Measurement of excitation-inhibition ratio in autism spectrum disorder using critical brain dynamics

Hilgo Bruining; Richard Hardstone; Erika L. Juarez-Martinez; Jan Sprengers; Arthur Ervin Avramiea; Sonja Simpraga; Simon J. Houtman; Simon Shlomo Poil; Eva Dallares; Satu Palva; Bob Oranje; J. Matias Palva; Huibert D. Mansvelder; Klaus Linkenkaer-Hansen

doi:10.1038/s41598-020-65500-4

Measurement of excitation-inhibition ratio in autism spectrum disorder using critical brain dynamics

Hilgo Bruining, Richard Hardstone, Erika L. Juarez-Martinez, Jan Sprengers, Arthur Ervin Avramiea, Sonja Simpraga, Simon J. Houtman, Simon Shlomo Poil, Eva Dallares, Satu Palva, Bob Oranje, J. Matias Palva, Huibert D. Mansvelder, Klaus Linkenkaer-Hansen^*

^*Corresponding author for this work

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

Balance between excitation (E) and inhibition (I) is a key principle for neuronal network organization and information processing. Consistent with this notion, excitation-inhibition imbalances are considered a pathophysiological mechanism in many brain disorders including autism spectrum disorder (ASD). However, methods to measure E/I ratios in human brain networks are lacking. Here, we present a method to quantify a functional E/I ratio (fE/I) from neuronal oscillations, and validate it in healthy subjects and children with ASD. We define structural E/I ratio in an in silico neuronal network, investigate how it relates to power and long-range temporal correlations (LRTC) of the network’s activity, and use these relationships to design the fE/I algorithm. Application of this algorithm to the EEGs of healthy adults showed that fE/I is balanced at the population level and is decreased through GABAergic enforcement. In children with ASD, we observed larger fE/I variability and stronger LRTC compared to typically developing children (TDC). Interestingly, visual grading for EEG abnormalities that are thought to reflect E/I imbalances revealed elevated fE/I and LRTC in ASD children with normal EEG compared to TDC or ASD with abnormal EEG. We speculate that our approach will help understand physiological heterogeneity also in other brain disorders.

Original language	English
Article number	9195
Pages (from-to)	1-15
Number of pages	15
Journal	Scientific Reports
Volume	10
Issue number	1
Early online date	8 Jun 2020
DOIs	https://doi.org/10.1038/s41598-020-65500-4
Publication status	Published - 8 Jun 2020

Funding

This work was funded by Netherlands Organization for Scientific Research (NWO) Physical Sciences Grant 612.001.123 (to K.L.-H.) and Social Sciences 406–15–256 (to A.-E.A. and K.L.-H.). H.B. and J.S. were funded by ZonMW Rational Pharmacotherapy Program (GGG project 836041015). S.S. was funded by EU MSCA-ITN CognitionNet (FP7-PEOPLE-2013-ITN 607508). H.D.M. received funding from EU H2020 ‘Human Brain Project’ grant agreement no. 604102. We thank Jan Bim and William Muñoz for discussions, and Joop van Gerven and Geert Jan Groeneveld from Centre for Human Drug Research for sharing the EEG data with the zolpidem intervention. We thank Mia Athina Thomaidou for reviewing EEG signals for artifacts on the adult validation sample.

Funders	Funder number
European Commission	FP7-PEOPLE-2013-ITN 607508
European Commission
ZonMw	836041015
ZonMw
Nederlandse Organisatie voor Wetenschappelijk Onderzoek	612.001.123
Nederlandse Organisatie voor Wetenschappelijk Onderzoek

Access to Document

10.1038/s41598-020-65500-4

Persistent URL (handle)

Persistent link

Cite this

Bruining, H., Hardstone, R., Juarez-Martinez, E. L., Sprengers, J., Avramiea, A. E., Simpraga, S., Houtman, S. J., Poil, S. S., Dallares, E., Palva, S., Oranje, B., Matias Palva, J., Mansvelder, H. D., & Linkenkaer-Hansen, K. (2020). Measurement of excitation-inhibition ratio in autism spectrum disorder using critical brain dynamics. Scientific Reports, 10(1), 1-15. Article 9195. https://doi.org/10.1038/s41598-020-65500-4

@article{1d78aadc7473421dbaa79504c5591d8e,

title = "Measurement of excitation-inhibition ratio in autism spectrum disorder using critical brain dynamics",

abstract = "Balance between excitation (E) and inhibition (I) is a key principle for neuronal network organization and information processing. Consistent with this notion, excitation-inhibition imbalances are considered a pathophysiological mechanism in many brain disorders including autism spectrum disorder (ASD). However, methods to measure E/I ratios in human brain networks are lacking. Here, we present a method to quantify a functional E/I ratio (fE/I) from neuronal oscillations, and validate it in healthy subjects and children with ASD. We define structural E/I ratio in an in silico neuronal network, investigate how it relates to power and long-range temporal correlations (LRTC) of the network{\textquoteright}s activity, and use these relationships to design the fE/I algorithm. Application of this algorithm to the EEGs of healthy adults showed that fE/I is balanced at the population level and is decreased through GABAergic enforcement. In children with ASD, we observed larger fE/I variability and stronger LRTC compared to typically developing children (TDC). Interestingly, visual grading for EEG abnormalities that are thought to reflect E/I imbalances revealed elevated fE/I and LRTC in ASD children with normal EEG compared to TDC or ASD with abnormal EEG. We speculate that our approach will help understand physiological heterogeneity also in other brain disorders.",

author = "Hilgo Bruining and Richard Hardstone and Juarez-Martinez, {Erika L.} and Jan Sprengers and Avramiea, {Arthur Ervin} and Sonja Simpraga and Houtman, {Simon J.} and Poil, {Simon Shlomo} and Eva Dallares and Satu Palva and Bob Oranje and {Matias Palva}, J. and Mansvelder, {Huibert D.} and Klaus Linkenkaer-Hansen",

year = "2020",

month = jun,

day = "8",

doi = "10.1038/s41598-020-65500-4",

language = "English",

volume = "10",

pages = "1--15",

journal = "Scientific Reports",

issn = "2045-2322",

publisher = "Nature Research",

number = "1",

}

Bruining, H, Hardstone, R, Juarez-Martinez, EL, Sprengers, J, Avramiea, AE, Simpraga, S, Houtman, SJ, Poil, SS, Dallares, E, Palva, S, Oranje, B, Matias Palva, J, Mansvelder, HD & Linkenkaer-Hansen, K 2020, 'Measurement of excitation-inhibition ratio in autism spectrum disorder using critical brain dynamics', Scientific Reports, vol. 10, no. 1, 9195, pp. 1-15. https://doi.org/10.1038/s41598-020-65500-4

TY - JOUR

T1 - Measurement of excitation-inhibition ratio in autism spectrum disorder using critical brain dynamics

AU - Bruining, Hilgo

AU - Hardstone, Richard

AU - Juarez-Martinez, Erika L.

AU - Sprengers, Jan

AU - Avramiea, Arthur Ervin

AU - Simpraga, Sonja

AU - Houtman, Simon J.

AU - Poil, Simon Shlomo

AU - Dallares, Eva

AU - Palva, Satu

AU - Oranje, Bob

AU - Matias Palva, J.

AU - Mansvelder, Huibert D.

AU - Linkenkaer-Hansen, Klaus

PY - 2020/6/8

Y1 - 2020/6/8

N2 - Balance between excitation (E) and inhibition (I) is a key principle for neuronal network organization and information processing. Consistent with this notion, excitation-inhibition imbalances are considered a pathophysiological mechanism in many brain disorders including autism spectrum disorder (ASD). However, methods to measure E/I ratios in human brain networks are lacking. Here, we present a method to quantify a functional E/I ratio (fE/I) from neuronal oscillations, and validate it in healthy subjects and children with ASD. We define structural E/I ratio in an in silico neuronal network, investigate how it relates to power and long-range temporal correlations (LRTC) of the network’s activity, and use these relationships to design the fE/I algorithm. Application of this algorithm to the EEGs of healthy adults showed that fE/I is balanced at the population level and is decreased through GABAergic enforcement. In children with ASD, we observed larger fE/I variability and stronger LRTC compared to typically developing children (TDC). Interestingly, visual grading for EEG abnormalities that are thought to reflect E/I imbalances revealed elevated fE/I and LRTC in ASD children with normal EEG compared to TDC or ASD with abnormal EEG. We speculate that our approach will help understand physiological heterogeneity also in other brain disorders.

AB - Balance between excitation (E) and inhibition (I) is a key principle for neuronal network organization and information processing. Consistent with this notion, excitation-inhibition imbalances are considered a pathophysiological mechanism in many brain disorders including autism spectrum disorder (ASD). However, methods to measure E/I ratios in human brain networks are lacking. Here, we present a method to quantify a functional E/I ratio (fE/I) from neuronal oscillations, and validate it in healthy subjects and children with ASD. We define structural E/I ratio in an in silico neuronal network, investigate how it relates to power and long-range temporal correlations (LRTC) of the network’s activity, and use these relationships to design the fE/I algorithm. Application of this algorithm to the EEGs of healthy adults showed that fE/I is balanced at the population level and is decreased through GABAergic enforcement. In children with ASD, we observed larger fE/I variability and stronger LRTC compared to typically developing children (TDC). Interestingly, visual grading for EEG abnormalities that are thought to reflect E/I imbalances revealed elevated fE/I and LRTC in ASD children with normal EEG compared to TDC or ASD with abnormal EEG. We speculate that our approach will help understand physiological heterogeneity also in other brain disorders.

UR - http://www.scopus.com/inward/record.url?scp=85086169006&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85086169006&partnerID=8YFLogxK

U2 - 10.1038/s41598-020-65500-4

DO - 10.1038/s41598-020-65500-4

M3 - Article

C2 - 32513931

AN - SCOPUS:85086169006

SN - 2045-2322

VL - 10

SP - 1

EP - 15

JO - Scientific Reports

JF - Scientific Reports

IS - 1

M1 - 9195

ER -

Measurement of excitation-inhibition ratio in autism spectrum disorder using critical brain dynamics

Abstract

Funding

Access to Document

Persistent URL (handle)

Other files and links

Fingerprint

Cite this