Inferring nonlinear neuronal computation based on physiologically plausible inputs.

The computation represented by a sensory neuron's response to stimuli is constructed from an array of physiological processes both belonging to that neuron and inherited from its inputs. Although many of these physiological processes are known to be nonlinear, linear approximations are commonly...

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Main Authors: James M McFarland, Yuwei Cui, Daniel A Butts
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2013-01-01
Series:PLoS Computational Biology
Online Access:http://europepmc.org/articles/PMC3715434?pdf=render
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spelling doaj-a43a7255d5de4c46a7e4935dd275b5f62020-11-25T01:37:14ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582013-01-0197e100314310.1371/journal.pcbi.1003143Inferring nonlinear neuronal computation based on physiologically plausible inputs.James M McFarlandYuwei CuiDaniel A ButtsThe computation represented by a sensory neuron's response to stimuli is constructed from an array of physiological processes both belonging to that neuron and inherited from its inputs. Although many of these physiological processes are known to be nonlinear, linear approximations are commonly used to describe the stimulus selectivity of sensory neurons (i.e., linear receptive fields). Here we present an approach for modeling sensory processing, termed the Nonlinear Input Model (NIM), which is based on the hypothesis that the dominant nonlinearities imposed by physiological mechanisms arise from rectification of a neuron's inputs. Incorporating such 'upstream nonlinearities' within the standard linear-nonlinear (LN) cascade modeling structure implicitly allows for the identification of multiple stimulus features driving a neuron's response, which become directly interpretable as either excitatory or inhibitory. Because its form is analogous to an integrate-and-fire neuron receiving excitatory and inhibitory inputs, model fitting can be guided by prior knowledge about the inputs to a given neuron, and elements of the resulting model can often result in specific physiological predictions. Furthermore, by providing an explicit probabilistic model with a relatively simple nonlinear structure, its parameters can be efficiently optimized and appropriately regularized. Parameter estimation is robust and efficient even with large numbers of model components and in the context of high-dimensional stimuli with complex statistical structure (e.g. natural stimuli). We describe detailed methods for estimating the model parameters, and illustrate the advantages of the NIM using a range of example sensory neurons in the visual and auditory systems. We thus present a modeling framework that can capture a broad range of nonlinear response functions while providing physiologically interpretable descriptions of neural computation.http://europepmc.org/articles/PMC3715434?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author James M McFarland
Yuwei Cui
Daniel A Butts
spellingShingle James M McFarland
Yuwei Cui
Daniel A Butts
Inferring nonlinear neuronal computation based on physiologically plausible inputs.
PLoS Computational Biology
author_facet James M McFarland
Yuwei Cui
Daniel A Butts
author_sort James M McFarland
title Inferring nonlinear neuronal computation based on physiologically plausible inputs.
title_short Inferring nonlinear neuronal computation based on physiologically plausible inputs.
title_full Inferring nonlinear neuronal computation based on physiologically plausible inputs.
title_fullStr Inferring nonlinear neuronal computation based on physiologically plausible inputs.
title_full_unstemmed Inferring nonlinear neuronal computation based on physiologically plausible inputs.
title_sort inferring nonlinear neuronal computation based on physiologically plausible inputs.
publisher Public Library of Science (PLoS)
series PLoS Computational Biology
issn 1553-734X
1553-7358
publishDate 2013-01-01
description The computation represented by a sensory neuron's response to stimuli is constructed from an array of physiological processes both belonging to that neuron and inherited from its inputs. Although many of these physiological processes are known to be nonlinear, linear approximations are commonly used to describe the stimulus selectivity of sensory neurons (i.e., linear receptive fields). Here we present an approach for modeling sensory processing, termed the Nonlinear Input Model (NIM), which is based on the hypothesis that the dominant nonlinearities imposed by physiological mechanisms arise from rectification of a neuron's inputs. Incorporating such 'upstream nonlinearities' within the standard linear-nonlinear (LN) cascade modeling structure implicitly allows for the identification of multiple stimulus features driving a neuron's response, which become directly interpretable as either excitatory or inhibitory. Because its form is analogous to an integrate-and-fire neuron receiving excitatory and inhibitory inputs, model fitting can be guided by prior knowledge about the inputs to a given neuron, and elements of the resulting model can often result in specific physiological predictions. Furthermore, by providing an explicit probabilistic model with a relatively simple nonlinear structure, its parameters can be efficiently optimized and appropriately regularized. Parameter estimation is robust and efficient even with large numbers of model components and in the context of high-dimensional stimuli with complex statistical structure (e.g. natural stimuli). We describe detailed methods for estimating the model parameters, and illustrate the advantages of the NIM using a range of example sensory neurons in the visual and auditory systems. We thus present a modeling framework that can capture a broad range of nonlinear response functions while providing physiologically interpretable descriptions of neural computation.
url http://europepmc.org/articles/PMC3715434?pdf=render
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AT danielabutts inferringnonlinearneuronalcomputationbasedonphysiologicallyplausibleinputs
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