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Interrogating theoretical models of neural computation with emergent property inference

A cornerstone of theoretical neuroscience is the circuit model: a system of equations that captures a hypothesized neural mechanism. Such models are valuable when they give rise to an experimentally observed phenomenon -- whether behavioral or a pattern of neural activity -- and thus can offer insig...

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Autores principales: Bittner, Sean R, Palmigiano, Agostina, Piet, Alex T, Duan, Chunyu A, Brody, Carlos D, Miller, Kenneth D, Cunningham, John
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8321557/
https://www.ncbi.nlm.nih.gov/pubmed/34323690
http://dx.doi.org/10.7554/eLife.56265
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author Bittner, Sean R
Palmigiano, Agostina
Piet, Alex T
Duan, Chunyu A
Brody, Carlos D
Miller, Kenneth D
Cunningham, John
author_facet Bittner, Sean R
Palmigiano, Agostina
Piet, Alex T
Duan, Chunyu A
Brody, Carlos D
Miller, Kenneth D
Cunningham, John
author_sort Bittner, Sean R
collection PubMed
description A cornerstone of theoretical neuroscience is the circuit model: a system of equations that captures a hypothesized neural mechanism. Such models are valuable when they give rise to an experimentally observed phenomenon -- whether behavioral or a pattern of neural activity -- and thus can offer insights into neural computation. The operation of these circuits, like all models, critically depends on the choice of model parameters. A key step is then to identify the model parameters consistent with observed phenomena: to solve the inverse problem. In this work, we present a novel technique, emergent property inference (EPI), that brings the modern probabilistic modeling toolkit to theoretical neuroscience. When theorizing circuit models, theoreticians predominantly focus on reproducing computational properties rather than a particular dataset. Our method uses deep neural networks to learn parameter distributions with these computational properties. This methodology is introduced through a motivational example of parameter inference in the stomatogastric ganglion. EPI is then shown to allow precise control over the behavior of inferred parameters and to scale in parameter dimension better than alternative techniques. In the remainder of this work, we present novel theoretical findings in models of primary visual cortex and superior colliculus, which were gained through the examination of complex parametric structure captured by EPI. Beyond its scientific contribution, this work illustrates the variety of analyses possible once deep learning is harnessed towards solving theoretical inverse problems.
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spelling pubmed-83215572021-07-30 Interrogating theoretical models of neural computation with emergent property inference Bittner, Sean R Palmigiano, Agostina Piet, Alex T Duan, Chunyu A Brody, Carlos D Miller, Kenneth D Cunningham, John eLife Computational and Systems Biology A cornerstone of theoretical neuroscience is the circuit model: a system of equations that captures a hypothesized neural mechanism. Such models are valuable when they give rise to an experimentally observed phenomenon -- whether behavioral or a pattern of neural activity -- and thus can offer insights into neural computation. The operation of these circuits, like all models, critically depends on the choice of model parameters. A key step is then to identify the model parameters consistent with observed phenomena: to solve the inverse problem. In this work, we present a novel technique, emergent property inference (EPI), that brings the modern probabilistic modeling toolkit to theoretical neuroscience. When theorizing circuit models, theoreticians predominantly focus on reproducing computational properties rather than a particular dataset. Our method uses deep neural networks to learn parameter distributions with these computational properties. This methodology is introduced through a motivational example of parameter inference in the stomatogastric ganglion. EPI is then shown to allow precise control over the behavior of inferred parameters and to scale in parameter dimension better than alternative techniques. In the remainder of this work, we present novel theoretical findings in models of primary visual cortex and superior colliculus, which were gained through the examination of complex parametric structure captured by EPI. Beyond its scientific contribution, this work illustrates the variety of analyses possible once deep learning is harnessed towards solving theoretical inverse problems. eLife Sciences Publications, Ltd 2021-07-29 /pmc/articles/PMC8321557/ /pubmed/34323690 http://dx.doi.org/10.7554/eLife.56265 Text en © 2021, Bittner et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Computational and Systems Biology
Bittner, Sean R
Palmigiano, Agostina
Piet, Alex T
Duan, Chunyu A
Brody, Carlos D
Miller, Kenneth D
Cunningham, John
Interrogating theoretical models of neural computation with emergent property inference
title Interrogating theoretical models of neural computation with emergent property inference
title_full Interrogating theoretical models of neural computation with emergent property inference
title_fullStr Interrogating theoretical models of neural computation with emergent property inference
title_full_unstemmed Interrogating theoretical models of neural computation with emergent property inference
title_short Interrogating theoretical models of neural computation with emergent property inference
title_sort interrogating theoretical models of neural computation with emergent property inference
topic Computational and Systems Biology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8321557/
https://www.ncbi.nlm.nih.gov/pubmed/34323690
http://dx.doi.org/10.7554/eLife.56265
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