Abstract

Sensory organs transmit information to downstream brain circuits using a neural code comprised of spikes from multiple neurons. According to the prominent efficient coding framework, the properties of sensory populations have evolved to encode maximum information about stimuli given biophysical constraints. How information coding depends on the way sensory signals from multiple channels converge downstream is still unknown, especially in the presence of noise which corrupts the signal at different points along the pathway. Here, we calculated the optimal information transfer of a population of nonlinear neurons under two scenarios. First, a lumped-coding channel where the information from different inputs converges to a single channel, thus reducing the number of neurons. Second, an independent-coding channel when different inputs contribute independent information without convergence. In each case, we investigated information loss when the sensory signal was corrupted by two sources of noise. We determined critical noise levels at which the optimal number of distinct thresholds of individual neurons in the population changes. Comparing our system to classical physical systems, these changes correspond to first- or second-order phase transitions for the lumped- or the independent-coding channel, respectively. We relate our theoretical predictions to coding in a population of auditory nerve fibers recorded experimentally, and find signatures of efficient coding. Our results yield important insights into the diverse coding strategies used by neural populations to optimally integrate sensory stimuli in the presence of distinct sources of noise.

Highlights

  • Neurons in sensory organs encode information about the environment and transmit it to downstream circuits in the brain

  • We considered different stimulus distributions, parametrized by the generalized normal distribution [41], but here we primarily discuss the case of a Gaussian stimulus distribution

  • Such a mapping can be implemented by a variety of sensory systems, for instance, the retina which processes various visual stimulus attributes, such as light intensity or contrast [42], the olfactory receptor neurons which process a range of concentrations of a single odor [9, 39, 43, 44], or the auditory nerve fibers (ANFs) which transmit information about sound pressure levels [45]

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Summary

Introduction

Neurons in sensory organs encode information about the environment and transmit it to downstream circuits in the brain. There are RGC types which in parallel encode a single stimulus feature differing in their firing thresholds [4,5,6], and provide parallel information streams Another example is the first synapse level of the auditory pathway, where each inner hair cell transmits information about sound intensity to approximately ten to thirty different auditory nerve fibers (ANFs) [7]. This results in a highly parallelized stream of sensory information This parallel encoding of a single stimulus feature with a population of neurons with different thresholds has been shown in olfactory receptor neurons [9], in mammalian touch receptors [10], and electro receptors of electric fish [11]

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