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Tinnitus-like “hallucinations” elicited by sensory deprivation in an entropy maximization recurrent neural network

Sensory deprivation has long been known to cause hallucinations or “phantom” sensations, the most common of which is tinnitus induced by hearing loss, affecting 10–20% of the population. An observable hearing loss, causing auditory sensory deprivation over a band of frequencies, is present in over 9...

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Detalles Bibliográficos
Autores principales: Dotan, Aviv, Shriki, Oren
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8687580/
https://www.ncbi.nlm.nih.gov/pubmed/34879061
http://dx.doi.org/10.1371/journal.pcbi.1008664
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author Dotan, Aviv
Shriki, Oren
author_facet Dotan, Aviv
Shriki, Oren
author_sort Dotan, Aviv
collection PubMed
description Sensory deprivation has long been known to cause hallucinations or “phantom” sensations, the most common of which is tinnitus induced by hearing loss, affecting 10–20% of the population. An observable hearing loss, causing auditory sensory deprivation over a band of frequencies, is present in over 90% of people with tinnitus. Existing plasticity-based computational models for tinnitus are usually driven by homeostatic mechanisms, modeled to fit phenomenological findings. Here, we use an objective-driven learning algorithm to model an early auditory processing neuronal network, e.g., in the dorsal cochlear nucleus. The learning algorithm maximizes the network’s output entropy by learning the feed-forward and recurrent interactions in the model. We show that the connectivity patterns and responses learned by the model display several hallmarks of early auditory neuronal networks. We further demonstrate that attenuation of peripheral inputs drives the recurrent network towards its critical point and transition into a tinnitus-like state. In this state, the network activity resembles responses to genuine inputs even in the absence of external stimulation, namely, it “hallucinates” auditory responses. These findings demonstrate how objective-driven plasticity mechanisms that normally act to optimize the network’s input representation can also elicit pathologies such as tinnitus as a result of sensory deprivation.
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spelling pubmed-86875802021-12-21 Tinnitus-like “hallucinations” elicited by sensory deprivation in an entropy maximization recurrent neural network Dotan, Aviv Shriki, Oren PLoS Comput Biol Research Article Sensory deprivation has long been known to cause hallucinations or “phantom” sensations, the most common of which is tinnitus induced by hearing loss, affecting 10–20% of the population. An observable hearing loss, causing auditory sensory deprivation over a band of frequencies, is present in over 90% of people with tinnitus. Existing plasticity-based computational models for tinnitus are usually driven by homeostatic mechanisms, modeled to fit phenomenological findings. Here, we use an objective-driven learning algorithm to model an early auditory processing neuronal network, e.g., in the dorsal cochlear nucleus. The learning algorithm maximizes the network’s output entropy by learning the feed-forward and recurrent interactions in the model. We show that the connectivity patterns and responses learned by the model display several hallmarks of early auditory neuronal networks. We further demonstrate that attenuation of peripheral inputs drives the recurrent network towards its critical point and transition into a tinnitus-like state. In this state, the network activity resembles responses to genuine inputs even in the absence of external stimulation, namely, it “hallucinates” auditory responses. These findings demonstrate how objective-driven plasticity mechanisms that normally act to optimize the network’s input representation can also elicit pathologies such as tinnitus as a result of sensory deprivation. Public Library of Science 2021-12-08 /pmc/articles/PMC8687580/ /pubmed/34879061 http://dx.doi.org/10.1371/journal.pcbi.1008664 Text en © 2021 Dotan, Shriki https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Dotan, Aviv
Shriki, Oren
Tinnitus-like “hallucinations” elicited by sensory deprivation in an entropy maximization recurrent neural network
title Tinnitus-like “hallucinations” elicited by sensory deprivation in an entropy maximization recurrent neural network
title_full Tinnitus-like “hallucinations” elicited by sensory deprivation in an entropy maximization recurrent neural network
title_fullStr Tinnitus-like “hallucinations” elicited by sensory deprivation in an entropy maximization recurrent neural network
title_full_unstemmed Tinnitus-like “hallucinations” elicited by sensory deprivation in an entropy maximization recurrent neural network
title_short Tinnitus-like “hallucinations” elicited by sensory deprivation in an entropy maximization recurrent neural network
title_sort tinnitus-like “hallucinations” elicited by sensory deprivation in an entropy maximization recurrent neural network
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8687580/
https://www.ncbi.nlm.nih.gov/pubmed/34879061
http://dx.doi.org/10.1371/journal.pcbi.1008664
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