Influence of oxytocin administration on somatosensory evoked magnetic fields induced by median nerve stimulation during hand action observation in healthy male volunteers
Watching another person’s hand movement modulates somatosensory evoked magnetic fields (SEFs). Assuming that the mirror neuron system may have a role in this phenomenon, oxytocin should enhance these effects. This single-blinded, placebo-controlled, crossover study therefore used magnetoencephalogra...
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Published in | PloS one Vol. 16; no. 3; p. e0249167 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
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31.03.2021
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ISSN | 1932-6203 1932-6203 |
DOI | 10.1371/journal.pone.0249167 |
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Abstract | Watching another person’s hand movement modulates somatosensory evoked magnetic fields (SEFs). Assuming that the mirror neuron system may have a role in this phenomenon, oxytocin should enhance these effects. This single-blinded, placebo-controlled, crossover study therefore used magnetoencephalography (MEG) to investigate SEFs following electrical stimulation of the right median nerve in 20 healthy male participants during hand movement observation, which were initially presented as static images followed by moving images. The participants were randomly assigned to receive either oxytocin or saline during the first trial, with the treatment being reversed during a second trial. Log-transformed ratios of the N20 and N30 amplitudes were calculated and compared between moving and static images observations. Phase locking (calculated using intertrial phase coherence) of brain oscillations was also analyzed to evaluate alpha, beta and gamma rhythm changes after oxytocin administration. Log N30 ratios showed no significant changes after placebo administration but showed a decreasing tendency (albeit not significant) after placebo administration, which may suggest mirror neuron system involvement. In contrast, log N20 ratios were increased after placebo administration, but showed no significant change after oxytocin administration. Interestingly, the gamma band activity around N20 increased after placebo administration, suggesting that oxytocin exerted an analgesic effect on median nerve stimulation, and inhibited the gamma band increase. Oxytocin might therefore modulate not only the mirror neuron system, but also the sensory processing associated with median nerve stimulation. |
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AbstractList | About the Authors: Yasuki Ono Roles Data curation, Formal analysis, Project administration, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing * E-mail: spfy7ff9@wish.ocn.ne.jp Affiliations Department of Neuropsychiatry, Graduate School of Medicine, Hirosaki University, Hirosaki, Japan, Department of Psychiatry and Neurobiology, Graduate School of Medical Science, Kanazawa University, Kanazawa, Japan ORCID logo https://orcid.org/0000-0002-3374-4407 Tetsu Hirosawa Roles Data curation Affiliation: Department of Psychiatry and Neurobiology, Graduate School of Medical Science, Kanazawa University, Kanazawa, Japan Chiaki Hasegawa Roles Data curation, Formal analysis Affiliation: Research Center for Child Mental Development, Kanazawa University, Kanazawa, Japan Takashi Ikeda Roles Formal analysis, Methodology Affiliation: Research Center for Child Mental Development, Kanazawa University, Kanazawa, Japan Kiwamu Kudo Roles Formal analysis Affiliation: Ricoh Company, Ltd, Kanazawa, Japan Nobushige Naito Roles Data curation Affiliation: Department of Psychiatry and Neurobiology, Graduate School of Medical Science, Kanazawa University, Kanazawa, Japan Yuko Yoshimura Roles Data curation Affiliation: Research Center for Child Mental Development, Kanazawa University, Kanazawa, Japan Mitsuru Kikuchi Roles Conceptualization, Supervision Affiliation: Department of Psychiatry and Neurobiology, Graduate School of Medical Science, Kanazawa University, Kanazawa, Japan Introduction Somatosensory inputs from the periphery reach the contralateral primary somatosensory cortex (SI), which subsequently activates the ipsilateral SI and bilateral secondary somatosensory cortex (SII) [1,2].
A recent study with a sequential EEG-functional magnetic resonance imaging (fMRI) design showed similar patterns of mirror neuron activity and mu suppression; however, mu suppression was not confined to the mirror neuron areas, but involved a range of subcortical areas related to motor preparation and visual sensitivity [10].
[...]they also found that the increase in N30 amplitude correlated with central and precentral alpha and parietal beta phase locking of ongoing electroencephalography (EEG) signals.
[9] suggested that mu and beta suppression over the sensory-motor regions reflected a resonance system in the human brain analogous to mirror neuron activity.
[...]we hypothesized that oxytocin would increase the N30 amplitude during hand movement observation, and enhance alpha and beta suppression during hand movement. Watching another person’s hand movement modulates somatosensory evoked magnetic fields (SEFs). Assuming that the mirror neuron system may have a role in this phenomenon, oxytocin should enhance these effects. This single-blinded, placebo-controlled, crossover study therefore used magnetoencephalography (MEG) to investigate SEFs following electrical stimulation of the right median nerve in 20 healthy male participants during hand movement observation, which were initially presented as static images followed by moving images. The participants were randomly assigned to receive either oxytocin or saline during the first trial, with the treatment being reversed during a second trial. Log-transformed ratios of the N20 and N30 amplitudes were calculated and compared between moving and static images observations. Phase locking (calculated using intertrial phase coherence) of brain oscillations was also analyzed to evaluate alpha, beta and gamma rhythm changes after oxytocin administration. Log N30 ratios showed no significant changes after placebo administration but showed a decreasing tendency (albeit not significant) after placebo administration, which may suggest mirror neuron system involvement. In contrast, log N20 ratios were increased after placebo administration, but showed no significant change after oxytocin administration. Interestingly, the gamma band activity around N20 increased after placebo administration, suggesting that oxytocin exerted an analgesic effect on median nerve stimulation, and inhibited the gamma band increase. Oxytocin might therefore modulate not only the mirror neuron system, but also the sensory processing associated with median nerve stimulation. Watching another person's hand movement modulates somatosensory evoked magnetic fields (SEFs). Assuming that the mirror neuron system may have a role in this phenomenon, oxytocin should enhance these effects. This single-blinded, placebo-controlled, crossover study therefore used magnetoencephalography (MEG) to investigate SEFs following electrical stimulation of the right median nerve in 20 healthy male participants during hand movement observation, which were initially presented as static images followed by moving images. The participants were randomly assigned to receive either oxytocin or saline during the first trial, with the treatment being reversed during a second trial. Log-transformed ratios of the N20 and N30 amplitudes were calculated and compared between moving and static images observations. Phase locking (calculated using intertrial phase coherence) of brain oscillations was also analyzed to evaluate alpha, beta and gamma rhythm changes after oxytocin administration. Log N30 ratios showed no significant changes after placebo administration but showed a decreasing tendency (albeit not significant) after placebo administration, which may suggest mirror neuron system involvement. In contrast, log N20 ratios were increased after placebo administration, but showed no significant change after oxytocin administration. Interestingly, the gamma band activity around N20 increased after placebo administration, suggesting that oxytocin exerted an analgesic effect on median nerve stimulation, and inhibited the gamma band increase. Oxytocin might therefore modulate not only the mirror neuron system, but also the sensory processing associated with median nerve stimulation.Watching another person's hand movement modulates somatosensory evoked magnetic fields (SEFs). Assuming that the mirror neuron system may have a role in this phenomenon, oxytocin should enhance these effects. This single-blinded, placebo-controlled, crossover study therefore used magnetoencephalography (MEG) to investigate SEFs following electrical stimulation of the right median nerve in 20 healthy male participants during hand movement observation, which were initially presented as static images followed by moving images. The participants were randomly assigned to receive either oxytocin or saline during the first trial, with the treatment being reversed during a second trial. Log-transformed ratios of the N20 and N30 amplitudes were calculated and compared between moving and static images observations. Phase locking (calculated using intertrial phase coherence) of brain oscillations was also analyzed to evaluate alpha, beta and gamma rhythm changes after oxytocin administration. Log N30 ratios showed no significant changes after placebo administration but showed a decreasing tendency (albeit not significant) after placebo administration, which may suggest mirror neuron system involvement. In contrast, log N20 ratios were increased after placebo administration, but showed no significant change after oxytocin administration. Interestingly, the gamma band activity around N20 increased after placebo administration, suggesting that oxytocin exerted an analgesic effect on median nerve stimulation, and inhibited the gamma band increase. Oxytocin might therefore modulate not only the mirror neuron system, but also the sensory processing associated with median nerve stimulation. |
Audience | Academic |
Author | Hirosawa, Tetsu Ikeda, Takashi Naito, Nobushige Hasegawa, Chiaki Kikuchi, Mitsuru Ono, Yasuki Kudo, Kiwamu Yoshimura, Yuko |
AuthorAffiliation | 4 Ricoh Company, Ltd, Kanazawa, Japan 1 Department of Neuropsychiatry, Graduate School of Medicine, Hirosaki University, Hirosaki, Japan 3 Research Center for Child Mental Development, Kanazawa University, Kanazawa, Japan 2 Department of Psychiatry and Neurobiology, Graduate School of Medical Science, Kanazawa University, Kanazawa, Japan Chiba Daigaku, JAPAN |
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CitedBy_id | crossref_primary_10_1089_cyber_2023_0040 crossref_primary_10_3389_fnins_2022_858070 |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Competing Interests: KK is a paid employee of Ricoh Company, Ltd. This does not alter our adherence to PLOS ONE policies on sharing data and materials. There are no patents, products in development or marketed products associated with this research to declare.This does not alter our adherence to PLOS ONE policies on sharing data and materials. |
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Snippet | Watching another person’s hand movement modulates somatosensory evoked magnetic fields (SEFs). Assuming that the mirror neuron system may have a role in this... Watching another person's hand movement modulates somatosensory evoked magnetic fields (SEFs). Assuming that the mirror neuron system may have a role in this... About the Authors: Yasuki Ono Roles Data curation, Formal analysis, Project administration, Supervision, Validation, Visualization, Writing – original draft,... |
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SubjectTerms | Amplitudes Autism Beta phase Biology and Life Sciences Biomagnetism Brain mapping Children Cortex (parietal) Cortex (somatosensory) Data analysis EEG Electroencephalography Frequency dependence Functional magnetic resonance imaging Genetic aspects Graduate schools Graduate studies Keyboards Locking Magnetic fields Magnetic resonance Magnetic resonance imaging Median nerve Medical science Medicine and Health Sciences Mental development Nervous system Neurobiology Neuroimaging Neuropsychiatry Neurosciences Oxytocin Physiological aspects Psychiatry Research and Analysis Methods Research facilities Resonance Schizophrenia Sensorimotor integration Social Sciences Somatosensory cortex Somatosensory evoked magnetic fields |
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Title | Influence of oxytocin administration on somatosensory evoked magnetic fields induced by median nerve stimulation during hand action observation in healthy male volunteers |
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