Predictability alters information flow during action observation in human electrocorticographic activity

Chaoyi Qin; Frederic Michon; Yoshiyuki Onuki; Yohei Ishishita; Keisuke Otani; Kensuke Kawai; Pascal Fries; Valeria Gazzola; Christian Keysers

doi:10.1016/j.celrep.2023.113432

Predictability alters information flow during action observation in human electrocorticographic activity

Chaoyi Qin, Frederic Michon, Yoshiyuki Onuki, Yohei Ishishita, Keisuke Otani, Kensuke Kawai, Pascal Fries, Valeria Gazzola, Christian Keysers

Research output: Contribution to journal/periodical › Article › Scientific › peer-review

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Abstract

The action observation network (AON) has been extensively studied using short, isolated motor acts. How activity in the network is altered when these isolated acts are embedded in meaningful sequences of actions remains poorly understood. Here we utilized intracranial electrocorticography to characterize how the exchange of information across key nodes of the AON-the precentral, supramarginal, and visual cortices-is affected by such embedding and the resulting predictability. We found more top-down beta oscillation from precentral to supramarginal contacts during the observation of predictable actions in meaningful sequences compared to the same actions in randomized, and hence less predictable, order. In addition, we find that expectations enabled by the embedding lead to a suppression of bottom-up visual responses in the high-gamma range in visual areas. These results, in line with predictive coding, inform how nodes of the AON integrate information to process the actions of others.

Original language	English
Pages (from-to)	113432
Journal	Cell Reports
Volume	42
Issue number	11
DOIs	https://doi.org/10.1016/j.celrep.2023.113432
Publication status	Published - 13 Nov 2023

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10.1016/j.celrep.2023.113432

Qin2023Final published version, 3.8 MBLicence: CC BY

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title = "Predictability alters information flow during action observation in human electrocorticographic activity",

abstract = "The action observation network (AON) has been extensively studied using short, isolated motor acts. How activity in the network is altered when these isolated acts are embedded in meaningful sequences of actions remains poorly understood. Here we utilized intracranial electrocorticography to characterize how the exchange of information across key nodes of the AON-the precentral, supramarginal, and visual cortices-is affected by such embedding and the resulting predictability. We found more top-down beta oscillation from precentral to supramarginal contacts during the observation of predictable actions in meaningful sequences compared to the same actions in randomized, and hence less predictable, order. In addition, we find that expectations enabled by the embedding lead to a suppression of bottom-up visual responses in the high-gamma range in visual areas. These results, in line with predictive coding, inform how nodes of the AON integrate information to process the actions of others.",

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T1 - Predictability alters information flow during action observation in human electrocorticographic activity

AU - Qin, Chaoyi

AU - Michon, Frederic

AU - Onuki, Yoshiyuki

AU - Ishishita, Yohei

AU - Otani, Keisuke

AU - Kawai, Kensuke

AU - Fries, Pascal

AU - Gazzola, Valeria

AU - Keysers, Christian

PY - 2023/11/13

Y1 - 2023/11/13

N2 - The action observation network (AON) has been extensively studied using short, isolated motor acts. How activity in the network is altered when these isolated acts are embedded in meaningful sequences of actions remains poorly understood. Here we utilized intracranial electrocorticography to characterize how the exchange of information across key nodes of the AON-the precentral, supramarginal, and visual cortices-is affected by such embedding and the resulting predictability. We found more top-down beta oscillation from precentral to supramarginal contacts during the observation of predictable actions in meaningful sequences compared to the same actions in randomized, and hence less predictable, order. In addition, we find that expectations enabled by the embedding lead to a suppression of bottom-up visual responses in the high-gamma range in visual areas. These results, in line with predictive coding, inform how nodes of the AON integrate information to process the actions of others.

AB - The action observation network (AON) has been extensively studied using short, isolated motor acts. How activity in the network is altered when these isolated acts are embedded in meaningful sequences of actions remains poorly understood. Here we utilized intracranial electrocorticography to characterize how the exchange of information across key nodes of the AON-the precentral, supramarginal, and visual cortices-is affected by such embedding and the resulting predictability. We found more top-down beta oscillation from precentral to supramarginal contacts during the observation of predictable actions in meaningful sequences compared to the same actions in randomized, and hence less predictable, order. In addition, we find that expectations enabled by the embedding lead to a suppression of bottom-up visual responses in the high-gamma range in visual areas. These results, in line with predictive coding, inform how nodes of the AON integrate information to process the actions of others.

U2 - 10.1016/j.celrep.2023.113432

DO - 10.1016/j.celrep.2023.113432

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SN - 2211-1247

VL - 42

SP - 113432

JO - Cell Reports

JF - Cell Reports

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Predictability alters information flow during action observation in human electrocorticographic activity

Abstract

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