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Cortical Processing of Multimodal Sensory Learning in Human Neonates

Following birth, infants must immediately process and rapidly adapt to the array of unknown sensory experiences associated with their new ex-utero environment. However, although it is known that unimodal stimuli induce activity in the corresponding primary sensory cortices of the newborn brain, it i...

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Autores principales: Dall'Orso, S, Fifer, W P, Balsam, P D, Brandon, J, O’Keefe, C, Poppe, T, Vecchiato, K, Edwards, A D, Burdet, E, Arichi, T
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7869081/
https://www.ncbi.nlm.nih.gov/pubmed/33207366
http://dx.doi.org/10.1093/cercor/bhaa340
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author Dall'Orso, S
Fifer, W P
Balsam, P D
Brandon, J
O’Keefe, C
Poppe, T
Vecchiato, K
Edwards, A D
Burdet, E
Arichi, T
author_facet Dall'Orso, S
Fifer, W P
Balsam, P D
Brandon, J
O’Keefe, C
Poppe, T
Vecchiato, K
Edwards, A D
Burdet, E
Arichi, T
author_sort Dall'Orso, S
collection PubMed
description Following birth, infants must immediately process and rapidly adapt to the array of unknown sensory experiences associated with their new ex-utero environment. However, although it is known that unimodal stimuli induce activity in the corresponding primary sensory cortices of the newborn brain, it is unclear how multimodal stimuli are processed and integrated across modalities. The latter is essential for learning and understanding environmental contingencies through encoding relationships between sensory experiences; and ultimately likely subserves development of life-long skills such as speech and language. Here, for the first time, we map the intracerebral processing which underlies auditory-sensorimotor classical conditioning in a group of 13 neonates (median gestational age at birth: 38 weeks + 4 days, range: 32 weeks + 2 days to 41 weeks + 6 days; median postmenstrual age at scan: 40 weeks + 5 days, range: 38 weeks + 3 days to 42 weeks + 1 days) with blood-oxygen-level-dependent (BOLD) functional magnetic resonance imaging (MRI) and magnetic resonance (MR) compatible robotics. We demonstrate that classical conditioning can induce crossmodal changes within putative unimodal sensory cortex even in the absence of its archetypal substrate. Our results also suggest that multimodal learning is associated with network wide activity within the conditioned neural system. These findings suggest that in early life, external multimodal sensory stimulation and integration shapes activity in the developing cortex and may influence its associated functional network architecture.
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spelling pubmed-78690812021-02-11 Cortical Processing of Multimodal Sensory Learning in Human Neonates Dall'Orso, S Fifer, W P Balsam, P D Brandon, J O’Keefe, C Poppe, T Vecchiato, K Edwards, A D Burdet, E Arichi, T Cereb Cortex Original Article Following birth, infants must immediately process and rapidly adapt to the array of unknown sensory experiences associated with their new ex-utero environment. However, although it is known that unimodal stimuli induce activity in the corresponding primary sensory cortices of the newborn brain, it is unclear how multimodal stimuli are processed and integrated across modalities. The latter is essential for learning and understanding environmental contingencies through encoding relationships between sensory experiences; and ultimately likely subserves development of life-long skills such as speech and language. Here, for the first time, we map the intracerebral processing which underlies auditory-sensorimotor classical conditioning in a group of 13 neonates (median gestational age at birth: 38 weeks + 4 days, range: 32 weeks + 2 days to 41 weeks + 6 days; median postmenstrual age at scan: 40 weeks + 5 days, range: 38 weeks + 3 days to 42 weeks + 1 days) with blood-oxygen-level-dependent (BOLD) functional magnetic resonance imaging (MRI) and magnetic resonance (MR) compatible robotics. We demonstrate that classical conditioning can induce crossmodal changes within putative unimodal sensory cortex even in the absence of its archetypal substrate. Our results also suggest that multimodal learning is associated with network wide activity within the conditioned neural system. These findings suggest that in early life, external multimodal sensory stimulation and integration shapes activity in the developing cortex and may influence its associated functional network architecture. Oxford University Press 2020-11-18 /pmc/articles/PMC7869081/ /pubmed/33207366 http://dx.doi.org/10.1093/cercor/bhaa340 Text en © The Author(s) 2020. Published by Oxford University Press. http://creativecommons.org/licenses/by/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Original Article
Dall'Orso, S
Fifer, W P
Balsam, P D
Brandon, J
O’Keefe, C
Poppe, T
Vecchiato, K
Edwards, A D
Burdet, E
Arichi, T
Cortical Processing of Multimodal Sensory Learning in Human Neonates
title Cortical Processing of Multimodal Sensory Learning in Human Neonates
title_full Cortical Processing of Multimodal Sensory Learning in Human Neonates
title_fullStr Cortical Processing of Multimodal Sensory Learning in Human Neonates
title_full_unstemmed Cortical Processing of Multimodal Sensory Learning in Human Neonates
title_short Cortical Processing of Multimodal Sensory Learning in Human Neonates
title_sort cortical processing of multimodal sensory learning in human neonates
topic Original Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7869081/
https://www.ncbi.nlm.nih.gov/pubmed/33207366
http://dx.doi.org/10.1093/cercor/bhaa340
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