Probing Intrinsic Neural Timescales in EEG with an Information-Theory Inspired Approach: Permutation Entropy Time Delay Estimation (PE-TD)

Author:

Buccellato Andrea12,Çatal Yasir3,Bisiacchi Patrizia12,Zang Di456789,Zilio Federico10ORCID,Wang Zhe456789,Qi Zengxin456789,Zheng Ruizhe456789,Xu Zeyu456789,Wu Xuehai456789,Del Felice Alessandra111ORCID,Mao Ying456789ORCID,Northoff Georg31213ORCID

Affiliation:

1. Padova Neuroscience Center, University of Padova, Via Orus 2/B, 35129 Padova, Italy

2. Department of General Psychology, University of Padova, Via Venezia, 8, 35131 Padova, Italy

3. The Royal’s Institute of Mental Health Research & University of Ottawa, Brain and Mind Research Institute, Centre for Neural Dynamics, Faculty of Medicine, University of Ottawa, 145 Carling Avenue, Rm. 6435, Ottawa, ON K1Z 7K4, Canada

4. Department of Neurosurgery, Huashan Hospital, Shanghai Medical College, Fudan University, Shanghai 200040, China

5. Shanghai Key Laboratory of Brain Function and Restoration and Neural Regeneration, Shanghai 200040, China

6. State Key Laboratory of Medical Neurobiology, MOE Frontiers Center for Brain Science, School of Basic Medical Sciences and Institutes of Brain Science, Fudan University, Shanghai 200032, China

7. National Center for Neurological Disorders, Shanghai 200040, China

8. Neurosurgical Institute, Fudan University, Shanghai 200040, China

9. Shanghai Clinical Medical Center of Neurosurgery, Shanghai 200040, China

10. Department of Philosophy, Sociology, Education and Applied Psychology, University of Padova, Piazza Capitaniato, 3, 35139 Padova, Italy

11. Department of Neuroscience, Section of Neurology, University of Padova, Via Belzoni, 160, 35121 Padova, Italy

12. Mental Health Center, Zhejiang University School of Medicine, Hangzhou 310013, China

13. Centre for Cognition and Brain Disorders, Hangzhou Normal University, Hangzhou 310013, China

Abstract

Time delays are a signature of many physical systems, including the brain, and considerably shape their dynamics; moreover, they play a key role in consciousness, as postulated by the temporo-spatial theory of consciousness (TTC). However, they are often not known a priori and need to be estimated from time series. In this study, we propose the use of permutation entropy (PE) to estimate time delays from neural time series as a more robust alternative to the widely used autocorrelation window (ACW). In the first part, we demonstrate the validity of this approach on synthetic neural data, and we show its resistance to regimes of nonstationarity in time series. Mirroring yet another example of comparable behavior between different nonlinear systems, permutation entropy–time delay estimation (PE-TD) is also able to measure intrinsic neural timescales (INTs) (temporal windows of neural activity at rest) from hd-EEG human data; additionally, this replication extends to the abnormal prolongation of INT values in disorders of consciousness (DoCs). Surprisingly, the correlation between ACW-0 and PE-TD decreases in a state-dependent manner when consciousness is lost, hinting at potential different regimes of nonstationarity and nonlinearity in conscious/unconscious states, consistent with many current theoretical frameworks on consciousness. In summary, we demonstrate the validity of PE-TD as a tool to extract relevant time scales from neural data; furthermore, given the divergence between ACW and PE-TD specific to DoC subjects, we hint at its potential use for the characterization of conscious states.

Funder

European Union’s Horizon 2020 Framework Programme for Research and Innovation

UMRF, uOBMRI, CIHR

Canada-UK Artificial Intelligence Initiative

PSI

Shanghai Center for Brain Science and Brain-Inspired Technology

Lingang Laboratory

National Natural Science Foundation of China

PRIN 2022

PNRR PE8 “Age-It”

University of Padova

Publisher

MDPI AG

Subject

General Physics and Astronomy

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