Abstract

Neurons in sensory systems often pool inputs over arrays of presynaptic cells, giving rise to functional subunits inside a neuron’s receptive field. The organization of these subunits provides a signature of the neuron’s presynaptic functional connectivity and determines how the neuron integrates sensory stimuli. Here we introduce the method of spike-triggered non-negative matrix factorization for detecting the layout of subunits within a neuron’s receptive field. The method only requires the neuron’s spiking responses under finely structured sensory stimulation and is therefore applicable to large populations of simultaneously recorded neurons. Applied to recordings from ganglion cells in the salamander retina, the method retrieves the receptive fields of presynaptic bipolar cells, as verified by simultaneous bipolar and ganglion cell recordings. The identified subunit layouts allow improved predictions of ganglion cell responses to natural stimuli and reveal shared bipolar cell input into distinct types of ganglion cells.

Highlights

  • Neurons in sensory systems often pool inputs over arrays of presynaptic cells, giving rise to functional subunits inside a neuron’s receptive field

  • We developed spike-triggered non-negative matrix factorization (STNMF) as a method for extracting the receptive field substructure that results from nonlinear pooling of functionally relevant inputs

  • negative matrix factorization (NMF) is a computational technique that is typically used to seek a decomposition of high-dimensional data into a relatively small set of modules and corresponding weights so that the individual samples in the data set are approximated by weighted combinations of the modules

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Summary

Introduction

Neurons in sensory systems often pool inputs over arrays of presynaptic cells, giving rise to functional subunits inside a neuron’s receptive field. A computational framework for analyzing the relation between functional connectivity and stimulus encoding is given by models that structure a neuron’s receptive field into subunits, corresponding to the functionally relevant input channels Such subunit models form the basis of our current understanding of, for example, retinal ganglion cell sensitivity to high spatial frequencies[1, 2], ganglion cell selectivity for specific types of motion signals[3,4,5,6], the emergence of orientation selectivity and phase invariance in primary visual cortex[7,8,9,10,11,12,13], and the processing of visual motion information along the cortical dorsal stream[14,15,16]. Output gain receptive fields of presynaptic bipolar cells, providing a novel perspective on the functional connectivity and signal transmission between these successive neuronal layers

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