Cross-Frequency Coupling and Intelligent Neuromodulation

Chien-Hung Yeh; Chuting Zhang; Wenbin Shi; Men-Tzung Lo; Gerd Tinkhauser; Ashwini Oswal

doi:10.34133/cbsystems.0034

journal article Jan 01, 2023

Cross-Frequency Coupling and Intelligent Neuromodulation

Chien-Hung Yeh

Chuting Zhang Wenbin Shi Men-Tzung Lo Gerd Tinkhauser

Ashwini Oswal

Cyborg and Bionic Systems Vol. 4 · American Association for the Advancement of Science (AAAS)

View at Publisher Save 10.34133/cbsystems.0034

Abstract

Cross-frequency coupling (CFC) reflects (nonlinear) interactions between signals of different frequencies. Evidence from both patient and healthy participant studies suggests that CFC plays an essential role in neuronal computation, interregional interaction, and disease pathophysiology. The present review discusses methodological advances and challenges in the computation of CFC with particular emphasis on potential solutions to spurious coupling, inferring intrinsic rhythms in a targeted frequency band, and causal interferences. We specifically focus on the literature exploring CFC in the context of cognition/memory tasks, sleep, and neurological disorders, such as Alzheimer's disease, epilepsy, and Parkinson's disease. Furthermore, we highlight the implication of CFC in the context and for the optimization of invasive and noninvasive neuromodulation and rehabilitation. Mainly, CFC could support advancing the understanding of the neurophysiology of cognition and motor control, serve as a biomarker for disease symptoms, and leverage the optimization of therapeutic interventions, e.g., closed-loop brain stimulation. Despite the evident advantages of CFC as an investigative and translational tool in neuroscience, further methodological improvements are required to facilitate practical and correct use in cyborg and bionic systems in the field.

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References

151

[1]

Deep brain stimulation can suppress pathological synchronisation in parkinsonian patients

A. Eusebio, W. Thevathasan, L. Doyle Gaynor et al.

Journal of Neurology, Neurosurgery &amp; Psych... 2011 10.1136/jnnp.2010.217489

[2]

10.1038/s41583-022-00598-1

[3]

Closed-loop neuromodulation in an individual with treatment-resistant depression

Katherine W. Scangos, Ankit N. Khambhati, Patrick M. Daly et al.

Nature Medicine 2021 10.1038/s41591-021-01480-w

[4]

10.1016/j.conb.2014.10.003

[5]

10.1152/jn.00263.2005

[6]

Wang Y, Shi W, Yeh C-H. A novel measure of cardiopulmonary coupling during sleep based on the synchrosqueezing transform algorithm. IEEE J Biomed Health Inform. 2023;27(4):1790–1800.

[7]

Hyafil A, Giraud AL, Fontolan L, Gutkin B. Neural cross-frequency coupling: Connecting architectures, mechanisms, and functions. Trends Neurosci. 2015;38(11):725–740. 10.1016/j.tins.2015.09.001

[8]

A mechanism for cognitive dynamics: neuronal communication through neuronal coherence

Pascal Fries

Trends in Cognitive Sciences 10.1016/j.tics.2005.08.011

[9]

Amzica F, Steriade M. Short- and long-range neuronal synchronization of the slow (<1 Hz) cortical oscillation. J Neurophysiol. 1995;73(1):20–38. 10.1152/jn.1995.73.1.20

[10]

Axmacher N, Henseler MM, Jensen O, Weinreich I, Elger CE, Fell J. Cross-frequency coupling supports multi-item working memory in the human hippocampus. Proc Natl Acad Sci USA. 2010;107(7):3228–3233. 10.1073/pnas.0911531107

[11]

10.1523/jneurosci.4122-11.2012

[12]

Scheffer-Teixeira R, Tort ABL. On cross-frequency phase-phase coupling between theta and gamma oscillations in the hippocampus. eLife. 2016;5: e20515. 10.7554/elife.20515

[13]

Pogosyan A, Gaynor LD, Eusebio A, Brown P. Boosting cortical activity at beta-band frequencies slows movement in humans. Curr Biol. 2009;19(19):1637–1641. 10.1016/j.cub.2009.07.074

[14]

Joundi RA, Jenkinson N, Brittain JS, Aziz TZ, Brown P. Driving oscillatory activity in the human cortex enhances motor performance. Curr Biol. 2012;22(5):403–407. 10.1016/j.cub.2012.01.024

[15]

Vinogradov S, Herman A. Psychiatric illnesses as oscillatory connectomopathies. Neuropsychopharmacology. 2016;41(1):387–388. 10.1038/npp.2015.308

[16]

10.1097/wco.0000000000000034

[17]

The functional role of cross-frequency coupling

Ryan T. Canolty, Robert T. Knight

Trends in Cognitive Sciences 10.1016/j.tics.2010.09.001

[18]

Riddle J, Alexander ML, Schiller CE, Rubinow DR, Frohlich F. Reward-based decision-making engages distinct modes of cross-frequency coupling. Cereb Cortex. 2022;32(10):2079–2094.

[19]

Yeh CH, Young HWV, Wang CY, Wang YH, Lee PL, Kang JH, Lo MT. Quantifying spasticity with limited swinging cycles using pendulum test based on phase amplitude coupling. IEEE Trans Neural Syst Rehabil Eng. 2016;24(10):1081–1088. 10.1109/tnsre.2016.2521612

[20]

Voytek B, Canolty RT, Shestyuk A, Crone NE, Parvizi J, Knight RT. Shifts in gamma phase-amplitude coupling frequency from theta to alpha over posterior cortex during visual tasks. Front Hum Neurosci. 2010;4:191. 10.3389/fnhum.2010.00191

[21]

van Wingerden M, van der Meij R, Kalenscher T, Maris E, Pennartz CMA. Phase-amplitude coupling in rat orbitofrontal cortex discriminates between correct and incorrect decisions during associative learning. J Neurosci. 2014;34(2):493. 10.1523/jneurosci.2098-13.2014

[22]

Chen KH, Tang AM, Gilbert ZD, Martin del Campo-Vera R, Sebastian R, Gogia AS, Sundaram S, Tabarsi E, Lee Y, Lee R, et al. Theta low-gamma phase amplitude coupling in the human orbitofrontal cortex increases during a conflict-processing task. J Neural Eng. 2022;19(1):016026. 10.1088/1741-2552/ac4f9b

[23]

Yeh CH, Lo MT, Hu K. Spurious cross-frequency amplitude-amplitude coupling in nonstationary, nonlinear signals. Physica A. 2016;454:143–150. 10.1016/j.physa.2016.02.012

[24]

Mazaheri A, Nieuwenhuis ILC, Van Dijk H, Jensen O. Prestimulus alpha and mu activity predicts failure to inhibit motor responses. Hum Brain Mapp. 2009;30(6):1791–1800. 10.1002/hbm.20763

[25]

10.1073/pnas.0908193106

[26]

10.1038/nature08573

[27]

Coordination of entorhinal–hippocampal ensemble activity during associative learning

Kei M. Igarashi, Li Lu, Laura L. Colgin et al.

Nature 10.1038/nature13162

[28]

10.1371/journal.pbio.2000219

[29]

Amemiya S, Redish AD. Hippocampal theta-gamma coupling reflects state-dependent information processing in decision making. Cell Rep. 2018;22(12):3328–3338. 10.1016/j.celrep.2018.02.091

[30]

10.1016/j.conb.2014.08.002

[31]

Yeh CH, al-Fatly B, Kühn AA, Meidahl AC, Tinkhauser G, Tan H, Brown P. Waveform changes with the evolution of beta bursts in the human subthalamic nucleus. Clin Neurophysiol. 2020;131(9):2086–2099. 10.1016/j.clinph.2020.05.035

[32]

Kramer MA, Tort ABL, Kopell NJ. Sharp edge artifacts and spurious coupling in EEG frequency comodulation measures. J Neurosci Methods. 2008;170(2):352–357. 10.1016/j.jneumeth.2008.01.020

[33]

Lo MT, Novak V, Peng CK, Liu Y, Hu K. Nonlinear phase interaction between nonstationary signals: A comparison study of methods based on Hilbert-Huang and Fourier transforms. Phys Rev E Stat Nonlinear Soft Matter Phys. 2009;79(6): 061924. 10.1103/physreve.79.061924

[34]

Lozano-Soldevilla D, Huurne N, Oostenveld R. Neuronal oscillations with non-sinusoidal morphology produce spurious phase-to-amplitude coupling and directionality. Front Comput Neurosci. 2016;10:87. 10.3389/fncom.2016.00087

[35]

The empirical mode decomposition and the Hilbert spectrum for nonlinear and non-stationary time series analysis

Norden E. Huang, Zheng Shen, Steven R. Long et al.

Proceedings of the Royal Society A: Mathematical,... 1998 10.1098/rspa.1998.0193

[36]

10.1016/j.jneumeth.2014.01.006

[37]

Shi W, Yeh CH, Hong Y. Cross-frequency transfer entropy characterize coupling of interacting nonlinear oscillators in complex systems. IEEE Trans Biomed Eng. 2019;66(2):521–529. 10.1109/tbme.2018.2849823

[38]

Yeh CH, Shi W. Identifying phase-amplitude coupling in cyclic alternating pattern using masking signals. Sci Rep. 2018;8(1):2649. 10.1038/s41598-018-21013-9

[39]

Hu Y, Shi W, Yeh C-H. A novel nonlinear bispectrum analysis for dynamical complex oscillations. Cogn Neurodyn. 2023;1–21.

[40]

Zhang C, Yeh C-H, Shi W. Variational phase-amplitude coupling characterizes signatures of anterior cortex under emotional processing. IEEE J Biomed Health Inform. 2023;27(4):1935–1945. 10.1109/jbhi.2023.3243275

[41]

Measuring Phase-Amplitude Coupling Between Neuronal Oscillations of Different Frequencies

Adriano B. L. Tort, Robert Komorowski, Howard Eichenbaum et al.

Journal of Neurophysiology 2010 10.1152/jn.00106.2010

[42]

Penny WD, Duzel E, Miller KJ, Ojemann JG. Testing for nested oscillation. J Neurosci Methods. 2008;174(1):50–61. 10.1016/j.jneumeth.2008.06.035

[43]

Cohen MX. Assessing transient cross-frequency coupling in EEG data. J Neurosci Methods. 2008;168(2):494–499. 10.1016/j.jneumeth.2007.10.012

[44]

High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex

R. T. Canolty, E. Edwards, S. S. Dalal et al.

Science 10.1126/science.1128115

[45]

Özkurt TE, Schnitzler A. A critical note on the definition of phase-amplitude cross-frequency coupling. J Neurosci Methods. 2011;201(2):438–443. 10.1016/j.jneumeth.2011.08.014

[46]

10.1002/hipo.20117

[47]

Bruns A, Eckhorn R. Task-related coupling from high- to low-frequency signals among visual cortical areas in human subdural recordings. Int J Psychophysiol. 2004;51(2):97–116. 10.1016/j.ijpsycho.2003.07.001

[48]

10.1155/2011/156869

[49]

Brainstorm: A User-Friendly Application for MEG/EEG Analysis

François Tadel, Sylvain Baillet, John C. Mosher et al.

Computational Intelligence and Neuroscience 10.1155/2011/879716

[50]

Combrisson E, Nest T, Brovelli A, Ince RAA, Soto JLP, Guillot A, Jerbi K. Tensorpac: An open-source Python toolbox for tensor-based phase-amplitude coupling measurement in electrophysiological brain signals. PLOS Comput Biol. 2020;16(10): e1008302. 10.1371/journal.pcbi.1008302

Showing 50 of 151 references

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Details

Published: Jan 01, 2023
Vol/Issue: 4

Authors

C

Chien-Hung Yeh

School of Information and Electronics, Beijing Institute of Technology, Beijing, China.

C

Chuting Zhang

School of Information and Electronics, Beijing Institute of Technology, Beijing, China.

W

Wenbin Shi

School of Information and Electronics, Beijing Institute of Technology, Beijing, China.

M

Men-Tzung Lo

Department of Biomedical Sciences and Engineering, National Central University, Taoyuan, Taiwan.

G

Gerd Tinkhauser

Department of Neurology, Bern University Hospital and University of Bern, Bern, Switzerland.

A

Ashwini Oswal

MRC Brain Network Dynamics Unit, University of Oxford, Oxford, UK.

Cite This Article

Chien-Hung Yeh, Chuting Zhang, Wenbin Shi, et al. (2023). Cross-Frequency Coupling and Intelligent Neuromodulation. Cyborg and Bionic Systems, 4. https://doi.org/10.34133/cbsystems.0034

Cross-Frequency Coupling and Intelligent Neuromodulation

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