Temporal dynamics of intranasal oxytocin in human brain electrophysiology

Marie Zelenina; MacIej Kosilo; Janir Da Cruz; Marília Antunes; Patrícia Figueiredo; Mitul A. Mehta; Diana Prata

doi:10.1093/cercor/bhab404

Temporal dynamics of intranasal oxytocin in human brain electrophysiology

Marie Zelenina, MacIej Kosilo, Janir Da Cruz, Marília Antunes, Patrícia Figueiredo, Mitul A. Mehta, Diana Prata^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

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Abstract

Oxytocin (OT) is a key modulator of human social cognition, popular in behavioral neuroscience. To adequately design and interpret intranasal OT (IN-OT) research, it is crucial to know for how long it affects human brain function once administered. However, this has been mostly deduced from peripheral body f luids studies, or uncommonly used dosages. We aimed to characterize IN-OT's effects on human brain function using resting-state EEG microstates across a typical experimental session duration. Nineteen healthy males participated in a double-blind, placebo-controlled, within-subject, cross-over design of 24 IU of IN-OT in 12-min windows 15 min-to1 h 42min after administration. We observed IN-OT effects on all microstates, across the observation span. During eyes-closed, IN-OT increased duration and contribution of A and contribution and occurrence of D, decreased duration and contribution of B and C; and increased transition probability C-to-B and C-to-D. In eyes-open, it increased A-to-C and A-to-D. As microstates A and D have been related to phonological auditory and attentional networks, respectively, we posit IN-OT may tune the brain for reception of external stimuli, particularly of social nature - tentatively supporting current neurocognitive hypotheses of OT. Moreover, we contrast our overall results against a comprehensive literature review of IN-OT time-course effects in the brain, highlighting comparability issues.

Original language	English
Pages (from-to)	3110-3126
Number of pages	17
Journal	Cerebral Cortex
Volume	32
Issue number	14
Early online date	4 Jan 2022
DOIs	https://doi.org/10.1093/cercor/bhab404
Publication status	Published - 15 Jul 2022

Keywords

electroencephalography
microstates
oxytocin
pharmacodynamics
resting-state

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Temporal dynamics of intranasal_ZELENINA_Publishedonline4January2022_GOLD VoR (CC BY)Final published version, 1.08 MBLicence: CC BY

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@article{cb916259d245460392962020b658a975,

title = "Temporal dynamics of intranasal oxytocin in human brain electrophysiology",

abstract = "Oxytocin (OT) is a key modulator of human social cognition, popular in behavioral neuroscience. To adequately design and interpret intranasal OT (IN-OT) research, it is crucial to know for how long it affects human brain function once administered. However, this has been mostly deduced from peripheral body f luids studies, or uncommonly used dosages. We aimed to characterize IN-OT's effects on human brain function using resting-state EEG microstates across a typical experimental session duration. Nineteen healthy males participated in a double-blind, placebo-controlled, within-subject, cross-over design of 24 IU of IN-OT in 12-min windows 15 min-to1 h 42min after administration. We observed IN-OT effects on all microstates, across the observation span. During eyes-closed, IN-OT increased duration and contribution of A and contribution and occurrence of D, decreased duration and contribution of B and C; and increased transition probability C-to-B and C-to-D. In eyes-open, it increased A-to-C and A-to-D. As microstates A and D have been related to phonological auditory and attentional networks, respectively, we posit IN-OT may tune the brain for reception of external stimuli, particularly of social nature - tentatively supporting current neurocognitive hypotheses of OT. Moreover, we contrast our overall results against a comprehensive literature review of IN-OT time-course effects in the brain, highlighting comparability issues. ",

keywords = "electroencephalography, microstates, oxytocin, pharmacodynamics, resting-state",

author = "Marie Zelenina and MacIej Kosilo and {Da Cruz}, Janir and Mar{\'i}lia Antunes and Patr{\'i}cia Figueiredo and Mehta, {Mitul A.} and Diana Prata",

note = "Funding Information: The European Commission Seventh Framework Programme Marie Curie Career Integration to D.P. Grant FP7-PEOPLE-2013-CIG-631952, the 2016 Bial Foundation Psychophysiology Grant grant—Ref. 292/16, and the Funda{\c c}{\~a}o para a Ci{\^e}ncia e Tecnologia (FCT) IF/00787/2014, LISBOA-01-0145-FEDER-030907 and DSAIPA/DS/0065/2018 grants, and the iMM Lisboa Director{\textquoteright}s Fund Breakthrough Idea Grant 2016; and is a co-founder and shareholder of the neuroimaging research services company NeuroPsyAI, Ltd MZ and M.K. were employed on FCT IF/00787/2014 and LISBOA-01-0145-FEDER-030907 grants. MA{\textquoteright}s research is partially funded by Funda{\c c}{\~a}o para a Ci{\^e}ncia e Tecnologia (FCT), under the project UID/MAT/00006/2019. Publisher Copyright: {\textcopyright} The Author(s) 2021.",

year = "2022",

month = jul,

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doi = "10.1093/cercor/bhab404",

language = "English",

volume = "32",

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T1 - Temporal dynamics of intranasal oxytocin in human brain electrophysiology

AU - Zelenina, Marie

AU - Kosilo, MacIej

AU - Da Cruz, Janir

AU - Antunes, Marília

AU - Figueiredo, Patrícia

AU - Mehta, Mitul A.

AU - Prata, Diana

N1 - Funding Information: The European Commission Seventh Framework Programme Marie Curie Career Integration to D.P. Grant FP7-PEOPLE-2013-CIG-631952, the 2016 Bial Foundation Psychophysiology Grant grant—Ref. 292/16, and the Fundação para a Ciência e Tecnologia (FCT) IF/00787/2014, LISBOA-01-0145-FEDER-030907 and DSAIPA/DS/0065/2018 grants, and the iMM Lisboa Director’s Fund Breakthrough Idea Grant 2016; and is a co-founder and shareholder of the neuroimaging research services company NeuroPsyAI, Ltd MZ and M.K. were employed on FCT IF/00787/2014 and LISBOA-01-0145-FEDER-030907 grants. MA’s research is partially funded by Fundação para a Ciência e Tecnologia (FCT), under the project UID/MAT/00006/2019. Publisher Copyright: © The Author(s) 2021.

PY - 2022/7/15

Y1 - 2022/7/15

N2 - Oxytocin (OT) is a key modulator of human social cognition, popular in behavioral neuroscience. To adequately design and interpret intranasal OT (IN-OT) research, it is crucial to know for how long it affects human brain function once administered. However, this has been mostly deduced from peripheral body f luids studies, or uncommonly used dosages. We aimed to characterize IN-OT's effects on human brain function using resting-state EEG microstates across a typical experimental session duration. Nineteen healthy males participated in a double-blind, placebo-controlled, within-subject, cross-over design of 24 IU of IN-OT in 12-min windows 15 min-to1 h 42min after administration. We observed IN-OT effects on all microstates, across the observation span. During eyes-closed, IN-OT increased duration and contribution of A and contribution and occurrence of D, decreased duration and contribution of B and C; and increased transition probability C-to-B and C-to-D. In eyes-open, it increased A-to-C and A-to-D. As microstates A and D have been related to phonological auditory and attentional networks, respectively, we posit IN-OT may tune the brain for reception of external stimuli, particularly of social nature - tentatively supporting current neurocognitive hypotheses of OT. Moreover, we contrast our overall results against a comprehensive literature review of IN-OT time-course effects in the brain, highlighting comparability issues.

AB - Oxytocin (OT) is a key modulator of human social cognition, popular in behavioral neuroscience. To adequately design and interpret intranasal OT (IN-OT) research, it is crucial to know for how long it affects human brain function once administered. However, this has been mostly deduced from peripheral body f luids studies, or uncommonly used dosages. We aimed to characterize IN-OT's effects on human brain function using resting-state EEG microstates across a typical experimental session duration. Nineteen healthy males participated in a double-blind, placebo-controlled, within-subject, cross-over design of 24 IU of IN-OT in 12-min windows 15 min-to1 h 42min after administration. We observed IN-OT effects on all microstates, across the observation span. During eyes-closed, IN-OT increased duration and contribution of A and contribution and occurrence of D, decreased duration and contribution of B and C; and increased transition probability C-to-B and C-to-D. In eyes-open, it increased A-to-C and A-to-D. As microstates A and D have been related to phonological auditory and attentional networks, respectively, we posit IN-OT may tune the brain for reception of external stimuli, particularly of social nature - tentatively supporting current neurocognitive hypotheses of OT. Moreover, we contrast our overall results against a comprehensive literature review of IN-OT time-course effects in the brain, highlighting comparability issues.

KW - electroencephalography

KW - microstates

KW - oxytocin

KW - pharmacodynamics

KW - resting-state

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DO - 10.1093/cercor/bhab404

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AN - SCOPUS:85134720742

SN - 1047-3211

VL - 32

SP - 3110

EP - 3126

JO - Cerebral Cortex

JF - Cerebral Cortex

IS - 14

ER -

Temporal dynamics of intranasal oxytocin in human brain electrophysiology

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Keywords

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