Dynamic coupling between the central and autonomic cardiac nervous systems in patients with refractory epilepsy: A pilot study

The heart and brain are reciprocally interconnected and engage in two-way communication for homeostatic regulation. Epilepsy is considered a network disease that also affects the autonomic nervous system (ANS). The neurovisceral integration model (NVM) proposes that cardiac vagal tone, indexed by he...

Full description

Bibliographic Details
Main Authors: Eline Melo, José Fiel, Rodrigo Milhomens, Thaynara Ribeiro, Raphael Navegantes, Francinaldo Gomes, Bruno Duarte Gomes, Antonio Pereira
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-08-01
Series:Frontiers in Neurology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fneur.2022.904052/full
_version_ 1798037909356412928
author Eline Melo
José Fiel
Rodrigo Milhomens
Thaynara Ribeiro
Raphael Navegantes
Francinaldo Gomes
Bruno Duarte Gomes
Bruno Duarte Gomes
Antonio Pereira
Antonio Pereira
Antonio Pereira
author_facet Eline Melo
José Fiel
Rodrigo Milhomens
Thaynara Ribeiro
Raphael Navegantes
Francinaldo Gomes
Bruno Duarte Gomes
Bruno Duarte Gomes
Antonio Pereira
Antonio Pereira
Antonio Pereira
author_sort Eline Melo
collection DOAJ
description The heart and brain are reciprocally interconnected and engage in two-way communication for homeostatic regulation. Epilepsy is considered a network disease that also affects the autonomic nervous system (ANS). The neurovisceral integration model (NVM) proposes that cardiac vagal tone, indexed by heart rate variability (HRV), can indicate the functional integrity of cognitive neural networks. ANS activity and the pattern of oscillatory EEG activity covary during the transition of arousal states and associations between cortical and autonomic activity are reflected by HRV. Cognitive dysfunction is one of the common comorbidities that occur in epilepsy, including memory, attention, and processing difficulties. Recent studies have shown evidence for the active involvement of alpha activity in cognitive processes through its active role in the control of neural excitability in the cortex through top-down modulation of cortical networks. In the present pilot study, we evaluated the association between resting EEG oscillatory behavior and ANS function in patients with refractory epilepsy. Our results show: (1) In patients with refractory epilepsy, there is a strong positive correlation between HRV and the power of cortical oscillatory cortical activity in all studied EEG bands (delta, theta, alpha, and beta) in all regions of interest in both hemispheres, the opposite pattern found in controls which had low or negative correlation between these variables; (2) higher heartbeat evoked potential amplitudes in patients with refractory epilepsy than in controls. Taken together, these results point to a significant alteration in heart-brain interaction in patients with refractory epilepsy.
first_indexed 2024-04-11T21:33:00Z
format Article
id doaj.art-6517ce77041b412ea0d9243de060cc98
institution Directory Open Access Journal
issn 1664-2295
language English
last_indexed 2024-04-11T21:33:00Z
publishDate 2022-08-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Neurology
spelling doaj.art-6517ce77041b412ea0d9243de060cc982022-12-22T04:01:52ZengFrontiers Media S.A.Frontiers in Neurology1664-22952022-08-011310.3389/fneur.2022.904052904052Dynamic coupling between the central and autonomic cardiac nervous systems in patients with refractory epilepsy: A pilot studyEline Melo0José Fiel1Rodrigo Milhomens2Thaynara Ribeiro3Raphael Navegantes4Francinaldo Gomes5Bruno Duarte Gomes6Bruno Duarte Gomes7Antonio Pereira8Antonio Pereira9Antonio Pereira10Graduate Program in Neuroscience and Cell Biology, Federal University of Pará, Belém, BrazilGraduate Program in Electrical Engineering, Federal University of Pará, Belém, BrazilDepartment of Electrical and Biomedical Engineering, Institute of Technology, Belém, BrazilDepartment of Electrical and Biomedical Engineering, Institute of Technology, Belém, BrazilGraduate Program in Electrical Engineering, Federal University of Pará, Belém, BrazilHospital Ophir Loyola, Belém, BrazilGraduate Program in Neuroscience and Cell Biology, Federal University of Pará, Belém, BrazilDepartment of Biotechnology, Institute of Biological Sciences, Federal University of Pará, Belém, BrazilGraduate Program in Neuroscience and Cell Biology, Federal University of Pará, Belém, BrazilGraduate Program in Electrical Engineering, Federal University of Pará, Belém, BrazilDepartment of Electrical and Biomedical Engineering, Institute of Technology, Belém, BrazilThe heart and brain are reciprocally interconnected and engage in two-way communication for homeostatic regulation. Epilepsy is considered a network disease that also affects the autonomic nervous system (ANS). The neurovisceral integration model (NVM) proposes that cardiac vagal tone, indexed by heart rate variability (HRV), can indicate the functional integrity of cognitive neural networks. ANS activity and the pattern of oscillatory EEG activity covary during the transition of arousal states and associations between cortical and autonomic activity are reflected by HRV. Cognitive dysfunction is one of the common comorbidities that occur in epilepsy, including memory, attention, and processing difficulties. Recent studies have shown evidence for the active involvement of alpha activity in cognitive processes through its active role in the control of neural excitability in the cortex through top-down modulation of cortical networks. In the present pilot study, we evaluated the association between resting EEG oscillatory behavior and ANS function in patients with refractory epilepsy. Our results show: (1) In patients with refractory epilepsy, there is a strong positive correlation between HRV and the power of cortical oscillatory cortical activity in all studied EEG bands (delta, theta, alpha, and beta) in all regions of interest in both hemispheres, the opposite pattern found in controls which had low or negative correlation between these variables; (2) higher heartbeat evoked potential amplitudes in patients with refractory epilepsy than in controls. Taken together, these results point to a significant alteration in heart-brain interaction in patients with refractory epilepsy.https://www.frontiersin.org/articles/10.3389/fneur.2022.904052/fullrefractory epilepsyheart rate variability (HRV)EEGheartbeat evoked potentialautonomic nervous system (ANS)
spellingShingle Eline Melo
José Fiel
Rodrigo Milhomens
Thaynara Ribeiro
Raphael Navegantes
Francinaldo Gomes
Bruno Duarte Gomes
Bruno Duarte Gomes
Antonio Pereira
Antonio Pereira
Antonio Pereira
Dynamic coupling between the central and autonomic cardiac nervous systems in patients with refractory epilepsy: A pilot study
Frontiers in Neurology
refractory epilepsy
heart rate variability (HRV)
EEG
heartbeat evoked potential
autonomic nervous system (ANS)
title Dynamic coupling between the central and autonomic cardiac nervous systems in patients with refractory epilepsy: A pilot study
title_full Dynamic coupling between the central and autonomic cardiac nervous systems in patients with refractory epilepsy: A pilot study
title_fullStr Dynamic coupling between the central and autonomic cardiac nervous systems in patients with refractory epilepsy: A pilot study
title_full_unstemmed Dynamic coupling between the central and autonomic cardiac nervous systems in patients with refractory epilepsy: A pilot study
title_short Dynamic coupling between the central and autonomic cardiac nervous systems in patients with refractory epilepsy: A pilot study
title_sort dynamic coupling between the central and autonomic cardiac nervous systems in patients with refractory epilepsy a pilot study
topic refractory epilepsy
heart rate variability (HRV)
EEG
heartbeat evoked potential
autonomic nervous system (ANS)
url https://www.frontiersin.org/articles/10.3389/fneur.2022.904052/full
work_keys_str_mv AT elinemelo dynamiccouplingbetweenthecentralandautonomiccardiacnervoussystemsinpatientswithrefractoryepilepsyapilotstudy
AT josefiel dynamiccouplingbetweenthecentralandautonomiccardiacnervoussystemsinpatientswithrefractoryepilepsyapilotstudy
AT rodrigomilhomens dynamiccouplingbetweenthecentralandautonomiccardiacnervoussystemsinpatientswithrefractoryepilepsyapilotstudy
AT thaynararibeiro dynamiccouplingbetweenthecentralandautonomiccardiacnervoussystemsinpatientswithrefractoryepilepsyapilotstudy
AT raphaelnavegantes dynamiccouplingbetweenthecentralandautonomiccardiacnervoussystemsinpatientswithrefractoryepilepsyapilotstudy
AT francinaldogomes dynamiccouplingbetweenthecentralandautonomiccardiacnervoussystemsinpatientswithrefractoryepilepsyapilotstudy
AT brunoduartegomes dynamiccouplingbetweenthecentralandautonomiccardiacnervoussystemsinpatientswithrefractoryepilepsyapilotstudy
AT brunoduartegomes dynamiccouplingbetweenthecentralandautonomiccardiacnervoussystemsinpatientswithrefractoryepilepsyapilotstudy
AT antoniopereira dynamiccouplingbetweenthecentralandautonomiccardiacnervoussystemsinpatientswithrefractoryepilepsyapilotstudy
AT antoniopereira dynamiccouplingbetweenthecentralandautonomiccardiacnervoussystemsinpatientswithrefractoryepilepsyapilotstudy
AT antoniopereira dynamiccouplingbetweenthecentralandautonomiccardiacnervoussystemsinpatientswithrefractoryepilepsyapilotstudy