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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...
Autores principales: | , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
eLife Sciences Publications, Ltd
2021
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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. |
format | Online Article Text |
id | pubmed-8820736 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | eLife Sciences Publications, Ltd |
record_format | MEDLINE/PubMed |
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 |
work_keys_str_mv | AT wuyuekris nonlineartransientamplificationinrecurrentneuralnetworkswithshorttermplasticity AT zenkefriedemann nonlineartransientamplificationinrecurrentneuralnetworkswithshorttermplasticity |