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Hyperbrain features of team mental models within a juggling paradigm: a proof of concept

BACKGROUND: Research on cooperative behavior and the social brain exists, but little research has focused on real-time motor cooperative behavior and its neural correlates. In this proof of concept study, we explored the conceptual notion of shared and complementary mental models through EEG mapping...

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Autores principales: Filho, Edson, Bertollo, Maurizio, Tamburro, Gabriella, Schinaia, Lorenzo, Chatel-Goldman, Jonas, di Fronso, Selenia, Robazza, Claudio, Comani, Silvia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: PeerJ Inc. 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5036110/
https://www.ncbi.nlm.nih.gov/pubmed/27688968
http://dx.doi.org/10.7717/peerj.2457
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author Filho, Edson
Bertollo, Maurizio
Tamburro, Gabriella
Schinaia, Lorenzo
Chatel-Goldman, Jonas
di Fronso, Selenia
Robazza, Claudio
Comani, Silvia
author_facet Filho, Edson
Bertollo, Maurizio
Tamburro, Gabriella
Schinaia, Lorenzo
Chatel-Goldman, Jonas
di Fronso, Selenia
Robazza, Claudio
Comani, Silvia
author_sort Filho, Edson
collection PubMed
description BACKGROUND: Research on cooperative behavior and the social brain exists, but little research has focused on real-time motor cooperative behavior and its neural correlates. In this proof of concept study, we explored the conceptual notion of shared and complementary mental models through EEG mapping of two brains performing a real-world interactive motor task of increasing difficulty. We used the recently introduced participative “juggling paradigm,” and collected neuro-physiological and psycho-social data. We were interested in analyzing the between-brains coupling during a dyadic juggling task, and in exploring the relationship between the motor task execution, the jugglers’skill level and the task difficulty. We also investigated how this relationship could be mirrored in the coupled functional organization of the interacting brains. METHODS: To capture the neural schemas underlying the notion of shared and complementary mental models, we examined the functional connectivity patterns and hyperbrain features of a juggling dyad involved in cooperative motor tasks of increasing difficulty. Jugglers’ cortical activity was measured using two synchronized 32-channel EEG systems during dyadic juggling performed with 3, 4, 5 and 6 balls. Individual and hyperbrain functional connections were quantified through coherence maps calculated across all electrode pairs in the theta and alpha bands (4–8 and 8–12 Hz). Graph metrics were used to typify the global topology and efficiency of the functional networks for the four difficulty levels in the theta and alpha bands. RESULTS: Results indicated that, as task difficulty increased, the cortical functional organization of the more skilled juggler became progressively more segregated in both frequency bands, with a small-world organization in the theta band during easier tasks, indicative of a flow-like state in line with the neural efficiency hypothesis. Conversely, more integrated functional patterns were observed for the less skilled juggler in both frequency bands, possibly related to cognitive overload due to the difficulty of the task at hand (reinvestment hypothesis). At the hyperbrain level, a segregated functional organization involving areas of the visuo-attentional networks of both jugglers was observed in both frequency bands and for the easier task only. DISCUSSION: These results suggest that cooperative juggling is supported by integrated activity of specialized cortical areas from both brains only during easier tasks, whereas it relies on individual skills, mirrored in uncorrelated individual brain activations, during more difficult tasks. These findings suggest that task difficulty and jugglers’ personal skills may influence the features of the hyperbrain network in its shared/integrative and complementary/segregative tendencies.
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spelling pubmed-50361102016-09-29 Hyperbrain features of team mental models within a juggling paradigm: a proof of concept Filho, Edson Bertollo, Maurizio Tamburro, Gabriella Schinaia, Lorenzo Chatel-Goldman, Jonas di Fronso, Selenia Robazza, Claudio Comani, Silvia PeerJ Neuroscience BACKGROUND: Research on cooperative behavior and the social brain exists, but little research has focused on real-time motor cooperative behavior and its neural correlates. In this proof of concept study, we explored the conceptual notion of shared and complementary mental models through EEG mapping of two brains performing a real-world interactive motor task of increasing difficulty. We used the recently introduced participative “juggling paradigm,” and collected neuro-physiological and psycho-social data. We were interested in analyzing the between-brains coupling during a dyadic juggling task, and in exploring the relationship between the motor task execution, the jugglers’skill level and the task difficulty. We also investigated how this relationship could be mirrored in the coupled functional organization of the interacting brains. METHODS: To capture the neural schemas underlying the notion of shared and complementary mental models, we examined the functional connectivity patterns and hyperbrain features of a juggling dyad involved in cooperative motor tasks of increasing difficulty. Jugglers’ cortical activity was measured using two synchronized 32-channel EEG systems during dyadic juggling performed with 3, 4, 5 and 6 balls. Individual and hyperbrain functional connections were quantified through coherence maps calculated across all electrode pairs in the theta and alpha bands (4–8 and 8–12 Hz). Graph metrics were used to typify the global topology and efficiency of the functional networks for the four difficulty levels in the theta and alpha bands. RESULTS: Results indicated that, as task difficulty increased, the cortical functional organization of the more skilled juggler became progressively more segregated in both frequency bands, with a small-world organization in the theta band during easier tasks, indicative of a flow-like state in line with the neural efficiency hypothesis. Conversely, more integrated functional patterns were observed for the less skilled juggler in both frequency bands, possibly related to cognitive overload due to the difficulty of the task at hand (reinvestment hypothesis). At the hyperbrain level, a segregated functional organization involving areas of the visuo-attentional networks of both jugglers was observed in both frequency bands and for the easier task only. DISCUSSION: These results suggest that cooperative juggling is supported by integrated activity of specialized cortical areas from both brains only during easier tasks, whereas it relies on individual skills, mirrored in uncorrelated individual brain activations, during more difficult tasks. These findings suggest that task difficulty and jugglers’ personal skills may influence the features of the hyperbrain network in its shared/integrative and complementary/segregative tendencies. PeerJ Inc. 2016-09-20 /pmc/articles/PMC5036110/ /pubmed/27688968 http://dx.doi.org/10.7717/peerj.2457 Text en © 2016 Filho et al. 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 use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited.
spellingShingle Neuroscience
Filho, Edson
Bertollo, Maurizio
Tamburro, Gabriella
Schinaia, Lorenzo
Chatel-Goldman, Jonas
di Fronso, Selenia
Robazza, Claudio
Comani, Silvia
Hyperbrain features of team mental models within a juggling paradigm: a proof of concept
title Hyperbrain features of team mental models within a juggling paradigm: a proof of concept
title_full Hyperbrain features of team mental models within a juggling paradigm: a proof of concept
title_fullStr Hyperbrain features of team mental models within a juggling paradigm: a proof of concept
title_full_unstemmed Hyperbrain features of team mental models within a juggling paradigm: a proof of concept
title_short Hyperbrain features of team mental models within a juggling paradigm: a proof of concept
title_sort hyperbrain features of team mental models within a juggling paradigm: a proof of concept
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5036110/
https://www.ncbi.nlm.nih.gov/pubmed/27688968
http://dx.doi.org/10.7717/peerj.2457
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