context of acoustic variability, 12 such as that between different talkers producing the same phoneme. These representations are 13 transformed as information is propagated throughout the ascending auditory system from the inner 14 ear to the auditory cortex. Investigating these transformations and their role in speech recognition is 15 key to understanding hearing impairment and the development of future clinical interventions. Here, 16 we obtained neural responses to an extensive set of natural vowel-consonant-vowel phoneme 17 sequences, each produced by multiple talkers, in three stages of the auditory processing pathway. 18 Auditory nerve (AN) representations were simulated using a model of the peripheral auditory system 19 and extracellular neuronal activity was recorded in the inferior colliculus (IC) and the primary 20 auditory cortex (AI) of anaesthetised guinea pigs. A classifier was developed to examine the efficacy 21 of these representations for recognizing the speech sounds. Individual neurons convey progressively 22 less information from AN to AI. Nonetheless, at the population level, representations are sufficiently 23 rich to facilitate recognition of consonants with a high degree of accuracy at all stages indicating a 24 progression from a dense, redundant representation to a sparse, distributed one. We examined the 25 timescale of the neural code for consonant recognition and found that optimal timescales increase 26 throughout the ascending auditory system from a few milliseconds in the periphery to several tens of 27 milliseconds in the cortex. Despite these longer timescales, we found little evidence to suggest that 28 representations up to the level of AI become increasingly invariant to across-talker differences. 29 Instead, our results support the idea that the role of the subcortical auditory system is one of 30 dimensionality expansion, which could provide a basis for flexible classification of arbitrary speech 31 sounds.