Abstract

One general principle of sensory information processing is that the brain must optimize efficiency by reducing the number of neurons that process the same information. The sparseness of the sensory representations in a population of neurons reflects the efficiency of the neural code. Here, we employ large-scale two-photon calcium imaging to examine the responses of a large population of neurons within the superficial layers of area V1 with single-cell resolution, while simultaneously presenting a large set of natural visual stimuli, to provide the first direct measure of the population sparseness in awake primates. The results show that only 0.5% of neurons respond strongly to any given natural image - indicating a ten-fold increase in the inferred sparseness over previous measurements. These population activities are nevertheless necessary and sufficient to discriminate visual stimuli with high accuracy, suggesting that the neural code in the primary visual cortex is both super-sparse and highly efficient.

Highlights

  • The efficient-coding hypothesis is an important organizing principle of any sensory system (Barlow, 1981; Olshausen and Field, 1996). It predicts that neuronal population responses should be sparse, the optimal level of sparseness depends on many factors

  • Most of the experimental evidence of sparse coding comes from the responses of individual neurons that were exposed to a large set of natural image stimuli, measured using single-unit recording techniques (Haider et al, 2010; Hromadka et al, 2008; Rust and DiCarlo, 2012; Vinje and Gallant, 2000)

  • Each monkey performed a fixation task while stimuli were presented to the appropriate retinotopic position in the visual field

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Summary

Introduction

The efficient-coding hypothesis is an important organizing principle of any sensory system (Barlow, 1981; Olshausen and Field, 1996) It predicts that neuronal population responses should be sparse, the optimal level of sparseness depends on many factors. The first direct measurement of population response sparseness was performed with two-photon (2P) GCaMP6 signal imaging in rodents (Froudarakis et al, 2014). We showed previously that GCaMP5 exhibits linear non-saturating responses across a wide range of firing rates (10–150 Hz) (Li et al, 2017), allowing us to measure accurately the response sparseness of almost all of the neurons in layer two in V1 within a 850 mm x 850 mm field of view—the spatial scale of about one hypercolumn

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Materials and methods
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