Sparse Representation of Sounds in the Unanesthetized Auditory Cortex

TLDR

Neuronal populations in the auditory cortex encode acoustic stimuli, but while anesthetized responses are mainly transient, unanesthetized recordings reveal subpopulations with distinct response properties. The study seeks to quantify how these subpopulations contribute to sound representation in awake rats. Using cell‑attached recordings that isolate single units independent of activity, the authors measured the fraction of neurons activated by tones, frequency‑modulated sweeps, white‑noise bursts, and natural sounds in the primary auditory cortex of head‑fixed awake rats. The population response is sparse, with less than 5 % of neurons firing at any instant, high firing rates exceeding 20 spikes s⁻¹ in active cells, a lognormal distribution of activity rather than exponential, and these results provide the first quantitative evidence that most neurons remain silent most of the time while sound representations are formed by small dynamic subsets of highly active neurons.

Abstract

How do neuronal populations in the auditory cortex represent acoustic stimuli? Although sound-evoked neural responses in the anesthetized auditory cortex are mainly transient, recent experiments in the unanesthetized preparation have emphasized subpopulations with other response properties. To quantify the relative contributions of these different subpopulations in the awake preparation, we have estimated the representation of sounds across the neuronal population using a representative ensemble of stimuli. We used cell-attached recording with a glass electrode, a method for which single-unit isolation does not depend on neuronal activity, to quantify the fraction of neurons engaged by acoustic stimuli (tones, frequency modulated sweeps, white-noise bursts, and natural stimuli) in the primary auditory cortex of awake head-fixed rats. We find that the population response is sparse, with stimuli typically eliciting high firing rates (>20 spikes/second) in less than 5% of neurons at any instant. Some neurons had very low spontaneous firing rates (<0.01 spikes/second). At the other extreme, some neurons had driven rates in excess of 50 spikes/second. Interestingly, the overall population response was well described by a lognormal distribution, rather than the exponential distribution that is often reported. Our results represent, to our knowledge, the first quantitative evidence for sparse representations of sounds in the unanesthetized auditory cortex. Our results are compatible with a model in which most neurons are silent much of the time, and in which representations are composed of small dynamic subsets of highly active neurons.