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Cortical control of object‐specific grasp relies on adjustments of both activity and effective connectivity: a common marmoset study

KEY POINTS: The cortical mechanisms of grasping have been extensively studied in macaques and humans; here, we investigated whether common marmosets could rely on similar mechanisms despite strong differences in hand morphology and grip diversity. We recorded electrocorticographic activity over the...

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Autores principales: Tia, Banty, Takemi, Mitsuaki, Kosugi, Akito, Castagnola, Elisa, Ansaldo, Alberto, Nakamura, Takafumi, Ricci, Davide, Ushiba, Junichi, Fadiga, Luciano, Iriki, Atsushi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5709338/
https://www.ncbi.nlm.nih.gov/pubmed/28791721
http://dx.doi.org/10.1113/JP274629
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author Tia, Banty
Takemi, Mitsuaki
Kosugi, Akito
Castagnola, Elisa
Ansaldo, Alberto
Nakamura, Takafumi
Ricci, Davide
Ushiba, Junichi
Fadiga, Luciano
Iriki, Atsushi
author_facet Tia, Banty
Takemi, Mitsuaki
Kosugi, Akito
Castagnola, Elisa
Ansaldo, Alberto
Nakamura, Takafumi
Ricci, Davide
Ushiba, Junichi
Fadiga, Luciano
Iriki, Atsushi
author_sort Tia, Banty
collection PubMed
description KEY POINTS: The cortical mechanisms of grasping have been extensively studied in macaques and humans; here, we investigated whether common marmosets could rely on similar mechanisms despite strong differences in hand morphology and grip diversity. We recorded electrocorticographic activity over the sensorimotor cortex of two common marmosets during the execution of different grip types, which allowed us to study cortical activity (power spectrum) and physiologically inferred connectivity (phase‐slope index). Analyses were performed in beta (16–35 Hz) and gamma (75–100 Hz) frequency bands and our results showed that beta power varied depending on grip type, whereas gamma power displayed clear epoch‐related modulation. Strength and direction of inter‐area connectivity varied depending on grip type and epoch. These findings suggest that fundamental control mechanisms are conserved across primates and, in future research, marmosets could represent an adequate model to investigate primate brain mechanisms. ABSTRACT: The cortical mechanisms of grasping have been extensively studied in macaques and humans. Here, we investigated whether common marmosets could rely on similar mechanisms despite striking differences in manual dexterity. Two common marmosets were trained to grasp‐and‐pull three objects eliciting different hand configurations: whole‐hand, finger and scissor grips. The animals were then chronically implanted with 64‐channel electrocorticogram arrays positioned over the left premotor, primary motor and somatosensory cortex. Power spectra, reflecting predominantly cortical activity, and phase‐slope index, reflecting the direction of information flux, were studied in beta (16–35 Hz) and gamma (75–100 Hz) bands. Differences related to grip type, epoch (reach, grasp) and cortical area were statistically assessed. Results showed that whole‐hand and scissor grips triggered stronger beta desynchronization than finger grip. Task epochs clearly modulated gamma power, especially for finger and scissor grips. Considering effective connectivity, finger and scissor grips evoked stronger outflow from primary motor to premotor cortex, whereas whole‐hand grip displayed the opposite pattern. These findings suggest that fundamental control mechanisms, relying on adjustments of cortical activity and connectivity, are conserved across primates. Consistently, marmosets could represent a good model to investigate primate brain mechanisms.
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spelling pubmed-57093382017-12-06 Cortical control of object‐specific grasp relies on adjustments of both activity and effective connectivity: a common marmoset study Tia, Banty Takemi, Mitsuaki Kosugi, Akito Castagnola, Elisa Ansaldo, Alberto Nakamura, Takafumi Ricci, Davide Ushiba, Junichi Fadiga, Luciano Iriki, Atsushi J Physiol Neuroscience ‐ Behavioural/Systems/Cognitive KEY POINTS: The cortical mechanisms of grasping have been extensively studied in macaques and humans; here, we investigated whether common marmosets could rely on similar mechanisms despite strong differences in hand morphology and grip diversity. We recorded electrocorticographic activity over the sensorimotor cortex of two common marmosets during the execution of different grip types, which allowed us to study cortical activity (power spectrum) and physiologically inferred connectivity (phase‐slope index). Analyses were performed in beta (16–35 Hz) and gamma (75–100 Hz) frequency bands and our results showed that beta power varied depending on grip type, whereas gamma power displayed clear epoch‐related modulation. Strength and direction of inter‐area connectivity varied depending on grip type and epoch. These findings suggest that fundamental control mechanisms are conserved across primates and, in future research, marmosets could represent an adequate model to investigate primate brain mechanisms. ABSTRACT: The cortical mechanisms of grasping have been extensively studied in macaques and humans. Here, we investigated whether common marmosets could rely on similar mechanisms despite striking differences in manual dexterity. Two common marmosets were trained to grasp‐and‐pull three objects eliciting different hand configurations: whole‐hand, finger and scissor grips. The animals were then chronically implanted with 64‐channel electrocorticogram arrays positioned over the left premotor, primary motor and somatosensory cortex. Power spectra, reflecting predominantly cortical activity, and phase‐slope index, reflecting the direction of information flux, were studied in beta (16–35 Hz) and gamma (75–100 Hz) bands. Differences related to grip type, epoch (reach, grasp) and cortical area were statistically assessed. Results showed that whole‐hand and scissor grips triggered stronger beta desynchronization than finger grip. Task epochs clearly modulated gamma power, especially for finger and scissor grips. Considering effective connectivity, finger and scissor grips evoked stronger outflow from primary motor to premotor cortex, whereas whole‐hand grip displayed the opposite pattern. These findings suggest that fundamental control mechanisms, relying on adjustments of cortical activity and connectivity, are conserved across primates. Consistently, marmosets could represent a good model to investigate primate brain mechanisms. John Wiley and Sons Inc. 2017-09-02 2017-12-01 /pmc/articles/PMC5709338/ /pubmed/28791721 http://dx.doi.org/10.1113/JP274629 Text en © 2017 The Authors. The Journal of Physiology published by John Wiley & Sons Ltd on behalf of The Physiological Society This is an open access article under the terms of the Creative Commons Attribution (http://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Neuroscience ‐ Behavioural/Systems/Cognitive
Tia, Banty
Takemi, Mitsuaki
Kosugi, Akito
Castagnola, Elisa
Ansaldo, Alberto
Nakamura, Takafumi
Ricci, Davide
Ushiba, Junichi
Fadiga, Luciano
Iriki, Atsushi
Cortical control of object‐specific grasp relies on adjustments of both activity and effective connectivity: a common marmoset study
title Cortical control of object‐specific grasp relies on adjustments of both activity and effective connectivity: a common marmoset study
title_full Cortical control of object‐specific grasp relies on adjustments of both activity and effective connectivity: a common marmoset study
title_fullStr Cortical control of object‐specific grasp relies on adjustments of both activity and effective connectivity: a common marmoset study
title_full_unstemmed Cortical control of object‐specific grasp relies on adjustments of both activity and effective connectivity: a common marmoset study
title_short Cortical control of object‐specific grasp relies on adjustments of both activity and effective connectivity: a common marmoset study
title_sort cortical control of object‐specific grasp relies on adjustments of both activity and effective connectivity: a common marmoset study
topic Neuroscience ‐ Behavioural/Systems/Cognitive
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5709338/
https://www.ncbi.nlm.nih.gov/pubmed/28791721
http://dx.doi.org/10.1113/JP274629
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