Skip to main content
Log in

Time-Resolved Directional Brain–Heart Interplay Measurement Through Synthetic Data Generation Models

  • Published:
Annals of Biomedical Engineering Aims and scope Submit manuscript

Abstract

Although a plethora of synthetic data generation models have been proposed to validate biomarkers of brain and cardiovascular dynamics separately, a limited number of computational methods estimating directed brain–heart information flow are currently available in the scientific literature. This study introduces a computational framework exploiting existing generative models for a novel time-resolved quantification of causal brain–heart interplay. Exemplarily, having electroencephalographic signals and heart rate variability series as inputs, respective synthetic data models are coupled through parametrised functions defined in accordance with current central autonomic network (CAN) knowledge. We validate this concept using data from 30 healthy volunteers undergoing notable sympathetic elicitation through a cold-pressor test, and further compare the obtained results with a state-of-the-art method as maximal information coefficient. Although our findings are in agreement with previous CAN findings, we report new insights into the role of fronto-parietal region activity and lateralisation mechanisms over the temporal cortices during prolonged peripheral elicitation, which occur with specific time delays. Additionally, the afferent autonomic outflow maps to brain oscillations in the δ and γ bands, whereas complementary cortical dynamics in the θ, α, and β bands act on efferent autonomic control. The proposed framework paves the way towards novel biomarker definitions for the assessment of complex physiological networks using existing data generation models for brain and peripheral dynamics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  1. Al-Nashash, H., Y. Al-Assaf, J. Paul, and N. Thakor. EEG signal modeling using adaptive markov process amplitude. IEEE Trans. Biomed. Eng. 51:744–751, 2004.

    Article  PubMed  Google Scholar 

  2. Bashan, A., R. P. Bartsch, J. W. Kantelhardt, S. Havlin, and P. C. Ivanov. Network physiology reveals relations between network topology and physiological function. Nat. Commun. 3:702, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Beissner, F., K. Meissner, K.-J. Bär, and V. Napadow. The autonomic brain: an activation likelihood estimation meta-analysis for central processing of autonomic function. J. Neurosci. 33:10503–10511, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Benarroch, E. E. Central Autonomic Control. In: Primer on the Autonomic Nervous System (Third Edition), 2012, pp. 9–12.

    Chapter  Google Scholar 

  5. Brennan, M., M. Palaniswami, and P. Kamen. Poincare plot interpretation using a physiological model of hrv based on a network of oscillators. Am. J. Physiol. Heart Circ. Physiol. 283:H1873–H1886, 2002.

    Article  CAS  PubMed  Google Scholar 

  6. Catrambone, V., A. Greco, M. Nardelli, S. Ghiasi, N. Vanello, E. P. Scilingo, and G. Valenza. A new modelling framework to study time-varying directional brain–heart interactions: preliminary evaluations and perspectives. In: 2018 40th Annual International Conference of the IEEE Engineering in Medicine and Biology Society, pp. 4611–4614, IEEE, 2018.

  7. Chang, P. F., L. Arendt-Nielsen, and A. C. Chen. Dynamic changes and spatial correlation of eeg activities during cold pressor test in man. Brain Res. Bull. 57:667–675, 2002.

    Article  PubMed  Google Scholar 

  8. Cui, J., T. E. Wilson, and C. G. Crandall. Baroreflex modulation of muscle sympathetic nerve activity during cold pressor test in humans. Am. J. Phys. 282:H1717–H1723, 2002.

    CAS  Google Scholar 

  9. Dorrance, A. M. and G. Fink. Effects of stroke on the autonomic nervous system. Compr. Physiol. 5:1241–1263, 2015.

    Article  PubMed  Google Scholar 

  10. Esler, M. D. Mental stress, panic disorder and the heart. Stress and Health 14:237–243, 1998.

    Google Scholar 

  11. Faes, L., D. Marinazzo, F. Jurysta, and G. Nollo. Linear and non-linear brain–heart and brain–brain interactions during sleep. Physiological measurement 36:683, 2015.

    Article  CAS  PubMed  Google Scholar 

  12. Hering, D., K. Lachowska, and M. Schlaich. Role of the sympathetic nervous system in stress-mediated cardiovascular disease. Current hypertension reports 17:80, 2015.

    Article  CAS  PubMed  Google Scholar 

  13. Lin, A., K. K. Liu, R. P. Bartsch, and P. C. Ivanov. Delay-correlation landscape reveals characteristic time delays of brain rhythms and heart interactions. Phil. Trans. R. Soc. A 374:20150182, 2016.

    Article  CAS  PubMed  Google Scholar 

  14. Lovallo, W. The cold pressor test and autonomic function: a review and integration. Psychophysiology 12:268–282, 1975.

    Article  CAS  PubMed  Google Scholar 

  15. Orini, M., R. Bailón, L. T. Mainardi, P. Laguna, and P. Flandrin. Characterization of dynamic interactions between cardiovascular signals by time-frequency coherence. IEEE Trans. on Biom. Eng. 59:663–673, 2012.

    Article  Google Scholar 

  16. Peng, R.-C., W.-R. Yan, X.-L. Zhou, N.-L. Zhang, W.-H. Lin, and Y.-T. Zhang. Time-frequency analysis of heart rate variability during the cold pressor test using a time-varying autoregressive model. Physiological measurement 36:441, 2015.

    Article  PubMed  Google Scholar 

  17. Pola, S., A. Macerata, M. Emdin, and C. Marchesi. Estimation of the power spectral density in nonstationary cardiovascular time series: assessing the role of the time-frequency representations (tfr). IEEE Transactions on Biomedical Engineering 43:46, 1996.

    Article  CAS  PubMed  Google Scholar 

  18. Pyner, S. The paraventricular nucleus and heart failure. Experimental physiology 99:332–339, 2014.

    Article  CAS  PubMed  Google Scholar 

  19. Reshef, D. N., Y. A. Reshef, H. K. Finucane, S. R. Grossman, G. McVean, P. J. Turnbaugh, E. S. Lander, M. Mitzenmacher, and P. C. Sabeti. Detecting novel associations in large data sets. Science 334:1518–1524, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Schulz, S., M. Bolz, K.-J. Bär, and A. Voss. Central-and autonomic nervous system coupling in schizophrenia. Phil. Trans. R. Soc. A 374:20150178, 2016.

    Article  PubMed  Google Scholar 

  21. Schwabe, L., L. Haddad, and H. Schachinger. Hpa axis activation by a socially evaluated cold-pressor test. Psychoneuroendocrinology 33:890–895, 2008.

    Article  CAS  Google Scholar 

  22. Stankovski, T., T. Pereira, P. V. McClintock, and A. Stefanovska. Coupling functions: universal insights into dynamical interaction mechanisms. Reviews of Modern Physics 89:045001, 2017.

    Article  Google Scholar 

  23. Stankovski, T., S. Petkoski, J. Raeder, A. F. Smith, P. V. McClintock, and A. Stefanovska. Alterations in the coupling functions between cortical and cardio-respiratory oscillations due to anaesthesia with propofol and sevoflurane. Phil. Trans. R. Soc. A 374:20150186, 2016.

    Article  CAS  PubMed  Google Scholar 

  24. Stokes, P. A. and P. L. Purdon. A study of problems encountered in granger causality analysis from a neuroscience perspective. Proceedings of the National Academy of Sciences 114:E7063–E7072, 2017.

    Article  CAS  PubMed  Google Scholar 

  25. Taggart, P., H. Critchley, and P. Lambiase. Heart–brain interactions in cardiac arrhythmia. Heart 97:698-708, 2011.

    Article  CAS  PubMed  Google Scholar 

  26. Tahsili-Fahadan, P. and R. G. Geocadin. Heart–brain axis: effects of neurologic injury on cardiovascular function. Circulation research 120:559–572, 2017.

    Article  CAS  PubMed  Google Scholar 

  27. Thayer, J. F., F. Åhs, M. Fredrikson, J. J. Sollers, and T. D. Wager. A meta-analysis of heart rate variability and neuroimaging studies: implications for heart rate variability as a marker of stress and health. Neuroscience & Biobehavioral Reviews 36:747–756, 2012.

    Article  PubMed  Google Scholar 

  28. Valenza, G., A. Duggento, L. Passamonti, S. Diciotti, C. Tessa, R. Barbieri, and N. Toschi. Resting-state brain correlates of instantaneous autonomic outflow. In: Proc. of IEEE-EMBC, pp. 3325–3328. 2017.

  29. Valenza, G., A. Duggento, L. Passamonti, S. Diciotti, C. Tessa, N. Toschi, and R. Barbieri. Resting-state brain correlates of cardiovascular complexity. In: 2017 39th Annual International Conference of the IEEE Engineering in Medicine and Biology Society, pp. 3317–3320, IEEE2017.

  30. Valenza, G., A. Greco, C. Gentili, A. Lanata, L. Sebastiani, D. Menicucci, A. Gemignani, and E. Scilingo. Combining electroencephalographic activity and instantaneous heart rate for assessing brain–heart dynamics during visual emotional elicitation in healthy subjects. Phil. Trans. R. Soc. A 374:20150176, 2016.

    Article  PubMed  Google Scholar 

  31. Valenza, G., N. Toschi, and R. Barbieri. Uncovering brain–heart information through advanced signal and image processing. Phil. Trans. R. Soc. A 374, 2016.

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Vincenzo Catrambone.

Additional information

Associate Editor Joel Stitzel oversaw the review of this article.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Electronic supplementary material 1 (PDF 3032 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Catrambone, V., Greco, A., Vanello, N. et al. Time-Resolved Directional Brain–Heart Interplay Measurement Through Synthetic Data Generation Models. Ann Biomed Eng 47, 1479–1489 (2019). https://doi.org/10.1007/s10439-019-02251-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10439-019-02251-y

Keywords

Navigation