Central Autonomic Network; Heart Rate Variability; Disorders of Consciousness
Abstract :
[en] Neuroimaging studies have demonstrated functional interactions between autonomic (ANS) and brain (CNS) structures involved in higher brain functions, including attention and conscious processes. These interactions have been described by the Central Autonomic Network (CAN), a concept model based on the brain-heart two-way integrated interaction. Heart rate variability (HRV) measures proved reliable as non-invasive descriptors of the ANS-CNS function setup and are thought to reflect higher brain functions. Autonomic function, ANS-mediated responsiveness and the ANS-CNS interaction qualify as possible independent indicators for clinical functional assessment and prognosis in Disorders of Consciousness (DoC). HRV has proved helpful to investigate residual responsiveness in DoC and predict clinical recovery. Variability due to internal (e.g. homeostatic and circadian processes) and environmental factors remains a key independent variable and systematic research with this regard is warranted. The interest in bidirectional ANS-CNS interactions in a variety of physiopathological conditions is growing, however these interactions have not been extensively investigated in DoC. In this brief review we illustrate the potentiality of brain-heart investigation by means of HRV analysis in assessing patients with DoC. The authors’ opinion is that this easy, inexpensive and non-invasive approach may provide useful information in the clinical assessment of this challenging patient population.
Di Perri, Carol ; Université de Liège - ULiège > Consciousness-Coma Science Group
Prada, Valeria; University of Genoa, Italy > Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics and Maternal
Sannita, G. Walter; University of Genoa, Italy > Department of Neuroscience, Rehabilitation, Ophthalmology, Genetics
LAUREYS, Steven ; Centre Hospitalier Universitaire de Liège - CHU > Département de médecine interne > Centre intégré pluridisc. étude cerveau-cognition-conscience
Language :
English
Title :
Measures Of CNS-Autonomic Interaction And Responsiveness In Disorder Of Consciousness.
Abbate, C., Trimarchi, P. D., Basile, I., Mazzucchi, A., and Devalle, G. (2014). Sensory stimulation for patients with disorders of consciousness: from stimulation to rehabilitation. Front. Hum. Neurosci. 8:616. doi: 10.3389/fnhum.2014.00616
Akselrod, S., Gordon, D., Ubel, F. A., Shannon, D. C., Berger, A. C., and Cohen, R. J. (1981). Power spectrum analysis of heart rate fluctuation: a quantitative probe of beat-to-beat cardiovascular control. Science 213, 220–222. doi: 10.1126/science.6166045
Almeida, R., Dias, C., Silva, M. E., and Rocha, A. P. (2017). “ARFIMA-GARCH modeling of HRV: clinical application in acute brain injury,” in Complexity and Nonlinearity in Cardiovascular Signals, eds R. Barbieri, E. P. Scilingo, and G. Valenza (Cham: Springer), 451–468. doi: 10.1007/978-3-319-58709-7_17
Babo-Rebelo, M., Richter, C. G., and Tallon-Baudry, C. (2016). Neural responses to heartbeats in the default network encode the self in spontaneous thoughts. J. Neurosci. 36, 7829–7840. doi: 10.1523/JNEUROSCI.0262-16.2016
Baselli, G., Cerutti, S., Badilini, F., Biancardi, L., Porta, A., Pagani, M., et al. (1994). Model for the assessment of heart period and arterial pressure variability interactions and of respiration influences. Med. Biol. Eng. Comput. 32, 143–152. doi: 10.1007/bf02518911
Bassi, A., and Bozzali, M. (2015). Potential interactions between the autonomic nervous system and higher level functions in neurological and neuropsychiatric conditions. Front. Neurol. 6:182. doi: 10.3389/fneur.2015.00182
Batchinsky, A. I., Cancio, L. C., Salinas, J., Kuusela, T., Cooke, W. H., Wang, J. J., et al. (2007). Prehospital loss of R-to-R interval complexity is associated with mortality in trauma patients. J. Trauma 63, 512–518. doi: 10.1097/TA.0b013e318142d2f0
Bekinschtein, T., Niklison, J., Sigman, L., Manes, F., Leiguarda, R., Armony, J., et al. (2004). Emotion processing in the minimally conscious state. J. Neurol. Neurosurg. Psychiatry 75, 788–788. doi: 10.1136/jnnp.2003.034876
Bekinschtein, T. A., Golombek, D. A., Simonetta, S. H., Coleman, M. R., and Manes, F. F. (2009). Circadian rhythms in the vegetative state. Brain Inj. 23, 915–919. doi: 10.1080/02699050903283197
Bekinschtein, T. A., Manes, F. F., Villarreal, M., Owen, A. M., and Della Maggiore, V. (2011). Functional imaging reveals movement preparatory activity in the vegetative state. Front. Hum. Neurosci. 5:5. doi: 10.3389/fnhum.2011.00005
Benarroch, E. E. (2007a). Enteric nervous system Functional organization and neurologic implications. Neurology 69, 1953–1957. doi: 10.1212/01.wnl.0000281999.56102.b5
Benarroch, E. E. (2007b). The autonomic nervous system: basic anatomy and physiology. Contin. Lifelong Learn. Neurol. 13, 13–32. doi: 10.1212/01.CON.0000299964.20642.9a
Berne, C., Fagius, J., Pollare, T., and Hjemdahl, P. (1992). The sympathetic response to euglycaemic hyperinsulinaemia. Diabetologia 35, 873–879. doi: 10.1007/BF00399935
Berntson, G. G., and Cacioppo, J. T. (2004). “Heart rate variability: stress and psychiatric conditions,” in Dynamic Electrocardiography, eds M. Malik and A. J. Camm (New York, NY: Blackwell/Futura), 57–64.
Berntson, G. G., Cacioppo, J. T., and Grossman, P. (2007). Whither vagal tone. Biol. Psychol. 74, 295–300. doi: 10.1016/j.biopsycho.2006.08.006
Bilan, A., Witczak, A., Palusiński, R., Myśliński, W., and Hanzlik, J. (2005). Circadian rhythm of spectral indices of heart rate variability in healthy subjects. J. Electrocardiol. 38, 239–243. doi: 10.1016/j.jelectrocard.2005.01.012
Biswas, A. K., Scott, W. A., Sommerauer, J. F., and Luckett, P. M. (2000). Heart rate variability after acute traumatic brain injury in children. Crit. Care Med. 28, 3907–3912. doi: 10.1097/00003246-200012000-00030
Blume, C., Lechinger, J., Santhi, N., del Giudice, R, Gnjezda, M. T., Pichler, G., et al. (2017). Significance of circadian rhythms in severely brain-injured patients: A clue to consciousness? Neurology 88, 1933–1941. doi: 10.1212/WNL.0000000000003942
Boly, M., Faymonville, M.-E., Schnakers, C., Peigneux, P., Lambermont, B., Phillips, C., et al. (2008). Perception of pain in the minimally conscious state with PET activation: an observational study. Lancet Neurol. 7, 1013–1020. doi: 10.1016/S1474-4422(08)70219-9
Boudreau, P., Dumont, G., Kin, N. M., Walker, C.-D., and Boivin, D. B. (2011). Correlation of heart rate variability and circadian markers in humans. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2011, 681–682.
Boudreau, P., Yeh, W. H., Dumont, G. A., and Boivin, D. B. (2012). A circadian rhythm in heart rate variability contributes to the increased cardiac sympathovagal response to awakening in the morning. Chronobiol. Int. 29, 757–768. doi: 10.3109/07420528.2012.674592
Bruno, M.-A., Vanhaudenhuyse, A., Schnakers, C., Boly, M., Gosseries, O., Demertzi, A., et al. (2010). Visual fixation in the vegetative state: an observational case series PET study. BMC Neurol. 10:35. doi: 10.1186/1471-2377-10-35
Bullock, T. H. (1970). The reliability of neurons. J. Gen. Physiol. 55, 565–584. doi: 10.1085/jgp.55.5.565
Burr, R. L. (2007). Interpretation of normalized spectral heart rate variability indices in sleep research: a critical review. Sleep 30, 913–919. doi: 10.1093/sleep/30.7.913
Calabrò, R. S., Naro, A., Manuli, A., Leo, A., Luca, R. D., Buono, V. L., et al. (2017). Pain perception in patients with chronic disorders of consciousness: What can limbic system tell us? Clin. Neurophysiol. 128, 454–462. doi: 10.1016/j.clinph.2016.12.011
Candelieri, A., Cortese, M. D., Dolce, G., Riganello, F., and Sannita, W. G. (2011). Visual pursuit: within-day variability in the severe disorder of consciousness. J. Neurotrauma 28, 2013–2017. doi: 10.1089/neu.2011.1885
Carney, R. M., Blumenthal, J. A., Freedland, K. E., Stein, P. K., Howells, W. B., Berkman, L. F., et al. (2005). Low heart rate variability and the effect of depression on post–myocardial infarction mortality. Arch. Intern. Med. 165, 1486–1491. doi: 10.1001/archinte.165.13.1486
Celesia, G. G. (2013). Conscious awareness in patients in vegetative states: myth or reality? Curr. Neurol. Neurosci. Rep. 13:395. doi: 10.1007/s11910-013-0395-7
Celesia, G. G., and Sannita, W. G. (2013). Can patients in vegetative state experience pain and have conscious awareness? Neurology 80, 328–329. doi: 10.1212/WNL.0b013e31827f0928
Cerutti, S. (1995). Spectral Analysis of the Heart Rate Variability Signal. Available at: https://ci.nii.ac.jp/naid/10014992161/ (accessed November 25, 2018).
Chen, Z., Venkat, P., Seyfried, D., Chopp, M., Yan, T., and Chen, J. (2017). Brain–Heart Interaction. Circ. Res. 121, 451–468. doi: 10.1161/CIRCRESAHA.117.311170
Chennu, S., Annen, J., Wannez, S., Thibaut, A., Chatelle, C., Cassol, H., et al. (2017). Brain networks predict metabolism, diagnosis and prognosis at the bedside in disorders of consciousness. Brain 140, 2120–2132. doi: 10.1093/brain/awx163
Claydon, V. E., and Krassioukov, A. V. (2008). Clinical correlates of frequency analyses of cardiovascular control after spinal cord injury. Am. J. Physiol. Heart Circ. Physiol. 294, H668–H678. doi: 10.1152/ajpheart.00869.2007
Cobos, M. I., Guerra, P. M., Vila, J., and Chica, A. B. (2019). Heart-rate modulations reveal attention and consciousness interactions: COBOS ET AL. Psychophysiology 56, e13295. doi: 10.1111/psyp.13295
Critchley, H. D. (2009). Psychophysiology of neural, cognitive and affective integration: fMRI and autonomic indicants. Int. J. Psychophysiol. 73, 88–94. doi: 10.1016/j.ijpsycho.2009.01.012
Crone, J. S., Bio, B. J., Vespa, P. M., Lutkenhoff, E. S., and Monti, M. M. (2017). Restoration of thalamo-cortical connectivity after brain injury: recovery of consciousness, complex behavior, or passage of time? J. Neurosci. Res. 96, 671–687. doi: 10.1002/jnr.24115
de Lartigue, G. (2014). Putative roles of neuropeptides in vagal afferent signaling. Physiol. Behav. 0, 155–169. doi: 10.1016/j.physbeh.2014.03.011
de Morree, H. M., Szabó, B. M., Rutten, G.-J., and Kop, W. J. (2013). Central nervous system involvement in the autonomic responses to psychological distress. Neth. Heart J. 21, 64–69. doi: 10.1007/s12471-012-0351-1
deBoer, R. W., Karemaker, J. M., and Strackee, J. (1987). Hemodynamic fluctuations and baroreflex sensitivity in humans: a beat-to-beat model. Am. J. Physiol. 253, H680–H689. doi: 10.1152/ajpheart.1987.253.3.H680
DeGiorgio, C. M., Miller, P., Meymandi, S., Chin, A., Epps, J., Gordon, S., et al. (2010). RMSSD, a measure of heart rate variability, is associated with risk factors for sudep: the SUDEP-7 inventory. Epilepsy Behav. 19, 78–81. doi: 10.1016/j.yebeh.2010.06.011
Demertzi, A., Antonopoulos, G., Heine, L., Voss, H. U., Crone, J. S., de Los Angeles, C., et al. (2015). Intrinsic functional connectivity differentiates minimally conscious from unresponsive patients. Brain 138, 2619–2631. doi: 10.1093/brain/awv169
Di Perri, C., Bahri, M. A., Amico, E., Thibaut, A., Heine, L., Antonopoulos, G., et al. (2016). Neural correlates of consciousness in patients who have emerged from a minimally conscious state: a cross-sectional multimodal imaging study. Lancet Neurol. 15, 830–842. doi: 10.1016/S1474-4422(16)00111-3
Di Perri, C., Bastianello, S., Bartsch, A. J., Pistarini, C., Maggioni, G., Magrassi, L., et al. (2013). Limbic hyperconnectivity in the vegetative state. Neurology 81, 1417–1424. doi: 10.1212/WNL.0b013e3182a43b78
Doehner, W., Ural, D., Haeusler, K. G., Čelutkienė, J., Bestetti, R., Cavusoglu, Y., et al. (2018). Heart and brain interaction in patients with heart failure: overview and proposal for a taxonomy. A position paper from the Study Group on Heart and Brain Interaction of the Heart Failure Association. Eur. J. Heart Fail. 20, 199–215. doi: 10.1002/ejhf.1100
Duclos, C., Dumont, M., Arbour, C., Paquet, J., Blais, H., Menon, D. K., et al. (2017). Parallel recovery of consciousness and sleep in acute traumatic brain injury. Neurology 88, 268–275. doi: 10.1212/WNL.0000000000003508
Ernst, G. (2017). Heart-rate variability—more than heart beats? Front. Public Health 5:240. doi: 10.3389/fpubh.2017.00240
Esler, M. (1993). Clinical application of noradrenaline spillover methodology: delineation of regional human sympathetic nervous responses. Pharmacol. Toxicol. 73, 243–253. doi: 10.1111/j.1600-0773.1993.tb00579.x
Faes, L., Nollo, G., Jurysta, F., and Marinazzo, D. (2014). Information dynamics of brain–heart physiological networks during sleep. New J. Phys. 16:105005. doi: 10.1088/1367-2630/16/10/105005
Friedman, B. H. (2007). An autonomic flexibility–neurovisceral integration model of anxiety and cardiac vagal tone. Biol. Psychol. 74, 185–199. doi: 10.1016/j.biopsycho.2005.08.009
Gao, L., Smielewski, P., Czosnyka, M., and Ercole, A. (2016). Cerebrovascular signal complexity six hours after intensive care unit admission correlates with outcome after severe traumatic brain injury. J. Neurotrauma 33, 2011–2018. doi: 10.1089/neu.2015.4228
Garan, H. (2009). Heart rate variability in acute myocardial infarction. Cardiology 114, 273–274. doi: 10.1159/000235567
Garbarino, S., Lanteri, P., Feeling, N. R., Jarczok, M. N., Quintana, D. S., Koenig, J., et al. (2019). Circadian rhythms, sleep, and the autonomic nervous system: a position paper. J. Psychophysiol. doi: 10.1027/0269-8803/a000236
Garbarino, S., Nobili, L., and Costa, G. (eds) (2014). Sleepiness and Human Impact Assessment. Basel: Springer.
Garbarino, S., and Sannita, W. G. (2015). DoC: a pathophysiological continuum with high variabiity? Neurology. doi: 10.13140/RG.2.1.1541.0006
Giacino, J. T., Kalmar, K., and Whyte, J. (2004). The JFK coma recovery scale-revised: measurement characteristics and diagnostic utility. Arch. Phys. Med. Rehabil. 85, 2020–2029. doi: 10.1016/j.apmr.2004.02.033
Goldstein, B., DeKing, D., DeLong, D. J., Kempski, M. H., Cox, C., Kelly, M. M., et al. (1993). Autonomic cardiovascular state after severe brain injury and brain death in children. Crit. Care Med. 21, 228–233.
Goldstein, B., Fiser, D. H., Kelly, M. M., Mickelsen, D., Ruttimann, U., and Pollack, M. M. (1998). Decomplexification in critical illness and injury: relationship between heart rate variability, severity of illness, and outcome. Crit. Care Med. 26, 352–357. doi: 10.1097/00003246-199802000-00040
Grimm, T., and Kreutz, G. (2018). Music interventions in disorders of consciousness (DOC) – a systematic review. Brain Inj. 32, 704–714. doi: 10.1080/02699052.2018.1451657
Gutiérrez, J., Machado, C., Estévez, M., Olivares, A., Hernández, H., Perez, J., et al. (2010). Heart rate variability changes induced by auditory stimulation in persistent vegetative state. Int. J. Disabil. Hum. Dev. 9, 357–362. doi: 10.1515/IJDHD.2010.041
Hagemann, D., Waldstein, S. R., and Thayer, J. F. (2003). Central and autonomic nervous system integration in emotion. Brain Cogn. 52, 79–87. doi: 10.1016/S0278-2626(03)00011-3
Hendén, P. L., Söndergaard, S., Rydenhag, B., Reinsfelt, B., Ricksten, S.-E., and Aneman, A. (2014). Can baroreflex sensitivity and heart rate variability predict late neurological outcome in patients with traumatic brain injury? J. Neurosurg. Anesthesiol. 26, 50–59. doi: 10.1097/ANA.0b013e3182a47b62
Keren, O., Yupatov, S., Radai, M. M., Elad-Yarum, R., Faraggi, D., Abboud, S., et al. (2005). Heart rate variability (HRV) of patients with traumatic brain injury (TBI) during the post-insult sub-acute period. Brain Inj. 19, 605–611. doi: 10.1080/02699050400024946
Kim, S. W., Jeon, H. R., Kim, J. Y., and Kim, Y. (2017). Heart rate variability among children with acquired brain injury. Ann. Rehabil. Med. 41, 951–960. doi: 10.5535/arm.2017.41.6.951
King, D. R., Ogilvie, M. P., Pereira, B. M., Chang, Y., Manning, R. J., Conner, J. A., et al. (2009). Heart rate variability as a triage tool in patients with trauma during prehospital helicopter transport. J. Trauma 67, 436–440. doi: 10.1097/TA.0b013e3181ad67de
Kiryachkov, Y., Shelkunova, I., Shelkunova, I. G., Kolesov, D. L., and Danilec, V. V. (2017). MON-P025: association between heart rate variability measures and energy homeostasis in patients with vegetative status: a prospective clinical cohort pilot study. Clin. Nutr. 36:S188.
Lane, R., Mcrae, K., Reiman, E., Chen, K., Ahern, G., and Thayer, J. (2009). Neural correlates of heart rate variability during emotion. Neuroimage 44, 213–222. doi: 10.1016/j.neuroimage.2008.07.056
Laureys, S., Celesia, G. G., Cohadon, F., Lavrijsen, J., León-Carrión, J., Sannita, W. G., et al. (2010). Unresponsive wakefulness syndrome: a new name for the vegetative state or apallic syndrome. BMC Med. 8:68. doi: 10.1186/1741-7015-8-68
Laureys, S., Faymonville, M.-E., Luxen, A., Lamy, M., Franck, G., and Maquet, P. (2000). Restoration of thalamocortical connectivity after recovery from persistent vegetative state. Lancet 355, 1790–1791. doi: 10.1016/s0140-6736(00)02271-6
Laureys, S., Faymonville, M. E., Peigneux, P., Damas, P., Lambermont, B., Del Fiore, G., et al. (2002). Cortical processing of noxious somatosensory stimuli in the persistent vegetative state. Neuroimage 17, 732–741. doi: 10.1006/nimg.2002.1236
Laureys, S., Perrin, F., and Brédart, S. (2007). Self-consciousness in non-communicative patients. Conscious. Cogn. 16, 722–741. doi: 10.1016/j.concog.2007.04.004
Lee, Y.-C., Lei, C.-Y., Shih, Y.-S., Zhang, W.-C., Wang, H.-M., Tseng, C.-L., et al. (2011). “HRV response of vegetative state patient with music therapy,” in Proceedings of the Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Boston, MA, 1701–1704. doi: 10.1109/IEMBS.2011.6090488
Lehrer, P., and Eddie, D. (2013). Dynamic processes in regulation and some implications for biofeedback and biobehavioral interventions. Appl. Psychophysiol. Biofeedback 38, 143–155. doi: 10.1007/s10484-013-9217-6
Lehrer, P. M. (2007). Biofeedback training to increase heart rate variability. Princ. Pract. Stress Manag. 3, 227–248.
Machado, C., Korein, J., Aubert, E., Bosch, J., Alvarez, M. A., Rodríguez, R., et al. (2007). Recognizing a Mother’s voice in the persistent vegetative state. Clin. EEG Neurosci. 38, 124–126. doi: 10.1177/155005940703800306
Majerus, S., Bruno, M.-A., Schnakers, C., Giacino, J. T., and Laureys, S. (2009). “The problem of aphasia in the assessment of consciousness in brain-damaged patients,” in Progress in Brain Research, ed. S. Laureys, N. D. Schiff, and A. M. Owen (Amsterdam: Elsevier), 49–61. doi: 10.1016/s0079-6123(09)17705-1
Malliani, A. (1995). Association of heart rate variability components with physiological regulatory mechanisms. Heart Rate Var. 8, 202–242.
Marino, S., Bonanno, L., Ciurleo, R., Baglieri, A., Morabito, R., Guerrera, S., et al. (2017). Functional evaluation of awareness in vegetative and minimally conscious state. Open Neuroimaging J. 11, 17–25. doi: 10.2174/1874440001711010017
Montano, N., Ruscone, T. G., Porta, A., Lombardi, F., Pagani, M., and Malliani, A. (1994). Power spectrum analysis of heart rate variability to assess the changes in sympathovagal balance during graded orthostatic tilt. Circulation 90, 1826–1831. doi: 10.1161/01.cir.90.4.1826
Monti, M. M. (2012). Cognition in the vegetative state. Annu. Rev. Clin. Psychol 8, 431–454. doi: 10.1146/annurev-clinpsy-032511-143050
Monti, M. M., Rosenberg, M., Finoia, P., Kamau, E., Pickard, J. D., and Owen, A. M. (2014). Thalamo-frontal connectivity mediates top-down cognitive functions in disorders of consciousness. Neurology 84, 167–173. doi: 10.1212/WNL.0000000000001123
Monti, M. M., and Sannita, W. G. (eds) (2016). Brain Function and Responsiveness in Disorders of Consciousness. Berlin: Springer.
Morris, J. A., Norris, P. R., Ozdas, A., Waitman, L. R., Harrell, F. E., Williams, A. E., et al. (2006). Reduced heart rate variability: an indicator of cardiac uncoupling and diminished physiologic reserve in 1,425 trauma patients. J. Trauma 60, 1165–1173. doi: 10.1097/01.ta.0000220384.04978.3b
Mowery, N. T., Norris, P. R., Riordan, W., Jenkins, J. M., Williams, A. E., and Morris, J. A. (2008). Cardiac uncoupling and heart rate variability are associated with intracranial hypertension and mortality: a study of 145 trauma patients with continuous monitoring. J. Trauma 65, 621–627. doi: 10.1097/TA.0b013e3181837980
Nait-Ali, A. (2009). Advanced Biosignal Processing. Berlin: Springer.
Napadow, V., Dhond, R., Conti, G., Makris, N., Brown, E. N., and Barbieri, R. (2008). Brain correlates of autonomic modulation: combining heart rate variability with fMRI. Neuroimage 42, 169–177. doi: 10.1016/j.neuroimage.2008.04.238
Naro, A., Leo, A., Bramanti, P., and Calabrò, R. S. (2015). Moving toward conscious pain processing detection in chronic disorders of consciousness: anterior cingulate cortex neuromodulation. J. Pain 16, 1022–1031. doi: 10.1016/j.jpain.2015.06.014
Norris, P. R., Anderson, S. M., Jenkins, J. M., Williams, A. E., and Morris, J. A. (2008a). Heart rate multiscale entropy at three hours predicts hospital mortality in 3,154 trauma patients. Shock 30, 17–22. doi: 10.1097/SHK.0b013e318164e4d0
Norris, P. R., Stein, P. K., and Morris, J. A. (2008b). Reduced heart rate multiscale entropy predicts death in critical illness: a study of physiologic complexity in 285 trauma patients. J. Crit. Care 23, 399–405. doi: 10.1016/j.jcrc.2007.08.001
Norris, P. R., Ozdas, A., Cao, H., Williams, A. E., Harrell, F. E., Jenkins, J. M., et al. (2006). Cardiac uncoupling and heart rate variability stratify ICU patients by mortality: a study of 2088 trauma patients. Ann. Surg. 243, 804–812.
O’Kelly, J., and Magee, W. L. (2013). Music therapy with disorders of consciousness and neuroscience: the need for dialogue. Nord. J. Music Ther. 22, 93–106. doi: 10.1080/08098131.2012.709269
Owen, A. M. (2014). Disorders of consciousness: diagnostic accuracy of brain imaging in the vegetative state. Nat. Rev. Neurol. 10, 370–371. doi: 10.1038/nrneurol.2014.102
Owen, A. M., Coleman, M. R., Boly, M., Davis, M. H., Laureys, S., and Pickard, J. D. (2006). Detecting awareness in the vegetative state. Science 313, 1402–1402. doi: 10.1126/science.1130197
Pagani, M., Lombardi, F., Guzzetti, S., Sandrone, G., Rimoldi, O., Malfatto, G., et al. (1984). Power spectral density of heart rate variability as an index of sympatho-vagal interaction in normal and hypertensive subjects. J. Hypertens. Suppl. 2, S383–S385.
Papaioannou, V., Giannakou, M., Maglaveras, N., Sofianos, E., and Giala, M. (2008). Investigation of heart rate and blood pressure variability, baroreflex sensitivity, and approximate entropy in acute brain injury patients. J. Crit. Care 23, 380–386. doi: 10.1016/j.jcrc.2007.04.006
Papaioannou, V. E., Maglaveras, N., Houvarda, I., Antoniadou, E., and Vretzakis, G. (2006). Investigation of altered heart rate variability, nonlinear properties of heart rate signals, and organ dysfunction longitudinally over time in intensive care unit patients. J. Crit. Care 21, 95–103. doi: 10.1016/j.jcrc.2005.12.007
Pistoia, F., Sacco, S., Stewart, J., Sarà, M., Carolei, A., Pistoia, F., et al. (2016). Disorders of consciousness: painless or painful conditions?—Evidence from neuroimaging studies. Brain Sci. 6:E47. doi: 10.3390/brainsci6040047
Rajendra Acharya, U., Paul Joseph, K., Kannathal, N., Lim, C. M., and Suri, J. S. (2006). Heart rate variability: a review. Med. Biol. Eng. Comput. 44, 1031–1051. doi: 10.1007/s11517-006-0119-0
Rapenne, T., Moreau, D., Lenfant, F., Vernet, M., Boggio, V., Cottin, Y., et al. (2001). Could heart rate variability predict outcome in patients with severe head injury? A pilot study. J. Neurosurg. Anesthesiol. 13, 260–268. doi: 10.1097/00008506-200107000-00016
Riganello, F. (2016). “Responsiveness and the autonomic control–CNS two-way interaction in disorders of consciousness,” in Brain Function and Responsiveness in Disorders of Consciousness, eds M. M. Monti and W. G. Sannita (Cham: Springer), 145–155. doi: 10.1007/978-3-319-21425-2_11
Riganello, F., Candelieri, A., Quintieri, M., Conforti, D., and Dolce, G. (2010). Heart rate variability: an index of brain processing in vegetative state? An artificial intelligence, data mining study. Clin. Neurophysiol. 121, 2024–2034. doi: 10.1016/j.clinph.2010.05.010
Riganello, F., Chatelle, C., Schnakers, C., and Laureys, S. (2018a). Heart Rate Variability as an indicator of nociceptive pain in disorders of consciousness? J. Pain Symptom Manage. 57, 47–56. doi: 10.1016/j.jpainsymman.2018.09.016
Riganello, F., Cortese, M. D., Arcuri, F., Dolce, G., Lucca, L. F., and Sannita, W. G. (2015a). Autonomic nervous system functional state, neuro-rehabiliation, and outcome in disorders of consciousness. J. Neurotrauma 32, 1071–1077.
Riganello, F., Cortese, M. D., Arcuri, F., Quintieri, M., and Dolce, G. (2015b). How Can music influence the autonomic nervous system response in patients with severe disorder of consciousness? Front. Neurosci. 9:461. doi: 10.3389/fnins.2015.00461
Riganello, F., Cortese, M. D., Dolce, G., Lucca, L. F., and Sannita, W. G. (2015c). The autonomic system functional state predicts responsiveness in DOC. J. Neurotrauma 32, 1071–1077. doi: 10.1089/neu.2014.3539
Riganello, F., Cortese, M. D., Dolce, G., and Sannita, W. G. (2013). Visual pursuit response in the severe disorder of consciousness: modulation by the central autonomic system and a predictive model. BMC Neurol. 13:164. doi: 10.1186/1471-2377-13-164
Riganello, F., Dolce, G., and Sannita, W. (2012a). Heart rate variability and the central autonomic network in the severe disorder of consciousness. J. Rehabil. Med. 44, 495–501. doi: 10.2340/16501977-0975
Riganello, F., Garbarino, S., and Sannita, W. G. (2012b). Heart rate variability, homeostasis, and brain function: a tutorial and review of application. J. Psychophysiol. 26, 178–203. doi: 10.1027/0269-8803/a000080
Riganello, F., Garbarino, S., and Sannita, W. G. (2014). Heart rate variability and the two-way interaction between CNS and the central autonomic network. J. Exp. Clin. Cardiol. 20, 5584–5595.
Riganello, F., Larroque, S. K., Bahri, M. A., Heine, L., Martial, C., Carrière, M., et al. (2018b). 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. Front. Neurol 9:769. doi: 10.3389/fneur.2018.00769
Riganello, F., Macri, S., Alleva, E., Petrini, C., Soddu, A., Leòn-Carriòn, J., et al. (2016). Pain perception in unresponsive wakefulness syndrome may challenge the interruption of artificial nutrition and hydration: neuroethics in action. Front. Neurol. 7:202. doi: 10.3389/fneur.2016.00202
Ruiz Vargas, E., Sörös, P., Shoemaker, J. K., and Hachinski, V. (2016). Human cerebral circuitry related to cardiac control: a neuroimaging meta-analysis: cardiac control. Ann. Neurol. 79, 709–716. doi: 10.1002/ana.24642
Ryan, M. L., Thorson, C. M., Otero, C. A., Vu, T., and Proctor, K. G. (2011). Clinical applications of heart rate variability in the triage and assessment of traumatically injured patients. Anesthesiol. Res. Pract. 2011:e416590. doi: 10.1155/2011/416590
Sannita, W. G. (2006). Individual variability, end-point effects and possible biases in electrophysiological research. Clin. Neurophysiol. 117, 2569–2583. doi: 10.1016/j.clinph.2006.04.026
Sannita, W. G. (2014). Human brain physiology investigated in the disorder of consciousness. Front. Neurol. 5:211. doi: 10.3389/fneur.2014.00211
Sannita, W. G. (2015). Responsiveness in DoC and individual variability. Front. Hum. Neurosci. 9:270. doi: 10.3389/fnhum.2015.00270
Saper, C. B. (2002). The central autonomic nervous system: conscious visceral perception and autonomic pattern generation. Annu. Rev. Neurosci. 25, 433–469. doi: 10.1146/annurev.neuro.25.032502.111311
Sarà, M., Sebastiano, F., Sacco, S., Pistoia, F., Onorati, P., Albertini, G., et al. (2008). Heart rate non linear dynamics in patients with persistent vegetative state: a preliminary report. Brain Inj. 22, 33–37. doi: 10.1080/02699050701810670
Shaffer, F., McCraty, R., and Zerr, C. L. (2014). A healthy heart is not a metronome: an integrative review of the heart’s anatomy and heart rate variability. Front Psychol. 5:1040. doi: 10.3389/fpsyg.2014.01040
Shen, D., Cui, L., Shen, Z., Garbarino, S., Sannita, W. G., and Stevens, R. D. (2016). Resting brain activity in disorders of consciousness: a systematic review and meta-analysis. Neurology 84, 1272–1280.
Shi, H., Yang, L., Zhao, L., Su, Z., Mao, X., Zhang, L., et al. (2017). Differences of heart rate variability between happiness and sadness emotion states: a pilot study. J. Med. Biol. Eng. 37, 527–539. doi: 10.1007/s40846-017-0238-0
Soddu, A., and Bassetti, C. L. (2017). A good sleep for a fresh mind in patients with acute traumatic brain injury. Neurology 88, 226–227. doi: 10.1212/WNL.0000000000003529
Soddu, A., Gómez, F., Heine, L., Di Perri, C., Bahri, M. A., Voss, H. U., et al. (2015). Correlation between resting state fMRI total neuronal activity and PET metabolism in healthy controls and patients with disorders of consciousness. Brain Behav. 6:e00424. doi: 10.1002/brb3.424
Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology (1996). Heart rate variability: standards of measurement, physiological interpretation and clinical use. Circulation 93, 1043–1065. doi: 10.1161/01.cir.93.5.1043
Thayer, J. F., Åhs, F., Fredrikson, M., Sollers, J. J., and Wager, T. D. (2012). A meta-analysis of heart rate variability and neuroimaging studies: implications for heart rate variability as a marker of stress and health. Neurosci. Biobehav. Rev. 36, 747–756. doi: 10.1016/j.neubiorev.2011.11.009
Thayer, J. F., and Lane, R. D. (2000). A model of neurovisceral integration in emotion regulation and dysregulation. J. Affect. Disord. 61, 201–216. doi: 10.1016/s0165-0327(00)00338-4
Thayer, J. F., and Lane, R. D. (2009). Claude Bernard and the heart–brain connection: further elaboration of a model of neurovisceral integration. Neurosci. Biobehav. Rev. 33, 81–88. doi: 10.1016/j.neubiorev.2008.08.004
Thayer, J. F., and Sternberg, E. (2006). Beyond heart rate variability. Ann. N. Y. Acad. Sci. 1088, 361–372. doi: 10.1196/annals.1366.014
Thome, J., Densmore, M., Frewen, P. A., McKinnon, M. C., Théberge, J., Nicholson, A. A., et al. (2017). Desynchronization of autonomic response and central autonomic network connectivity in posttraumatic stress disorder: CAN Connectivity and HRV in PTSD. Hum. Brain Mapp. 38, 27–40. doi: 10.1002/hbm.23340
Tobaldini, E., Toschi-Dias, E., Trimarchi, P. D., Brena, N., Comanducci, A., Casarotto, S., et al. (2018). Cardiac autonomic responses to nociceptive stimuli in patients with chronic disorders of consciousness. Clin. Neurophysiol. 129, 1083–1089. doi: 10.1016/j.clinph.2018.01.068
Tonhajzerova, I., Ondrejka, I., Turianikova, Z., Javorka, K., Calkovska, A., and Javorka, M. (2012). “Heart rate variability: an index of the brain–heart interaction,” in Tachycardia, ed. T. Yamad (Rijeka: Intech), 185–202.
Valenza, G., Duggento, A., Passamonti, L., Diciotti, S., Tessa, C., Barbieri, R., et al. (2017). “Resting-state brain correlates of instantaneous autonomic outflow,” in Proceedings of the 39th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC), (Seogwipo: IEEE), 3325–3328.
Vaschillo, E. G., Vaschillo, B., Pandina, R. J., and Bates, M. E. (2011). Resonances in the cardiovascular system caused by rhythmical muscle tension: rhythmical muscle tension and resonance. Psychophysiology 48, 927–936. doi: 10.1111/j.1469-8986.2010.01156.x
Wallin, B. G., and Charkoudian, N. (2007). Sympathetic neural control of integrated cardiovascular function: insights from measurement of human sympathetic nerve activity. Muscle Nerve 36, 595–614. doi: 10.1002/mus.20831
Weir, J., Steyerberg, E. W., Butcher, I., Lu, J., Lingsma, H. F., McHugh, G. S., et al. (2012). Does the extended glasgow outcome scale add value to the conventional Glasgow outcome scale? J. Neurotrauma 29, 53–58. doi: 10.1089/neu.2011.2137
Wijnen, V. J., Heutink, M., van Boxtel, G. J., Eilander, H. J., and de Gelder, B. (2006). Autonomic reactivity to sensory stimulation is related to consciousness level after severe traumatic brain injury. Clin. Neurophysiol. 117, 1794–1807. doi: 10.1016/j.clinph.2006.03.006
Winchell, R. J., and Hoyt, D. B. (1997). Analysis of heart-rate variability: a noninvasive predictor of death and poor outcome in patients with severe head injury. J. Trauma Acute Care Surg. 43, 927–933. doi: 10.1097/00005373-199712000-00010
Yentes, J. M., Hunt, N., Schmid, K. K., Kaipust, J. P., McGrath, D., and Stergiou, N. (2013). The appropriate use of approximate entropy and sample entropy with short data sets. Ann. Biomed. Eng. 41, 349–365. doi: 10.1007/s10439-012-0668-3