Layer-specific activation in human primary somatosensory cortex during tactile temporal prediction error processing
The human brain continuously generates predictions of incoming sensory input and calculates corresponding prediction errors from the perceived inputs to update internal predictions. In human primary somatosensory cortex (area 3b), different cortical layers are involved in receiving the sensory input...
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| Vydané v: | NeuroImage (Orlando, Fla.) Ročník 248; s. 118867 |
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| Hlavní autori: | , , , , , , , , , , , , |
| Médium: | Journal Article |
| Jazyk: | English |
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United States
Elsevier Inc
01.03.2022
Elsevier Limited Elsevier |
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| ISSN: | 1053-8119, 1095-9572, 1095-9572 |
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| Abstract | The human brain continuously generates predictions of incoming sensory input and calculates corresponding prediction errors from the perceived inputs to update internal predictions. In human primary somatosensory cortex (area 3b), different cortical layers are involved in receiving the sensory input and generation of error signals. It remains unknown, however, how the layers in the human area 3b contribute to the temporal prediction error processing. To investigate prediction error representation in the area 3b across layers, we acquired layer-specific functional magnetic resonance imaging (fMRI) data at 7T from human area 3b during a task of index finger poking with no-delay, short-delay and long-delay touching sequences. We demonstrate that all three tasks increased activity in both superficial and deep layers of area 3b compared to the random sensory input. The fMRI signal was differentially modulated solely in the deep layers rather than the superficial layers of area 3b by the delay time. Compared with the no-delay stimuli, activity was greater in the deep layers of area 3b during the short-delay stimuli but lower during the long-delay stimuli. This difference activity features in the superficial and deep layers suggest distinct functional contributions of area 3b layers to tactile temporal prediction error processing. The functional segregation in area 3b across layers may reflect that the excitatory and inhibitory interplay in the sensory cortex contributions to flexible communication between cortical layers or between cortical areas.
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| AbstractList | The human brain continuously generates predictions of incoming sensory input and calculates corresponding prediction errors from the perceived inputs to update internal predictions. In human primary somatosensory cortex (area 3b), different cortical layers are involved in receiving the sensory input and generation of error signals. It remains unknown, however, how the layers in the human area 3b contribute to the temporal prediction error processing. To investigate prediction error representation in the area 3b across layers, we acquired layer-specific functional magnetic resonance imaging (fMRI) data at 7T from human area 3b during a task of index finger poking with no-delay, short-delay and long-delay touching sequences. We demonstrate that all three tasks increased activity in both superficial and deep layers of area 3b compared to the random sensory input. The fMRI signal was differentially modulated solely in the deep layers rather than the superficial layers of area 3b by the delay time. Compared with the no-delay stimuli, activity was greater in the deep layers of area 3b during the short-delay stimuli but lower during the long-delay stimuli. This difference activity features in the superficial and deep layers suggest distinct functional contributions of area 3b layers to tactile temporal prediction error processing. The functional segregation in area 3b across layers may reflect that the excitatory and inhibitory interplay in the sensory cortex contributions to flexible communication between cortical layers or between cortical areas. The human brain continuously generates predictions of incoming sensory input and calculates corresponding prediction errors from the perceived inputs to update internal predictions. In human primary somatosensory cortex (area 3b), different cortical layers are involved in receiving the sensory input and generation of error signals. It remains unknown, however, how the layers in the human area 3b contribute to the temporal prediction error processing. To investigate prediction error representation in the area 3b across layers, we acquired layer-specific functional magnetic resonance imaging (fMRI) data at 7T from human area 3b during a task of index finger poking with no-delay, short-delay and long-delay touching sequences. We demonstrate that all three tasks increased activity in both superficial and deep layers of area 3b compared to the random sensory input. The fMRI signal was differentially modulated solely in the deep layers rather than the superficial layers of area 3b by the delay time. Compared with the no-delay stimuli, activity was greater in the deep layers of area 3b during the short-delay stimuli but lower during the long-delay stimuli. This difference activity features in the superficial and deep layers suggest distinct functional contributions of area 3b layers to tactile temporal prediction error processing. The functional segregation in area 3b across layers may reflect that the excitatory and inhibitory interplay in the sensory cortex contributions to flexible communication between cortical layers or between cortical areas. [Display omitted] The human brain continuously generates predictions of incoming sensory input and calculates corresponding prediction errors from the perceived inputs to update internal predictions. In human primary somatosensory cortex (area 3b), different cortical layers are involved in receiving the sensory input and generation of error signals. It remains unknown, however, how the layers in the human area 3b contribute to the temporal prediction error processing. To investigate prediction error representation in the area 3b across layers, we acquired layer-specific functional magnetic resonance imaging (fMRI) data at 7T from human area 3b during a task of index finger poking with no-delay, short-delay and long-delay touching sequences. We demonstrate that all three tasks increased activity in both superficial and deep layers of area 3b compared to the random sensory input. The fMRI signal was differentially modulated solely in the deep layers rather than the superficial layers of area 3b by the delay time. Compared with the no-delay stimuli, activity was greater in the deep layers of area 3b during the short-delay stimuli but lower during the long-delay stimuli. This difference activity features in the superficial and deep layers suggest distinct functional contributions of area 3b layers to tactile temporal prediction error processing. The functional segregation in area 3b across layers may reflect that the excitatory and inhibitory interplay in the sensory cortex contributions to flexible communication between cortical layers or between cortical areas.The human brain continuously generates predictions of incoming sensory input and calculates corresponding prediction errors from the perceived inputs to update internal predictions. In human primary somatosensory cortex (area 3b), different cortical layers are involved in receiving the sensory input and generation of error signals. It remains unknown, however, how the layers in the human area 3b contribute to the temporal prediction error processing. To investigate prediction error representation in the area 3b across layers, we acquired layer-specific functional magnetic resonance imaging (fMRI) data at 7T from human area 3b during a task of index finger poking with no-delay, short-delay and long-delay touching sequences. We demonstrate that all three tasks increased activity in both superficial and deep layers of area 3b compared to the random sensory input. The fMRI signal was differentially modulated solely in the deep layers rather than the superficial layers of area 3b by the delay time. Compared with the no-delay stimuli, activity was greater in the deep layers of area 3b during the short-delay stimuli but lower during the long-delay stimuli. This difference activity features in the superficial and deep layers suggest distinct functional contributions of area 3b layers to tactile temporal prediction error processing. The functional segregation in area 3b across layers may reflect that the excitatory and inhibitory interplay in the sensory cortex contributions to flexible communication between cortical layers or between cortical areas. |
| ArticleNumber | 118867 |
| Author | Jangraw, David C. Bandettini, Peter A. Yu, Yinghua Sadato, Norihiro Wu, Jinglong Yang, Jiajia Handwerker, Daniel A. Molfese, Peter J. Ejima, Yoshimichi Huber, Laurentius Chen, Gang Fukunaga, Masaki Chai, Yuhui |
| AuthorAffiliation | 1. Graduate School of Interdisciplinary Science and Engineering in Health Systems, Okayama University, 3-1-1 Tsushima-Naka, Kita-ku, Okayama 700-8530, Japan 5. Scientific and Statistical Computational Core, National Institute of Mental Health, Building 10, 10 Center Dr Bethesda, MD 20892, USA 3. MR-Methods Group, MBIC, Cognitive Neuroscience Department, Faculty of Psychology and Neuroscience, University of Maastricht, Cognitive Neuroscience, Room 1.014, Oxfordlaan 55, 6229 EV Maastricht, The Netherlands 4. Division of Cerebral Research, National Institute for Physiological Sciences, 38 Nishigonaka, Myodaiji, Okazaki, Aichi, 444-8585 Japan 6. Beijing Institute of Technology, 5 South Zhongguancun Street, Hiadian District, Beijing 100081, China 7. Functional MRI Core Facility, National Institute of Mental Health, Building 10, 10 Center Dr Bethesda, MD 20892, USA 2. Section on Functional Imaging Methods, National Institute of Mental Health, Building 10, 10 Center Dr Bethesda, MD 20892, USA |
| AuthorAffiliation_xml | – name: 1. Graduate School of Interdisciplinary Science and Engineering in Health Systems, Okayama University, 3-1-1 Tsushima-Naka, Kita-ku, Okayama 700-8530, Japan – name: 5. Scientific and Statistical Computational Core, National Institute of Mental Health, Building 10, 10 Center Dr Bethesda, MD 20892, USA – name: 4. Division of Cerebral Research, National Institute for Physiological Sciences, 38 Nishigonaka, Myodaiji, Okazaki, Aichi, 444-8585 Japan – name: 6. Beijing Institute of Technology, 5 South Zhongguancun Street, Hiadian District, Beijing 100081, China – name: 3. MR-Methods Group, MBIC, Cognitive Neuroscience Department, Faculty of Psychology and Neuroscience, University of Maastricht, Cognitive Neuroscience, Room 1.014, Oxfordlaan 55, 6229 EV Maastricht, The Netherlands – name: 2. Section on Functional Imaging Methods, National Institute of Mental Health, Building 10, 10 Center Dr Bethesda, MD 20892, USA – name: 7. Functional MRI Core Facility, National Institute of Mental Health, Building 10, 10 Center Dr Bethesda, MD 20892, USA |
| Author_xml | – sequence: 1 givenname: Yinghua surname: Yu fullname: Yu, Yinghua email: yinghua.yyh@gmail.com organization: Graduate School of Interdisciplinary Science and Engineering in Health Systems, Okayama University, 3-1-1 Tsushima-Naka, Kita-ku, Okayama 700-8530, Japan – sequence: 2 givenname: Laurentius surname: Huber fullname: Huber, Laurentius organization: MR-Methods Group, MBIC, Cognitive Neuroscience Department, Faculty of Psychology and Neuroscience, University of Maastricht, Cognitive Neuroscience, Room 1.014, Oxfordlaan 55, 6229 EV Maastricht, The Netherlands – sequence: 3 givenname: Jiajia surname: Yang fullname: Yang, Jiajia organization: Graduate School of Interdisciplinary Science and Engineering in Health Systems, Okayama University, 3-1-1 Tsushima-Naka, Kita-ku, Okayama 700-8530, Japan – sequence: 4 givenname: Masaki surname: Fukunaga fullname: Fukunaga, Masaki organization: Division of Cerebral Research, National Institute for Physiological Sciences, 38 Nishigonaka, Myodaiji, Okazaki, Aichi, 444-8585 Japan – sequence: 5 givenname: Yuhui surname: Chai fullname: Chai, Yuhui organization: Section on Functional Imaging Methods, National Institute of Mental Health, Building 10, 10 Center Dr Bethesda, MD 20892, USA – sequence: 6 givenname: David C. surname: Jangraw fullname: Jangraw, David C. organization: Section on Functional Imaging Methods, National Institute of Mental Health, Building 10, 10 Center Dr Bethesda, MD 20892, USA – sequence: 7 givenname: Gang surname: Chen fullname: Chen, Gang organization: Scientific and Statistical Computational Core, National Institute of Mental Health, Building 10, 10 Center Dr Bethesda, MD 20892, USA – sequence: 8 givenname: Daniel A. surname: Handwerker fullname: Handwerker, Daniel A. organization: Section on Functional Imaging Methods, National Institute of Mental Health, Building 10, 10 Center Dr Bethesda, MD 20892, USA – sequence: 9 givenname: Peter J. surname: Molfese fullname: Molfese, Peter J. organization: Section on Functional Imaging Methods, National Institute of Mental Health, Building 10, 10 Center Dr Bethesda, MD 20892, USA – sequence: 10 givenname: Yoshimichi surname: Ejima fullname: Ejima, Yoshimichi organization: Graduate School of Interdisciplinary Science and Engineering in Health Systems, Okayama University, 3-1-1 Tsushima-Naka, Kita-ku, Okayama 700-8530, Japan – sequence: 11 givenname: Norihiro surname: Sadato fullname: Sadato, Norihiro organization: Division of Cerebral Research, National Institute for Physiological Sciences, 38 Nishigonaka, Myodaiji, Okazaki, Aichi, 444-8585 Japan – sequence: 12 givenname: Jinglong surname: Wu fullname: Wu, Jinglong organization: Graduate School of Interdisciplinary Science and Engineering in Health Systems, Okayama University, 3-1-1 Tsushima-Naka, Kita-ku, Okayama 700-8530, Japan – sequence: 13 givenname: Peter A. surname: Bandettini fullname: Bandettini, Peter A. organization: Section on Functional Imaging Methods, National Institute of Mental Health, Building 10, 10 Center Dr Bethesda, MD 20892, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34974114$$D View this record in MEDLINE/PubMed |
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| CitedBy_id | crossref_primary_10_1162_imag_a_00140 crossref_primary_10_1016_j_neuroimage_2025_121126 crossref_primary_10_1016_j_pneurobio_2023_102401 crossref_primary_10_1111_ejn_16381 crossref_primary_10_1177_20416695241264736 crossref_primary_10_1002_nbm_70105 crossref_primary_10_1038_s42256_025_01062_2 crossref_primary_10_1002_hbm_26227 crossref_primary_10_1162_imag_a_00264 crossref_primary_10_1002_hbm_26193 |
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| Copyright | 2021 The Authors Copyright © 2021 The Authors. Published by Elsevier Inc. All rights reserved. 2021. The Authors |
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| Keywords | Tactile prediction Temporal prediction error Layer-specific fMRI Primary somatosensory cortex High-resolution CBV–fMRI |
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| SubjectTerms | Adult Brain Mapping Cortex (somatosensory) Cortex (temporal) Feedback Female Fingers - physiology Functional magnetic resonance imaging Healthy Volunteers High-resolution CBV–fMRI Humans Image Processing, Computer-Assisted Information processing Layer-specific fMRI Magnetic Resonance Imaging - methods Male Neuroimaging Physiology Predictions Primary somatosensory cortex Reproducibility of Results Sensitivity and Specificity Somatosensory Cortex - physiology Tactile prediction Temporal prediction error Time Perception Time series Touch - physiology |
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| Title | Layer-specific activation in human primary somatosensory cortex during tactile temporal prediction error processing |
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