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Homogeneous Intrinsic Neuronal Excitability Induces Overfitting to Sensory Noise: A Robot Model of Neurodevelopmental Disorder

Neurodevelopmental disorders, including autism spectrum disorder, have been intensively investigated at the neural, cognitive, and behavioral levels, but the accumulated knowledge remains fragmented. In particular, developmental learning aspects of symptoms and interactions with the physical environ...

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Autores principales: Idei, Hayato, Murata, Shingo, Yamashita, Yuichi, Ogata, Tetsuya
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7434834/
https://www.ncbi.nlm.nih.gov/pubmed/32903328
http://dx.doi.org/10.3389/fpsyt.2020.00762
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author Idei, Hayato
Murata, Shingo
Yamashita, Yuichi
Ogata, Tetsuya
author_facet Idei, Hayato
Murata, Shingo
Yamashita, Yuichi
Ogata, Tetsuya
author_sort Idei, Hayato
collection PubMed
description Neurodevelopmental disorders, including autism spectrum disorder, have been intensively investigated at the neural, cognitive, and behavioral levels, but the accumulated knowledge remains fragmented. In particular, developmental learning aspects of symptoms and interactions with the physical environment remain largely unexplored in computational modeling studies, although a leading computational theory has posited associations between psychiatric symptoms and an unusual estimation of information uncertainty (precision), which is an essential aspect of the real world and is estimated through learning processes. Here, we propose a mechanistic explanation that unifies the disparate observations via a hierarchical predictive coding and developmental learning framework, which is demonstrated in experiments using a neural network-controlled robot. The results show that, through the developmental learning process, homogeneous intrinsic neuronal excitability at the neural level induced via self-organization changes at the information processing level, such as hyper sensory precision and overfitting to sensory noise. These changes led to multifaceted alterations at the behavioral level, such as inflexibility, reduced generalization, and motor clumsiness. In addition, these behavioral alterations were accompanied by fluctuating neural activity and excessive development of synaptic connections. These findings might bridge various levels of understandings in autism spectrum and other neurodevelopmental disorders and provide insights into the disease processes underlying observed behaviors and brain activities in individual patients. This study shows the potential of neurorobotics frameworks for modeling how psychiatric disorders arise from dynamic interactions among the brain, body, and uncertain environments.
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spelling pubmed-74348342020-09-03 Homogeneous Intrinsic Neuronal Excitability Induces Overfitting to Sensory Noise: A Robot Model of Neurodevelopmental Disorder Idei, Hayato Murata, Shingo Yamashita, Yuichi Ogata, Tetsuya Front Psychiatry Psychiatry Neurodevelopmental disorders, including autism spectrum disorder, have been intensively investigated at the neural, cognitive, and behavioral levels, but the accumulated knowledge remains fragmented. In particular, developmental learning aspects of symptoms and interactions with the physical environment remain largely unexplored in computational modeling studies, although a leading computational theory has posited associations between psychiatric symptoms and an unusual estimation of information uncertainty (precision), which is an essential aspect of the real world and is estimated through learning processes. Here, we propose a mechanistic explanation that unifies the disparate observations via a hierarchical predictive coding and developmental learning framework, which is demonstrated in experiments using a neural network-controlled robot. The results show that, through the developmental learning process, homogeneous intrinsic neuronal excitability at the neural level induced via self-organization changes at the information processing level, such as hyper sensory precision and overfitting to sensory noise. These changes led to multifaceted alterations at the behavioral level, such as inflexibility, reduced generalization, and motor clumsiness. In addition, these behavioral alterations were accompanied by fluctuating neural activity and excessive development of synaptic connections. These findings might bridge various levels of understandings in autism spectrum and other neurodevelopmental disorders and provide insights into the disease processes underlying observed behaviors and brain activities in individual patients. This study shows the potential of neurorobotics frameworks for modeling how psychiatric disorders arise from dynamic interactions among the brain, body, and uncertain environments. Frontiers Media S.A. 2020-08-12 /pmc/articles/PMC7434834/ /pubmed/32903328 http://dx.doi.org/10.3389/fpsyt.2020.00762 Text en Copyright © 2020 Idei, Murata, Yamashita and Ogata http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Psychiatry
Idei, Hayato
Murata, Shingo
Yamashita, Yuichi
Ogata, Tetsuya
Homogeneous Intrinsic Neuronal Excitability Induces Overfitting to Sensory Noise: A Robot Model of Neurodevelopmental Disorder
title Homogeneous Intrinsic Neuronal Excitability Induces Overfitting to Sensory Noise: A Robot Model of Neurodevelopmental Disorder
title_full Homogeneous Intrinsic Neuronal Excitability Induces Overfitting to Sensory Noise: A Robot Model of Neurodevelopmental Disorder
title_fullStr Homogeneous Intrinsic Neuronal Excitability Induces Overfitting to Sensory Noise: A Robot Model of Neurodevelopmental Disorder
title_full_unstemmed Homogeneous Intrinsic Neuronal Excitability Induces Overfitting to Sensory Noise: A Robot Model of Neurodevelopmental Disorder
title_short Homogeneous Intrinsic Neuronal Excitability Induces Overfitting to Sensory Noise: A Robot Model of Neurodevelopmental Disorder
title_sort homogeneous intrinsic neuronal excitability induces overfitting to sensory noise: a robot model of neurodevelopmental disorder
topic Psychiatry
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7434834/
https://www.ncbi.nlm.nih.gov/pubmed/32903328
http://dx.doi.org/10.3389/fpsyt.2020.00762
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