Neural control of the heart: Recent concepts and clinical correlations

Palma, Jose-Alberto; Benarroch, Eduardo E.

doi:10.1212/wnl.0000000000000605

Cited by 237Heart Rate Variability and Autonomic ControlCardiac electrophysiology and arrhythmiasNeuroscience of respiration and sleep

Neural control of the heart: Recent concepts and clinical correlations

Palma, Jose-Alberto, Benarroch, Eduardo E.·2014·Neurology

DOI 10.1212/wnl.0000000000000605

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Abstract

Areas distributed throughout the neuraxis, including the anterior insula, anterior cingulate cortex (ACC), amygdala, hypothalamus, periaqueductal gray matter, parabrachial nucleus, and several regions of the medulla, exert a beat-to-beat control on cardiac function. These areas are critically involved in emotional behavior, stress responses, and homeostatic reflexes and exert their influence on heart rate (HR) and cardiac contractility via the sympathetic and parasympathetic nervous systems. Over the past several years, advances in neuroanatomical, neurophysiologic, and functional imaging studies have provided insight into the central and peripheral mechanisms of neural control of cardiac function in humans. Whereas some issues, such as lateralization of this central control, remain unresolved, the adverse cardiac consequences of a wide variety of neurologic disorders emphasize the need to better understand the functional anatomy and neurochemical mechanisms of the neural control of the heart. Important examples are severe arrhythmias and myocardial injury in the setting of neurologic catastrophes and sudden unexplained death in epilepsy. This review will focus on some of the current experimental and clinical information related to these relevant issues for the neurologist.

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Impact of Sleep on Arrhythmogenesis
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Electrocardiographic Changes During Electrographic Seizures
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Funny Current and Cardiac Rhythm: Insights from HCN Knockout and Transgenic Mouse Models
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Heart rate variability - a potential early marker of sub-acute post-stroke infections
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Involvement of the dorsomedial hypothalamus and the nucleus tractus solitarii in chronic cardiovascular changes associated with anxiety in rats
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Clinical Importance of Cardiac Troponin Release and Cardiac Abnormalities in Patients With Supratentorial Cerebral Hemorrhages
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Cardiovascular manifestations of autonomic epilepsy
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Apical Ballooning Resulting from Limbic Encephalitis
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Cardiac autonomic impairment during sleep is linked with disease severity in Parkinson’s disease
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Ictal Modulation of Cardiac Repolarization, but Not of Heart Rate, Is Lateralized in Mesial Temporal Lobe Epilepsy
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Hypocretin-1 (orexin A) prevents the effects of hypoxia/hypercapnia and enhances the GABAergic pathway from the lateral paragigantocellular nucleus to cardiac vagal neurons in the nucleus ambiguus
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Tako-tsubo cardiomyopathy in a patient with bilateral lesions in the dorsal medulla
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Controlling Parasympathetic Regulation of Heart Rate: A Gatekeeper Role for RGS Proteins in the Sinoatrial Node
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Chronotropic and dromotropic responses to localized glutamate microinjections in the rat nucleus ambiguus
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Cardiac Electrophysiology and the Athlete
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Cardiac autonomic impairment during sleep as a marker of human prion diseases: A preliminary report
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Post-Stroke Cardiovascular Complications and Neurogenic Cardiac Injury
Sposato, L. A., Hilz, M. J., Aspberg, S., Murthy, S. B., Bahit, M. C., Hsieh, C., Sheppard, M. N., & Scheitz, J. F. (2020) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2020.10.009 · Cited by 328 · see citing works
Stroke-heart syndrome: clinical presentation and underlying mechanisms
Scheitz, J. F., Nolte, C. H., Doehner, W., Hachinski, V., & Endres, M. (2018) · The Lancet Neurology · doi:10.1016/s1474-4422(18)30336-3 · Cited by 319 · see citing works
Advances in Photopletysmography Signal Analysis for Biomedical Applications
Moraes, J. L., Rocha, M. X., Vasconcelos, G. G., Vasconcelos Filho, J. E., De Albuquerque, V. H. C., & Alexandria, A. R. (2018) · Sensors · doi:10.3390/s18061894 · Cited by 292 · see citing works
Heart–Brain Axis: Effects of Neurologic Injury on Cardiovascular Function
Tahsili-Fahadan, P., & Geocadin, R. G. (2017) · Circulation Research · doi:10.1161/circresaha.116.308446 · Cited by 291 · see citing works
Publication guidelines for human heart rate and heart rate variability studies in psychophysiology—Part 1: Physiological underpinnings and foundations of measurement
Quigley, K. S., Gianaros, P. J., Norman, G. J., Jennings, J. R., Berntson, G. G., & de Geus, E. J. C. (2024) · Psychophysiology · doi:10.1111/psyp.14604 · Cited by 253 · see citing works
The Investigation of the Cardiovascular and Sudomotor Autonomic Nervous System—A Review
Ziemssen, T., & Siepmann, T. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.00053 · Cited by 176 · see citing works
Cardiovascular and autonomic reactivity to psychological stress: Neurophysiological substrates and links to cardiovascular disease
Ginty, A. T., Kraynak, T. E., Fisher, J. P., & Gianaros, P. J. (2017) · Autonomic Neuroscience · doi:10.1016/j.autneu.2017.03.003 · Cited by 168 · see citing works
Autonomic Modulation for Cardiovascular Disease
Hadaya, J. E., & Ardell, J. L. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.617459 · Cited by 145 · see citing works
Conscious processing of narrative stimuli synchronizes heart rate between individuals
Pérez, P., Madsen, J., Banellis, L., Türker, B., Raimondo, F., Perlbarg, V., Valente, M., Niérat, M.-C., Puybasset, L., Naccache, L., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109692 · Cited by 139 · see citing works
Stroke in right dorsal anterior insular cortex Is related to myocardial injury
Krause, T., Werner, K., Fiebach, J., Villringer, K., Piper, S., Haeusler, K., Endres, M., Scheitz, J., & Nolte, C. (2017) · Annals of Neurology · doi:10.1002/ana.24906 · Cited by 128 · see citing works
Heart rate variability in bipolar disorder: A systematic review and meta-analysis
Faurholt‐Jepsen, M., Kessing, L. V., & Munkholm, K. (2016) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2016.12.007 · Cited by 120 · see citing works
Takotsubo Syndrome Associated With Structural Brain Alterations of the Limbic System
Hiestand, T., Hänggi, J., Klein, C., Topka, M., Jaguszewski, M. J., Ghadri, J. R., Lüscher, T. F., Jäncke, L., & Templin, C. (2018) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2017.12.022 · Cited by 120 · see citing works
Cardiovascular autonomic dysfunctions and sleep disorders
Buonaura, G. C., Provini, F., Guaraldi, P., Plazzi, G., & Cortelli, P. (2015) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2015.05.005 · Cited by 120 · see citing works
Autonomic and Brain Morphological Predictors of Stress Resilience
Carnevali, L., Koenig, J., Sgoifo, A., & Ottaviani, C. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00228 · Cited by 117 · see citing works
Autonomic manifestations of epilepsy: emerging pathways to sudden death?
Thijs, R. D., Ryvlin, P., & Surges, R. (2021) · Nature Reviews Neurology · doi:10.1038/s41582-021-00574-w · Cited by 111 · see citing works
Molecularly defined circuits for cardiovascular and cardiopulmonary control
Veerakumar, A., Yung, A. R., Liu, Y., & Krasnow, M. A. (2022) · Nature · doi:10.1038/s41586-022-04760-8 · Cited by 110 · see citing works
Brain-heart axis--Review Article.
Manea, M. M., Comsa, M., Mincă, A., Dragoș, D., & Popa, C. (2015) · Europe PMC (PubMed Central) · Cited by 90 · see citing works
Cardiovascular Dysfunction in Multiple Sclerosis
Kaplan, T., Berkowitz, A. L., & Samuels, M. A. (2015) · The Neurologist · doi:10.1097/nrl.0000000000000064 · Cited by 87 · see citing works
Asymmetry and Heterogeneity: Part and Parcel in Cardiac Autonomic Innervation and Function
Zandstra, T. E., Notenboom, R. G. E., Wink, J., Kiès, P., Vliegen, H. W., Egorova, A. D., Schalij, M. J., de Ruiter, M. C., & Jongbloed, M. R. M. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.665298 · Cited by 83 · see citing works
Association of Resting Heart Rate and Blood Pressure in Late Adolescence With Subsequent Mental Disorders: A Longitudinal Population Study of More Than 1 Million Men in Sweden
Latvala, A., Kuja-Halkola, R., Rück, C., D’Onofrio, B. M., Jernberg, T., Almqvist, C., Mataix-Cols, D., Larsson, H., & Lichtenstein, P. (2016) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2016.2717 · Cited by 82 · see citing works
Heart rate variability interventions for concussion and rehabilitation
Conder, R. L., & Conder, A. A. (2014) · Frontiers in Psychology · doi:10.3389/fpsyg.2014.00890 · Cited by 82 · see citing works
Human adult cardiac autonomic innervation: Controversies in anatomical knowledge and relevance for cardiac neuromodulation
Wink, J., van Delft, R., Notenboom, R. G. E., Wouters, P. F., DeRuiter, M. C., Plevier, J. W. M., & Jongbloed, M. R. M. (2020) · Autonomic Neuroscience · doi:10.1016/j.autneu.2020.102674 · Cited by 79 · see citing works
Distinct Neural Circuits Control Rhythm Inhibition and Spitting by the Myogenic Pharynx of C. elegans
Bhatla, N., Droste, R., Sando, S. R., Huang, A., & Horvitz, H. R. (2015) · Current Biology · doi:10.1016/j.cub.2015.06.052 · Cited by 71 · see citing works
A heartbeat away from consciousness: heart rate variability entropy can discriminate disorders of consciousness and is correlated with resting-state fMRI brain connectivity of the central autonomic network
Riganello, F., Larroque, S. K., Bahri, M. A., Heine, L., Martial, C., Carrière, M., Charland-Verville, V., Aubinet, C., Vanhaudenhuyse, A., Chatelle, C., et al. (2018) · Frontiers in Neurology · doi:10.3389/fneur.2018.00769 · Cited by 70 · see citing works
Noninvasive neuromodulation of subregions of the human insula differentially affect pain processing and heart-rate variability: a within-subjects pseudo-randomized trial
Legon, W., Strohman, A., In, A., & Payne, B. (2024) · Pain · doi:10.1097/j.pain.0000000000003171 · Cited by 69 · see citing works
Heart–brain axis in health and disease: role of innate and adaptive immunity
Simats, A., Sager, H. B., & Liesz, A. (2024) · Cardiovascular Research · doi:10.1093/cvr/cvae185 · Cited by 66 · see citing works
Blood Pressure in Seizures and Epilepsy
Nass, R. D., Hampel, K. G., Elger, C. E., & Surges, R. (2019) · Frontiers in Neurology · doi:10.3389/fneur.2019.00501 · Cited by 64 · see citing works
Identifying patients with epilepsy at high risk of cardiac death: signs, risk factors and initial management of high risk of cardiac death
Surges, R., Shmuely, S., Dietze, C. S., Ryvlin, P., & Thijs, R. D. (2021) · Epileptic Disorders · doi:10.1684/epd.2021.1254 · Cited by 63 · see citing works
Circadian rhythms of cardiovascular autonomic function: Physiology and clinical implications in neurodegenerative diseases
Baschieri, F., & Cortelli, P. (2019) · Autonomic Neuroscience · doi:10.1016/j.autneu.2019.01.009 · Cited by 61 · see citing works
Distinguishing pain from nociception, salience, and arousal: How autonomic nervous system activity can improve neuroimaging tests of specificity
Lee, I., Necka, E. A., & Atlas, L. Y. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.116254 · Cited by 58 · see citing works
Sinus Tachycardia: a Multidisciplinary Expert Focused Review
Mayuga, K. A., Fedorowski, A., Ricci, F., Gopinathannair, R., Dukes, J. W., Gibbons, C., Hanna, P., Sorajja, D., Chung, M., Benditt, D., et al. (2022) · Circulation: Arrhythmia and Electrophysiology · doi:10.1161/circep.121.007960 · Cited by 59 · see citing works
Valsalva maneuver unveils central baroreflex dysfunction with altered blood pressure control in persons with a history of mild traumatic brain injury
Hilz, M. J., Liu, M., Koehn, J., Wang, R., Ammon, F., Flanagan, S. R., & Hösl, K. M. (2016) · BMC Neurology · doi:10.1186/s12883-016-0584-5 · Cited by 59 · see citing works
Takotsubo Syndrome – Predictable from brain imaging data
Klein, C., Hiestand, T., Ghadri, J. R., Templin, C., Jäncke, L., & Hänggi, J. (2017) · Scientific Reports · doi:10.1038/s41598-017-05592-7 · Cited by 55 · see citing works
Effects of Thoracic Epidural Anesthesia on Neuronal Cardiac Regulation and Cardiac Function
Wink, J., Veering, B. T., Aarts, L. P. H. J., & Wouters, P. F. (2019) · Anesthesiology · doi:10.1097/aln.0000000000002558 · Cited by 55 · see citing works
Cortical thickness and resting‐state cardiac function across the lifespan: A cross‐sectional pooled mega‐analysis
Koenig, J., Abler, B., Agartz, I., Åkerstedt, T., Andreassen, O. A., Anthony, M., Bär, K., Bertsch, K., Brown, R. C., Brunner, R. M., et al. (2020) · Psychophysiology · doi:10.1111/psyp.13688 · Cited by 53 · see citing works
Cardiac autonomic innervation
Jamali, H. K., Waqar, F., & Gerson, M. C. (2016) · Journal of Nuclear Cardiology · doi:10.1007/s12350-016-0725-7 · Cited by 53 · see citing works
Seizure‐related modulation of systemic arterial blood pressure in focal epilepsy
Hampel, K. G., Jahanbekam, A., Elger, C. E., & Surges, R. (2016) · Epilepsia · doi:10.1111/epi.13504 · Cited by 52 · see citing works
Auricular transcutaneous vagus nerve stimulation modulates the heart-evoked potential
Poppa, T., Benschop, L., Horczak, P., Vanderhasselt, M., Carrette, E., Bechara, A., Baeken, C., & Vonck, K. E. J. (2021) · Brain stimulation · doi:10.1016/j.brs.2021.12.004 · Cited by 50 · see citing works
Uncovering brain–heart information through advanced signal and image processing
Valenza, G., Toschi, N., & Barbieri, R. (2016) · Philosophical Transactions of the Royal Society A Mathematical Physical and Engineering Sciences · doi:10.1098/rsta.2016.0020 · Cited by 49 · see citing works
Cardiovascular autonomic dysfunction after stroke
Jiménez‐Ruiz, A., Racosta, J. M., Kimpinski, K., Hilz, M. J., & Sposato, L. A. (2021) · Neurological Sciences · doi:10.1007/s10072-021-05128-y · Cited by 52 · see citing works
Cardiac Vulnerability to Cerebrogenic Stress as a Possible Cause of Troponin Elevation in Stroke
Ahn, S., Kim, Y., Shin, C., Lee, J. S., Kim, B. J., Kim, Y. J., Noh, S., Kim, S. M., Kang, H., Kang, D., et al. (2016) · Journal of the American Heart Association · doi:10.1161/jaha.116.004135 · Cited by 47 · see citing works
Machine learning in biosignals processing for mental health: A narrative review
Sajno, E., Bartolotta, S., Tuena, C., Cipresso, P., Pedroli, E., & Riva, G. (2023) · Frontiers in Psychology · doi:10.3389/fpsyg.2022.1066317 · Cited by 50 · see citing works
Prognostic Significance of Troponin Elevation for Long-Term Mortality after Ischemic Stroke
Ahn, S., Lee, J. S., Kim, Y., Kim, B. J., Kim, Y. J., Kang, D., Kim, J. S., & Kwon, S. U. (2017) · Journal of Stroke · doi:10.5853/jos.2016.01942 · Cited by 46 · see citing works
Recurrence risk of ictal asystole in epilepsy
Hampel, K. G., Thijs, R. D., Elger, C. E., & Surges, R. (2017) · Neurology · doi:10.1212/wnl.0000000000004266 · Cited by 44 · see citing works
Understanding the heart-brain axis response in COVID-19 patients: A suggestive perspective for therapeutic development
Lionetti, V., Bollini, S., Coppini, R., Gerbino, A., Ghigo, A., Iaccarino, G., Madonna, R., Mangiacapra, F., Miragoli, M., Moccia, F. D., et al. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2021.105581 · Cited by 44 · see citing works
The association between individual differences in executive functioning and resting high-frequency heart rate variability
Williams, P. G., Cribbet, M. R., Tinajero, R., Rau, H. K., Thayer, J. F., & Suchy, Y. (2019) · Biological Psychology · doi:10.1016/j.biopsycho.2019.107772 · Cited by 41 · see citing works
Autonomic Nervous System Function in Anorexia Nervosa: A Systematic Review
Jenkins, Z., Eikelis, N., Phillipou, A., Castle, D. J., Wilding, H., & Lambert, É. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.682208 · Cited by 42 · see citing works
Brain functional connectivity is altered in patients with Takotsubo Syndrome
Silva, R., Magalhães, R. J. D. S., Arantes, C., Moreira, P. S., Rodrigues, M., Marques, P., Marques, J. H. S., Sousa, N., & Pereira, V. (2019) · Scientific Reports · doi:10.1038/s41598-019-40695-3 · Cited by 39 · see citing works
Interictal Heart Rate Variability Analysis Reveals Lateralization of Cardiac Autonomic Control in Temporal Lobe Epilepsy
Dono, F., Evangelista, G., Frazzini, V., Vollono, C., Carrarini, C., Russo, M., Ferrante, C., Stefano, V. D., Marchionno, L., Angelis, M. D. D., et al. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.00842 · Cited by 34 · see citing works
Autonomic dysfunction and treatment strategies in intracerebral hemorrhage
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Authors: Palma, J.-A., & Benarroch, E. E.
Affiliations: Mayo Clinic (US)
ORCID: Palma, Jose-Alberto
Benarroch, Eduardo E.
Venue: Neurology
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2014-07-15
Volume: 83
Issue: 3
Pages: 261-271
ISSN: 0028-3878 (ISSN-L)
1526-632X
DOI: 10.1212/wnl.0000000000000605
OpenAlex: W2074959430
Cited by: 237
References: 130
Citations by year: 2026: 15 · 2025: 21 · 2024: 35 · 2023: 29 · 2022: 20 · 2021: 26 · 2020: 18 · 2019: 20 · 2018: 16 · 2017: 14 · 2016: 13 · 2015: 9 · 2014: 1
FWCI: 1.99
Type: journal article
Language: en
Open access: closed
Locations: Neurology (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac electrophysiology and arrhythmias
Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroscience of respiration and sleep
Keywords: cardiac autonomic regulation, heart rate, cardiac contractility, sympathetic nervous system, parasympathetic nervous system, anterior insula, anterior cingulate cortex, amygdala, hypothalamus, periaqueductal gray, parabrachial nucleus, medulla, emotional behavior, stress response, cardiac arrhythmias, myocardial injury, neurological disorders
MeSH terms: Autonomic Nervous System, Brain, Heart, Heart Diseases, Humans, Nervous System Diseases

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Neural control of the heart: Recent concepts and clinical correlations

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