Abstract

The processing characteristics of neurons in the central auditory system are directly shaped by and reflect the statistics of natural acoustic environments, but the principles that govern the relationship between natural sound ensembles and observed responses in neurophysiological studies remain unclear. In particular, accumulating evidence suggests the presence of a code based on sustained neural firing rates, where central auditory neurons exhibit strong, persistent responses to their preferred stimuli. Such a strategy can indicate the presence of ongoing sounds, is involved in parsing complex auditory scenes, and may play a role in matching neural dynamics to varying time scales in acoustic signals. In this paper, we describe a computational framework for exploring the influence of a code based on sustained firing rates on the shape of the spectro-temporal receptive field (STRF), a linear kernel that maps a spectro-temporal acoustic stimulus to the instantaneous firing rate of a central auditory neuron. We demonstrate the emergence of richly structured STRFs that capture the structure of natural sounds over a wide range of timescales, and show how the emergent ensembles resemble those commonly reported in physiological studies. Furthermore, we compare ensembles that optimize a sustained firing code with one that optimizes a sparse code, another widely considered coding strategy, and suggest how the resulting population responses are not mutually exclusive. Finally, we demonstrate how the emergent ensembles contour the high-energy spectro-temporal modulations of natural sounds, forming a discriminative representation that captures the full range of modulation statistics that characterize natural sound ensembles. These findings have direct implications for our understanding of how sensory systems encode the informative components of natural stimuli and potentially facilitate multi-sensory integration.

Highlights

  • It is widely believed that sensory representations are optimized to process the stimuli to which they are exposed in natural environments [1]

  • We explore a fundamental question with regard to the representation of sound in the auditory system, namely: what are the coding strategies that underlie observed neurophysiological responses in central auditory areas? There has been debate in recent years as to whether neural ensembles explicitly minimize their propensity to fire or whether neurons exhibit strong, sustained firing rates when processing their preferred stimuli

  • How do the emergent spectro-temporal receptive field (STRF) learned under the sustained firing objective compare to those observed in physiological studies? Broadly speaking, we find that the emergent STRFs share many of the trends with biological receptive fields typically observed in animal models

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Summary

Introduction

It is widely believed that sensory representations are optimized to process the stimuli to which they are exposed in natural environments [1]. A popular hypothesis explored in recent years assumes that neural populations optimize a sparse code. This means that at any given time, only a small subset of a neural population fires to encode a given stimulus [2]. Such a representation is attractive for reasons of coding efficiency (see, e.g., [3]) and conservation of physiological resources [4]. The sparse coding hypothesis has enjoyed particular success in studies of vision (e.g., [5,6]), and has been supported more recently by both neurophysiological [7,8] and computational studies [9,10,11] of the auditory system

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