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Constructing the hierarchy of predictive auditory sequences in the marmoset brain

Our brains constantly generate predictions of sensory input that are compared with actual inputs, propagate the prediction-errors through a hierarchy of brain regions, and subsequently update the internal predictions of the world. However, the essential feature of predictive coding, the notion of hi...

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Autores principales: Jiang, Yuwei, Komatsu, Misako, Chen, Yuyan, Xie, Ruoying, Zhang, Kaiwei, Xia, Ying, Gui, Peng, Liang, Zhifeng, Wang, Liping
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8893719/
https://www.ncbi.nlm.nih.gov/pubmed/35174784
http://dx.doi.org/10.7554/eLife.74653
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author Jiang, Yuwei
Komatsu, Misako
Chen, Yuyan
Xie, Ruoying
Zhang, Kaiwei
Xia, Ying
Gui, Peng
Liang, Zhifeng
Wang, Liping
author_facet Jiang, Yuwei
Komatsu, Misako
Chen, Yuyan
Xie, Ruoying
Zhang, Kaiwei
Xia, Ying
Gui, Peng
Liang, Zhifeng
Wang, Liping
author_sort Jiang, Yuwei
collection PubMed
description Our brains constantly generate predictions of sensory input that are compared with actual inputs, propagate the prediction-errors through a hierarchy of brain regions, and subsequently update the internal predictions of the world. However, the essential feature of predictive coding, the notion of hierarchical depth and its neural mechanisms, remains largely unexplored. Here, we investigated the hierarchical depth of predictive auditory processing by combining functional magnetic resonance imaging (fMRI) and high-density whole-brain electrocorticography (ECoG) in marmoset monkeys during an auditory local-global paradigm in which the temporal regularities of the stimuli were designed at two hierarchical levels. The prediction-errors and prediction updates were examined as neural responses to auditory mismatches and omissions. Using fMRI, we identified a hierarchical gradient along the auditory pathway: midbrain and sensory regions represented local, shorter-time-scale predictive processing followed by associative auditory regions, whereas anterior temporal and prefrontal areas represented global, longer-time-scale sequence processing. The complementary ECoG recordings confirmed the activations at cortical surface areas and further differentiated the signals of prediction-error and update, which were transmitted via putative bottom-up γ and top-down β oscillations, respectively. Furthermore, omission responses caused by absence of input, reflecting solely the two levels of prediction signals that are unique to the hierarchical predictive coding framework, demonstrated the hierarchical top-down process of predictions in the auditory, temporal, and prefrontal areas. Thus, our findings support the hierarchical predictive coding framework, and outline how neural networks and spatiotemporal dynamics are used to represent and arrange a hierarchical structure of auditory sequences in the marmoset brain.
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spelling pubmed-88937192022-03-04 Constructing the hierarchy of predictive auditory sequences in the marmoset brain Jiang, Yuwei Komatsu, Misako Chen, Yuyan Xie, Ruoying Zhang, Kaiwei Xia, Ying Gui, Peng Liang, Zhifeng Wang, Liping eLife Neuroscience Our brains constantly generate predictions of sensory input that are compared with actual inputs, propagate the prediction-errors through a hierarchy of brain regions, and subsequently update the internal predictions of the world. However, the essential feature of predictive coding, the notion of hierarchical depth and its neural mechanisms, remains largely unexplored. Here, we investigated the hierarchical depth of predictive auditory processing by combining functional magnetic resonance imaging (fMRI) and high-density whole-brain electrocorticography (ECoG) in marmoset monkeys during an auditory local-global paradigm in which the temporal regularities of the stimuli were designed at two hierarchical levels. The prediction-errors and prediction updates were examined as neural responses to auditory mismatches and omissions. Using fMRI, we identified a hierarchical gradient along the auditory pathway: midbrain and sensory regions represented local, shorter-time-scale predictive processing followed by associative auditory regions, whereas anterior temporal and prefrontal areas represented global, longer-time-scale sequence processing. The complementary ECoG recordings confirmed the activations at cortical surface areas and further differentiated the signals of prediction-error and update, which were transmitted via putative bottom-up γ and top-down β oscillations, respectively. Furthermore, omission responses caused by absence of input, reflecting solely the two levels of prediction signals that are unique to the hierarchical predictive coding framework, demonstrated the hierarchical top-down process of predictions in the auditory, temporal, and prefrontal areas. Thus, our findings support the hierarchical predictive coding framework, and outline how neural networks and spatiotemporal dynamics are used to represent and arrange a hierarchical structure of auditory sequences in the marmoset brain. eLife Sciences Publications, Ltd 2022-02-17 /pmc/articles/PMC8893719/ /pubmed/35174784 http://dx.doi.org/10.7554/eLife.74653 Text en © 2022, Jiang et al 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
Jiang, Yuwei
Komatsu, Misako
Chen, Yuyan
Xie, Ruoying
Zhang, Kaiwei
Xia, Ying
Gui, Peng
Liang, Zhifeng
Wang, Liping
Constructing the hierarchy of predictive auditory sequences in the marmoset brain
title Constructing the hierarchy of predictive auditory sequences in the marmoset brain
title_full Constructing the hierarchy of predictive auditory sequences in the marmoset brain
title_fullStr Constructing the hierarchy of predictive auditory sequences in the marmoset brain
title_full_unstemmed Constructing the hierarchy of predictive auditory sequences in the marmoset brain
title_short Constructing the hierarchy of predictive auditory sequences in the marmoset brain
title_sort constructing the hierarchy of predictive auditory sequences in the marmoset brain
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8893719/
https://www.ncbi.nlm.nih.gov/pubmed/35174784
http://dx.doi.org/10.7554/eLife.74653
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