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Oscillation-Induced Signal Transmission and Gating in Neural Circuits

Reliable signal transmission constitutes a key requirement for neural circuit function. The propagation of synchronous pulse packets through recurrent circuits is hypothesized to be one robust form of signal transmission and has been extensively studied in computational and theoretical works. Yet, a...

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Autores principales: Jahnke, Sven, Memmesheimer, Raoul-Martin, Timme, Marc
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4263355/
https://www.ncbi.nlm.nih.gov/pubmed/25503492
http://dx.doi.org/10.1371/journal.pcbi.1003940
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author Jahnke, Sven
Memmesheimer, Raoul-Martin
Timme, Marc
author_facet Jahnke, Sven
Memmesheimer, Raoul-Martin
Timme, Marc
author_sort Jahnke, Sven
collection PubMed
description Reliable signal transmission constitutes a key requirement for neural circuit function. The propagation of synchronous pulse packets through recurrent circuits is hypothesized to be one robust form of signal transmission and has been extensively studied in computational and theoretical works. Yet, although external or internally generated oscillations are ubiquitous across neural systems, their influence on such signal propagation is unclear. Here we systematically investigate the impact of oscillations on propagating synchrony. We find that for standard, additive couplings and a net excitatory effect of oscillations, robust propagation of synchrony is enabled in less prominent feed-forward structures than in systems without oscillations. In the presence of non-additive coupling (as mediated by fast dendritic spikes), even balanced oscillatory inputs may enable robust propagation. Here, emerging resonances create complex locking patterns between oscillations and spike synchrony. Interestingly, these resonances make the circuits capable of selecting specific pathways for signal transmission. Oscillations may thus promote reliable transmission and, in co-action with dendritic nonlinearities, provide a mechanism for information processing by selectively gating and routing of signals. Our results are of particular interest for the interpretation of sharp wave/ripple complexes in the hippocampus, where previously learned spike patterns are replayed in conjunction with global high-frequency oscillations. We suggest that the oscillations may serve to stabilize the replay.
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spelling pubmed-42633552014-12-19 Oscillation-Induced Signal Transmission and Gating in Neural Circuits Jahnke, Sven Memmesheimer, Raoul-Martin Timme, Marc PLoS Comput Biol Research Article Reliable signal transmission constitutes a key requirement for neural circuit function. The propagation of synchronous pulse packets through recurrent circuits is hypothesized to be one robust form of signal transmission and has been extensively studied in computational and theoretical works. Yet, although external or internally generated oscillations are ubiquitous across neural systems, their influence on such signal propagation is unclear. Here we systematically investigate the impact of oscillations on propagating synchrony. We find that for standard, additive couplings and a net excitatory effect of oscillations, robust propagation of synchrony is enabled in less prominent feed-forward structures than in systems without oscillations. In the presence of non-additive coupling (as mediated by fast dendritic spikes), even balanced oscillatory inputs may enable robust propagation. Here, emerging resonances create complex locking patterns between oscillations and spike synchrony. Interestingly, these resonances make the circuits capable of selecting specific pathways for signal transmission. Oscillations may thus promote reliable transmission and, in co-action with dendritic nonlinearities, provide a mechanism for information processing by selectively gating and routing of signals. Our results are of particular interest for the interpretation of sharp wave/ripple complexes in the hippocampus, where previously learned spike patterns are replayed in conjunction with global high-frequency oscillations. We suggest that the oscillations may serve to stabilize the replay. Public Library of Science 2014-12-11 /pmc/articles/PMC4263355/ /pubmed/25503492 http://dx.doi.org/10.1371/journal.pcbi.1003940 Text en © 2014 Jahnke et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Jahnke, Sven
Memmesheimer, Raoul-Martin
Timme, Marc
Oscillation-Induced Signal Transmission and Gating in Neural Circuits
title Oscillation-Induced Signal Transmission and Gating in Neural Circuits
title_full Oscillation-Induced Signal Transmission and Gating in Neural Circuits
title_fullStr Oscillation-Induced Signal Transmission and Gating in Neural Circuits
title_full_unstemmed Oscillation-Induced Signal Transmission and Gating in Neural Circuits
title_short Oscillation-Induced Signal Transmission and Gating in Neural Circuits
title_sort oscillation-induced signal transmission and gating in neural circuits
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4263355/
https://www.ncbi.nlm.nih.gov/pubmed/25503492
http://dx.doi.org/10.1371/journal.pcbi.1003940
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