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Nonlinear transient amplification in recurrent neural networks with short-term plasticity

To rapidly process information, neural circuits have to amplify specific activity patterns transiently. How the brain performs this nonlinear operation remains elusive. Hebbian assemblies are one possibility whereby strong recurrent excitatory connections boost neuronal activity. However, such Hebbi...

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Autores principales: Wu, Yue Kris, Zenke, Friedemann
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8820736/
https://www.ncbi.nlm.nih.gov/pubmed/34895468
http://dx.doi.org/10.7554/eLife.71263
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author Wu, Yue Kris
Zenke, Friedemann
author_facet Wu, Yue Kris
Zenke, Friedemann
author_sort Wu, Yue Kris
collection PubMed
description To rapidly process information, neural circuits have to amplify specific activity patterns transiently. How the brain performs this nonlinear operation remains elusive. Hebbian assemblies are one possibility whereby strong recurrent excitatory connections boost neuronal activity. However, such Hebbian amplification is often associated with dynamical slowing of network dynamics, non-transient attractor states, and pathological run-away activity. Feedback inhibition can alleviate these effects but typically linearizes responses and reduces amplification gain. Here, we study nonlinear transient amplification (NTA), a plausible alternative mechanism that reconciles strong recurrent excitation with rapid amplification while avoiding the above issues. NTA has two distinct temporal phases. Initially, positive feedback excitation selectively amplifies inputs that exceed a critical threshold. Subsequently, short-term plasticity quenches the run-away dynamics into an inhibition-stabilized network state. By characterizing NTA in supralinear network models, we establish that the resulting onset transients are stimulus selective and well-suited for speedy information processing. Further, we find that excitatory-inhibitory co-tuning widens the parameter regime in which NTA is possible in the absence of persistent activity. In summary, NTA provides a parsimonious explanation for how excitatory-inhibitory co-tuning and short-term plasticity collaborate in recurrent networks to achieve transient amplification.
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spelling pubmed-88207362022-02-09 Nonlinear transient amplification in recurrent neural networks with short-term plasticity Wu, Yue Kris Zenke, Friedemann eLife Neuroscience To rapidly process information, neural circuits have to amplify specific activity patterns transiently. How the brain performs this nonlinear operation remains elusive. Hebbian assemblies are one possibility whereby strong recurrent excitatory connections boost neuronal activity. However, such Hebbian amplification is often associated with dynamical slowing of network dynamics, non-transient attractor states, and pathological run-away activity. Feedback inhibition can alleviate these effects but typically linearizes responses and reduces amplification gain. Here, we study nonlinear transient amplification (NTA), a plausible alternative mechanism that reconciles strong recurrent excitation with rapid amplification while avoiding the above issues. NTA has two distinct temporal phases. Initially, positive feedback excitation selectively amplifies inputs that exceed a critical threshold. Subsequently, short-term plasticity quenches the run-away dynamics into an inhibition-stabilized network state. By characterizing NTA in supralinear network models, we establish that the resulting onset transients are stimulus selective and well-suited for speedy information processing. Further, we find that excitatory-inhibitory co-tuning widens the parameter regime in which NTA is possible in the absence of persistent activity. In summary, NTA provides a parsimonious explanation for how excitatory-inhibitory co-tuning and short-term plasticity collaborate in recurrent networks to achieve transient amplification. eLife Sciences Publications, Ltd 2021-12-13 /pmc/articles/PMC8820736/ /pubmed/34895468 http://dx.doi.org/10.7554/eLife.71263 Text en © 2021, Wu and Zenke 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 Neuroscience
Wu, Yue Kris
Zenke, Friedemann
Nonlinear transient amplification in recurrent neural networks with short-term plasticity
title Nonlinear transient amplification in recurrent neural networks with short-term plasticity
title_full Nonlinear transient amplification in recurrent neural networks with short-term plasticity
title_fullStr Nonlinear transient amplification in recurrent neural networks with short-term plasticity
title_full_unstemmed Nonlinear transient amplification in recurrent neural networks with short-term plasticity
title_short Nonlinear transient amplification in recurrent neural networks with short-term plasticity
title_sort nonlinear transient amplification in recurrent neural networks with short-term plasticity
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8820736/
https://www.ncbi.nlm.nih.gov/pubmed/34895468
http://dx.doi.org/10.7554/eLife.71263
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