The Trace Conditional Learning of the Noxious Stimulus in UWS Patients and Its Prognostic Value in a GSR and HRV Entropy Study

Cortese, Daniela; Riganello, Francesco; Arcuri, Francesco; Lucca, Lucia Francesca; Tonin, Paolo; Schnakers, Caroline; Laureys, Steven

doi:10.3389/fnhum.2020.00097

Article (Scientific journals)

The Trace Conditional Learning of the Noxious Stimulus in UWS Patients and Its Prognostic Value in a GSR and HRV Entropy Study

Cortese, Daniela; Riganello, Francesco; Arcuri, Francesco et al.

2020 • In Frontiers in Human Neuroscience, 14

Peer Reviewed verified by ORBi

Permalink
https://hdl.handle.net/2268/249248

DOI
10.3389/fnhum.2020.00097

Files (1)Send to Details Statistics Bibliography Similar publications

Files

Full Text

Cortese_Trace_2020.pdf

Publisher postprint (1.06 MB)

Download

All documents in ORBi are protected by a user license.

Send to

RIS BibTex APA Chicago Permalink X Linkedin

Details

Keywords :

Galvanic Skin Response (GSR); HRV (heart rate variability)

Abstract :

[en] The assessment of the consciousness level of Unresponsive Wakefulness Syndrome (UWS) patients often depends on a subjective interpretation of the observed spontaneous and volitional behavior. To date, the misdiagnosis level is around 30%. The aim of this study was to observe the behavior of UWS patients, during the administration of noxious stimulation by a Trace Conditioning protocol, assessed by the Galvanic Skin Response (GSR) and Heart Rate Variability (HRV) entropy. We recruited 13 Healthy Control (HC) and 30 UWS patients at 31 ± 9 days from the acute event evaluated by Coma Recovery Scale–Revised (CRS-R) and Nociception Coma Scale (NCS). Two different stimuli [musical stimulus (MUS) and nociceptive stimulus (NOC)], preceded, respectively by two different tones, were administered following the sequences (A) MUS1 – NOC1 – MUS2 – MUS3 – NOC2 – MUS4 – NOC3 – NOC*, and (B) MUS1*, NOC1*, NOC2*, MUS2*, NOC3*, MUS3*, NOC4*, MUS4*. All the (*) indicate the only tones administration. CRS-R and NCS assessments were repeated for three consecutive weeks. MUS4, NOC3, and NOC* were compared for GSR wave peak magnitude, time to reach the peak, and time of wave's decay by Wilcoxon's test to assess the Conditioned Response (CR). The Sample Entropy (SampEn) was recorded in baseline and both sequences. Machine Learning approach was used to identify a rule to discriminate the CR. The GSR magnitude of CR was higher comparing music stimulus (p < 0.0001) and CR extinction (p < 0.002) in nine patients and in HC. Patients with CR showed a higher SampEn in sequence A compared to patients without CR. Within the third and fourth weeks from protocol administration, eight of the nine patients (88.9%) evolved into MCS. The Machine-learning showed a high performance to differentiate presence/absence of CR (≥95%). The possibility to observe the CR to the noxious stimulus, by means of the GSR and SampEn, can represent a potential method to reduce the misdiagnosis in UWS patients. © Copyright © 2020 Cortese, Riganello, Arcuri, Lucca, Tonin, Schnakers and Laureys.

Research center :

CHU de Liège-Centre du Cerveau² - ULiège

Disciplines :

Neurosciences & behavior

Author, co-author :

Cortese, Daniela; Research in Advanced NeuroRehabilitation, Istituto Sant'Anna, Crotone, Italy

Riganello, Francesco; Research in Advanced NeuroRehabilitation, Istituto Sant'Anna, Crotone, Italy, Coma Science Group, GIGA-Consciousness, University Hospital of Liege, Liege, Belgium

Arcuri, Francesco; Research in Advanced NeuroRehabilitation, Istituto Sant'Anna, Crotone, Italy

Lucca, Lucia Francesca; Research in Advanced NeuroRehabilitation, Istituto Sant'Anna, Crotone, Italy

Tonin, Paolo; Research in Advanced NeuroRehabilitation, Istituto Sant'Anna, Crotone, Italy

Schnakers, Caroline; Neurosurgery Department, University of California, Los Angeles, Los Angeles, CA, United States, Research Institute, Casa Colina Hospital and Centers of Healthcare, Pomona, CA, United States

Laureys, Steven ; Université de Liège - ULiège > GIGA Consciousness-Coma Science Group

Language :

English

Title :

The Trace Conditional Learning of the Noxious Stimulus in UWS Patients and Its Prognostic Value in a GSR and HRV Entropy Study

Publication date :

2020

Journal title :

Frontiers in Human Neuroscience

eISSN :

1662-5161

Publisher :

Frontiers Media S.A.

Volume :

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 06 July 2020

Statistics

Number of views

49 (3 by ULiège)

Number of downloads

63 (2 by ULiège)

More statistics

Scopus citations^®

Scopus citations^®
without self-citations

OpenCitations

Bibliography

Andrews K., Murphy L., Munday R., Littlewood C., (1996). Misdiagnosis of the vegetative state: retrospective study in a rehabilitation unit. BMJ 313, 13–16. 10.1136/bmj.313.7048.138664760
Arunodaya G. R., Taly A. B., (1995). Sympathetic skin response: a decade later. J. Neurol. Sci. 129, 81–89. 10.1016/0022-510X(94)00265-P7608740
Arzi A., Shedlesky L., Ben-Shaul M., Nasser K., Oksenberg A., Hairston I. S., et al. (2012). Humans can learn new information during sleep. Nat. Neurosci. 15, 1460–1465. 10.1038/nn.319322922782
Baba M., Watahiki Y., Matsunaga M., Takebe K., (1988). Sympathetic skin response in healthy man. Electromyogr. Clin. Neurophysiol. 28, 277–283.3191879
Bayne T., Hohwy J., Owen A. M., (2016). Are there levels of consciousness? Trends Cogn. Sci. 20, 405–413. 10.1016/j.tics.2016.03.00927101880
Bekinschtein T. A., Shalom D. E., Forcato C., Herrera M., Coleman M. R., Manes F. F., et al. (2009). Classical conditioning in the vegetative and minimally conscious state. Nat. Neurosci. 12, 1343–1349. 10.1038/nn.239119767746
Benedek M., (2016). Analysis of EDA Using Ledalab. Available online at: http://www.ledalab.de/download/Analysis%20of%20EDA%20data%20using%20Ledalab.pdf
Blain S., Power S. D., Sejdic E., Mihailidis A., Chau T., (2010). A cardiorespiratory classifier of voluntary and involuntary electrodermal activity. BioMed. Eng. Online 9:11. 10.1186/1475-925X-9-1120184746
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. 10.1016/S1474-4422(08)70219-918835749
Bosco A., Lancioni G. E., Belardinelli M. O., Singh N. N., O'Reilly M. F., Sigafoos J., (2010). Vegetative state: efforts to curb misdiagnosis. Cogn. Process. 11, 87–90. 10.1007/s10339-009-0355-y20043186
Breska A., Maoz K., Ben-Shakhar G., (2011). Interstimulus intervals for skin conductance response measurement. Psychophysiology 48, 437–440. 10.1111/j.1469-8986.2010.01084.x20701710
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. 10.1016/j.clinph.2016.12.01128160751
Candelieri A., Cortese M. D., Dolce G., Riganello F., Sannita W. G., (2011). Visual pursuit: within-day variability in the severe disorder of consciousness. J. Neurotrauma 28, 2013–2017. 10.1089/neu.2011.188521770758
Çevik M. Ö., (2014). Habituation, sensitization, and pavlovian conditioning. Front. Integr. Neurosci. 8:13. 10.3389/fnint.2014.0001324574983
Chatelle C., Hauger S. L., Martial C., Becker F., Eifert B., Boering D., et al. (2018). Assessment of nociception and pain in participants in an unresponsive or minimally conscious state after acquired brain injury: the relation between the coma recovery scale–revised and the nociception coma scale–revised. Arch. Phys. Med. Rehabil. 99, 1755–1762. 10.1016/j.apmr.2018.03.00929653106
Chatelle C., Laureys S., (2015). Assessing Pain and Communication in Disorders of consciousness. New York, NY: Psychology Press. 10.4324/9781315747200
Chatelle C., Thibaut A., (2014). Pain issues in disorders of consciousness. Brain Inj. 28, 1202–1208. 10.3109/02699052.2014.92051825099024
Chatelle C., Thibaut A., Bruno M-A., Boly M., Bernard C., Hustinx R., et al. (2014). Nociception coma scale-revised scores correlate with metabolism in the anterior cingulate cortex. Neurorehabil. Neural Repair 28, 149–152. 10.1177/154596831350322024065132
Clark R. E., (1998). Classical conditioning and brain systems: the role of awareness. Science 280, 77–81. 10.1126/science.280.5360.779525860
Coghill R. C., McHaffie J. G., Yen Y-F., (2003). Neural correlates of interindividual differences in the subjective experience of pain. Proc. Natl. Acad. Sci. U.S.A. 100, 8538–8542. 10.1073/pnas.143068410012824463
Corrales M. M., de la Cruz T., Esquivel A. G., Antonio M., Salazar G., Orellana J. N., (2012). Normal values of heart rate variability at rest in a young, healthy and active Mexican population. Health 4, 377–385. 10.4236/health.2012.47060
Cortese M. D., Riganello F., Arcuri F., Pugliese M. E., Lucca L. F., Giuliano D., et al. (2014). Coma recovery scale-r: variability in the disorder of consciousness. BMC Neurol. 15:186. 10.1186/s12883-015-0455-526450569
Costa M., Goldberger A., (2015). Generalized multiscale entropy analysis: application to quantifying the complex volatility of human heartbeat time series. Entropy 17, 1197–1203. 10.3390/e1703119727099455
Costa M., Goldberger A. L., Peng C-K., (2005). Multiscale entropy analysis of biological signals. Phys. Rev. E Stat. Nonlin. Soft. Matter Phys. 71:021906. 10.1103/PhysRevE.71.02190615783351
Critchley H. D., (2002). Book review: electrodermal responses: what happens in the brain. Neuroscientist 8, 132–142. 10.1177/107385840200800209
Critchley H. D., Mathias C. J., Josephs O., O'Doherty J., Zanini S., Dewar B-K., et al. (2003). Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. Brain 126, 2139–2152. 10.1093/brain/awg21612821513
Cruse D., Monti M. M., Owen A. M., (2011). Neuroimaging in disorders of consciousness: contributions to diagnosis and prognosis. Future Neurol. 6, 291–299. 10.2217/fnl.10.87
Dawson M. E., Schell A. M., Filion D. L., (2007). “The electrodermal system,” in Handbook of Psychophysiology, eds J. T. Cacioppo, L. G. Tassinary, and G. G. Berntson (New York, NY: Cambridge University Press), 159–181. 10.1017/CBO9780511546396.007
de Tommaso M., Navarro J., Lanzillotti C., Ricci K., Buonocunto F., Livrea P., et al. (2015). Cortical responses to salient nociceptive and not nociceptive stimuli in vegetative and minimal conscious state. Front. Hum. Neurosci. 9:17. 10.3389/fnhum.2015.00017
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. 10.1093/brain/awv16926117367
Demertzi A., Ledoux D., Bruno M-A., Vanhaudenhuyse A., Gosseries O., Soddu A., et al. (2011). Attitudes towards end-of-life issues in disorders of consciousness: a European survey. J. Neurol. 258, 1058–1065. 10.1007/s00415-010-5882-z21221625
Di Perri C., Heine L., Amico E., Soddu A., Laureys S., Demertzi A., (2014). Technology-based assessment in patients with disorders of consciousness. Ann. Ist. Super. Sanita 50, 209–220. 10.4415/ANN_14_03_0325292268
Dolce G., Riganello F., Quintieri M., Candelieri A., Conforti D., (2008). Personal interaction in the vegetative state: a data-mining study. J. Psychophysiol. 22, 150–156. 10.1027/0269-8803.22.3.150
Dolce G., Sannita W. G., European Task Force on the the vegetative state. (2010). The vegetative state: a syndrome seeking revision? Brain Inj. 24, 1628–1629. 10.3109/02699052.2010.52305521058901
Eelen P., (2018). Classical conditioning: classical yet modern. Psychol. Belg. 58, 196–211. 10.5334/pb.45130479817
Elie B., Guiheneuc P., (1990). Sympathetic skin response: normal results in different experimental conditions. Electroencephalogr. Clin. Neurophysiol. 76, 258–267. 10.1016/0013-4694(90)90020-K1697257
Erkkinen M. G., Kim M-O., Geschwind M. D., (2018). Clinical neurology and epidemiology of the major neurodegenerative diseases. Cold Spring Harb. Perspect. Biol. 10:a033118. 10.1101/cshperspect.a03311828716886
Fernández-Espejo D., Owen A. M., (2013). Detecting awareness after severe brain injury. Nat. Rev. Neurosci. 14, 801–809. 10.1038/nrn360824088810
Fins J. J., (2005). Clinical pragmatism and the care of brain damaged patients: toward a palliative neuroethics for disorders of consciousness. Prog. Brain Res. 150, 565–582. 10.1016/S0079-6123(05)50040-216186050
Freedman L. W., Scerbo A. S., Dawson M. E., Raine A., McClure W. O., Venables P. H., (1994). The relationship of sweat gland count to electrodermal activity. Psychophysiology 31, 196–200. 10.1111/j.1469-8986.1994.tb01040.x8153256
Fritz C. O., Morris P. E., Richler J. J., (2012). Effect size estimates: current use, calculations, and interpretation. J. Exp. Psychol. 141, 2–18. 10.1037/a002433821823805
Fujimori B., (1956). Studies on the galvanic skin response using the current-and potential method. Jpn. J. Physiol. 5, 394–405. 10.2170/jjphysiol.5.39413318787
Gantner I. S., Bodart O., Laureys S., Demertzi A., (2012). Our rapidly changing understanding of acute and chronic disorders of consciousness: challenges for neurologists. Future Neurol. 8, 43–54. 10.2217/fnl.12.77
Garcia-Larrea L., Bastuji H., (2018). Pain and consciousness. Prog. Neuropsychopharmacol. Biol. Psychiatry 87, 193–199. 10.1016/j.pnpbp.2017.10.00729031510
Giacino J. T., Ashwal S., Childs N., Cranford R., Jennett B., Katz D. I., et al. (2002). The minimally conscious state definition and diagnostic criteria. Neurology 58, 349–353. 10.1212/WNL.58.3.34911839831
Giacino J. T., Kalmar K., Whyte J., (2004). The JFK coma recovery scale-revised: measurement characteristics and diagnostic utility. Arch. Phys. Med. Rehabil. 85, 2020–2029. 10.1016/j.apmr.2004.02.03315605342
Gitler A. D., Dhillon P., Shorter J., (2017). Neurodegenerative disease: models, mechanisms, and a new hope. Dis. Model Mech. 10, 499–502. 10.1242/dmm.03020528468935
Havsteen I., Ohlhues A., Madsen K. H., Nybing J. D., Christensen H., Christensen A., (2017). Are movement artifacts in magnetic resonance imaging a real problem?—a narrative review. Front Neurol 8:232. 10.3389/fneur.2017.0023228611728
Hermans D., Craske M. G., Mineka S., Lovibond P. F., (2006). Extinction in human fear conditioning. Biol. Psychiatry 60, 361–368. 10.1016/j.biopsych.2005.10.00616503330
Hildebrandt H., Zieger A., Engel A., Fritz K. W., Bussmann B., (1998). Differentiation of autonomic nervous activity in different stages of coma displayed by power spectrum analysis of heart rate variability. Eur. Arch. Psychiatry Clin. Neurosci. 248, 46–52. 10.1007/s0040600500169561352
Hoeldtke R. D., Davis K. M., Hshieh P. B., Gaspar S. R., Dworkin G. E., (1992). Autonomic surface potential analysis: assessment of reproducibility and sensitivity. Muscle Nerve 15, 926–931. 10.1002/mus.8801508101495508
Holte R. C., (1993). Very simple classification rules perform well on most commonly used datasets. Mach. Learn. 11, 63–90. 10.1023/A:1022631118932
Iannetti G. D., Mouraux A., (2010). From the neuromatrix to the pain matrix (and back). Exp. Brain Res. 205, 1–12. 10.1007/s00221-010-2340-120607220
Ingvar M., (1999). Pain and functional imaging. Philos. Trans. R Soc. Lond. B Biol. Sci. 354, 1347–1358. 10.1098/rstb.1999.048310466155
Jeanne M., Logier R., De Jonckheere J., Tavernier B., (2009). Heart rate variability during total intravenous anesthesia: effects of nociception and analgesia. Auton Neurosci. 147, 91–96. 10.1016/j.autneu.2009.01.00519201661
Jennett B., (2002). The vegetative state. J. Neurol. Neurosurg. Psychiatry 73, 355–357. 10.1136/jnnp.73.4.35512235296
Jiang X., Bian G-B., Tian Z., (2019). Removal of artifacts from EEG signals: a review. Sensors 19:987. 10.3390/s1905098730813520
Juan E., Nguepnjo Nguissi N. A., Tzovara A., Viceic D., Rusca M., Oddo M., et al. (2016). Evidence of trace conditioning in comatose patients revealed by the reactivation of EEG responses to alerting sounds. NeuroImage 141, 530–541. 10.1016/j.neuroimage.2016.07.03927444570
Kassubek J., Juengling F. D., Els T., Spreer J., Herpers M., Krause T., et al. (2003). Activation of a residual cortical network during painful stimulation in long-term postanoxic vegetative state: a 15O-H2O PET study. J. Neurol. Sci. 212, 85–91. 10.1016/S0022-510X(03)00106-012810004
Keller I., Hülsdunk A., Müller F., (2007). The influence of acoustic and tactile stimulation on vegetative parameters and EEG in persistent vegetative state. Funct. Neurol. 22, 159–163.17925166
Kelley H. H., Michela J. L., (1980). Attribution theory and research. Ann. Rev.Psychol. 31, 457–501. 10.1146/annurev.ps.31.020180.00232520809783
Kennedy W. R., Wendelschafer-Crabb G., Brelje T. C., (1994). Innervation and vasculature of human sweat glands: an immunohistochemistry-laser scanning confocal fluorescence microscopy study. J. Neurosci. 14, 6825–6833. 10.1523/JNEUROSCI.14-11-06825.19947525893
Khalfa S., Isabelle P., Jean-Pierre B., Manon R., (2002). Event-related skin conductance responses to musical emotions in humans. Neurosci. Lett. 328, 145–149. 10.1016/S0304-3940(02)00462-712133576
Knezevic W., Bajada S., (1985). Peripheral autonomic surface potential. A quantitative technique for recording sympathetic conduction in man. J. Neurol. Sci. 67, 239–251. 10.1016/0022-510X(85)90120-03981220
Koenig J., Jarczok M. N., Ellis R. J., Hillecke T. K., Thayer J. F., (2014). Heart rate variability and experimentally induced pain in healthy adults: a systematic review: HRV nociceptive stimulation review. Eur. J. Pain 18, 301–314. 10.1002/j.1532-2149.2013.00379.x
Kotchoubey B., Merz S., Lang S., Markl A., Müller F., Yu T., et al. (2013). Global functional connectivity reveals highly significant differences between the vegetative and the minimally conscious state. J. Neurol. 260, 975–983. 10.1007/s00415-012-6734-923128970
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. 10.1186/1741-7015-8-68
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. 10.1006/nimg.2002.123612377148
Lee H. R., (2003). Effects of relaxing music on stress response of patients with acute myocardial infarction. J. Korean Acad. Nurs. 33, 693–704. 10.4040/jkan.2003.33.6.69315314387
Levy D. M., Reid G., Rowley D. A., Abraham R. R., (1992). Quantitative measures of sympathetic skin response in diabetes: relation to sudomotor and neurological function. J. Neurol. Neurosurg. Psychiatry 55, 902–908. 10.1136/jnnp.55.10.9021331334
Lockwood P. L., Iannetti G. D., Haggard P., (2013). Transcranial magnetic stimulation over human secondary somatosensory cortex disrupts perception of pain intensity. Cortex 49, 2201–2209. 10.1016/j.cortex.2012.10.00623290634
Loeser J. D., Treede R-D., (2008). The kyoto protocol of IASP basic pain terminology. Pain 137, 473–477. 10.1016/j.pain.2008.04.02518583048
Lovibond P. F., Shanks D. R., (2002). The role of awareness in pavlovian conditioning: empirical evidence and theoretical implications. J. Exp. Psychol. 28, 3–26. 10.1037//0097-7403.28.1.311868231
Lui S., Grunberg D., (2017). “Using skin conductance to evaluate the effect of music silence to relieve and intensify arousal,” in 2017 International Conference on Orange Technologies (ICOT) (Singapore), 91–94. 10.1109/ICOT.2017.8336096
Markl A., Yu T., Vogel D., Müller F., Kotchoubey B., Lang S., (2013). Brain processing of pain in patients with unresponsive wakefulness syndrome. Brain Behav. 3, 95–103. 10.1002/brb3.11023533065
Mather M., Thayer J. F., (2018). How heart rate variability affects emotion regulation brain networks. Curr. Opin. Behav. Sci. 19, 98–104. 10.1016/j.cobeha.2017.12.01729333483
Meaney D. F., Morrison B., Dale Bass C., (2014). The mechanics of traumatic brain injury: a review of what we know and what we need to know for reducing its societal burden. J. Biomech. Eng. 136:021008. 10.1115/1.402636424384610
Medford N., Critchley H. D., (2010). Conjoint activity of anterior insular and anterior cingulate cortex: awareness and response. Brain Struct. Funct. 214, 535–549. 10.1007/s00429-010-0265-x20512367
Naro A., Leo A., Bramanti P., Calabrò R. S., (2015). Moving toward conscious pain processing detection in chronic disorders of consciousness: anterior cingulate cortex neuromodulation. J. Pain 16, 1022–1031. 10.1016/j.jpain.2015.06.01426208761
Naro A., Leo A., Cannavò A., Buda A., Bramanti P., Calabrò R. S., (2016). Do unresponsive wakefulness syndrome patients feel pain? Role of laser-evoked potential-induced gamma-band oscillations in detecting cortical pain processing. Neuroscience 317, 141–148. 10.1016/j.neuroscience.2016.01.00926791527
Owen A. M., Coleman M. R., Boly M., Davis M. H., Laureys S., Pickard J. D., (2007). Using functional magnetic resonance imaging to detect covert awareness in the vegetative state. Arch. Neurol. 64, 1098–1102. 10.1001/archneur.64.8.109817698699
Pavlov I. P., (1927). Conditioned Reflexes. London: Oxford Univ. Press.
Peterson A., Cruse D., Naci L., Weijer C., Owen A. M., (2015). Risk, diagnostic error, and the clinical science of consciousness. Neuroimage 7, 588–597. 10.1016/j.nicl.2015.02.00825844313
Ploner M., Gross J., Timmermann L., Schnitzler A., (2002). Cortical representation of first and second pain sensation in humans. Proc. Natl. Acad. Sci. U.S.A. 99, 12444–12448. 10.1073/pnas.18227289912209003
Rainville P., Carrier B., Hofbauer R. K., Bushnell M. C., Duncan G. H., (1999). Dissociation of sensory and affective dimensions of pain using hypnotic modulation. Pain 82, 159–171. 10.1016/S0304-3959(99)00048-210467921
Reis P. M. R., Hebenstreit F., Gabsteiger F., von Tscharner V., Lochmann M., (2014). Methodological aspects of EEG and body dynamics measurements during motion. Front. Hum. Neurosci. 8:156. 10.3389/fnhum.2014.0015624715858
Richman J. S., Moorman J. R., (2000). Physiological time-series analysis using approximate entropy and sample entropy. Am. J. Physiol. Heart Circ. Physiol. 278, H2039–H2049. 10.1152/ajpheart.2000.278.6.H203910843903
Riedl B., Nischik M., Birklein F., Neundörfer B., Handwerker H. O., (1998). Spatial extension of sudomotor axon reflex sweating in human skin. J. Auton. Nerv. Syst. 69, 83–88. 10.1016/S0165-1838(98)00016-29696262
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 International Publishing), 145–155. 10.1007/978-3-319-21425-2_11
Riganello F., Chatelle C., Schnakers C., Laureys S., (2018a). Heart rate variability as an indicator of nociceptive pain in disorders of consciousness? J. Pain Symptom Manage. 57, 47–56. 10.1016/j.jpainsymman.2018.09.01630267843
Riganello F., Cortese M. D., Arcuri F., Candelieri A., Guglielmino F., Dolce G., et al. (2014). A study of the reliability of the nociception coma scale. Clin. Rehabil. 29, 388–393. 10.1177/026921551454676725172088
Riganello F., Garbarino S., Sannita W. G., (2012). Heart rate variability, homeostasis, and brain function: a tutorial and review of application. J. Psychophysiol. 26, 178–203. 10.1027/0269-8803/a000080
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. 10.3389/fneur.2018.0076930258400
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. 10.3389/fneur.2016.0020227899911
Riganello F., Sannita W. G., (2009). Residual brain processing in the vegetative state. J. Psychophysiol. 23, 18–26. 10.1027/0269-8803.23.1.18
Roebuck-Spencer T., Cernich A., (2014). “Epidemiology and societal impact of traumatic brain injury,” in Handbook on the Neuropsychology of Traumatic Brain Injury. Clinical Handbooks in Neuropsychology, eds M. Sherer and A. Sander (New York, NY: Springer), 3–23. 10.1007/978-1-4939-0784-7_1
Rosenthal R., (1991). Effect sizes: pearson's correlation, its display via the BESD, and alternative indices. Am. Psychol. 46, 1086–1087. 10.1037/0003-066X.46.10.1086
Roy J-C., Boucsein W., Fowles D. C., Gruzelier J., (2012). Progress in Electrodermal Research. New York, NY: Springer Science & Business Media.
Ryan M. L., Thorson C. M., Otero C. A., Vu T., Proctor K. G., (2011). Clinical applications of heart rate variability in the triage and assessment of traumatically injured patients. Anesthesiol. Res. Pract. 2011:416590. 10.1155/2011/41659021350685
Schiff N. D., Rodriguez-Moreno D., Kamal A., Kim K. H. S., Giacino J. T., Plum F., et al. (2005). fMRI reveals large-scale network activation in minimally conscious patients. Neurology 64, 514–523. 10.1212/01.WNL.0000150883.10285.4415699384
Schnakers C., Chatelle C., Vanhaudenhuyse A., Majerus S., Ledoux D., Boly M., et al. (2010). The Nociception coma scale: a new tool to assess nociception in disorders of consciousness. Pain 148, 215–219. 10.1016/j.pain.2009.09.02819854576
Schnakers C., Zasler N., (2015). Assessment and management of pain in patients with disorders of consciousness. PM R 7(11 Suppl.), S270–S277. 10.1016/j.pmrj.2015.09.01626568506
Schnakers C., Zasler N. D., (2007). Pain assessment and management in disorders of consciousness. Curr. Opin. Neurol. 20, 620–626. 10.1097/WCO.0b013e3282f169d917992079
Shackman A. J., Salomons T. V., Slagter H. A., Fox A. S., Winter J. J., Davidson R. J., (2011). The integration of negative affect, pain and cognitive control in the cingulate cortex. Nat. Rev. Neurosci. 12, 154–167. 10.1038/nrn299421331082
Storm H., (2008). Changes in skin conductance as a tool to monitor nociceptive stimulation and pain. Curr. Opin. Anaesthesiol. 21, 796–804. 10.1097/ACO.0b013e3283183fe418997532
Tarvainen M. P., Niskanen J-P., Lipponen J. A., Ranta-Aho P. O., Karjalainen P. A., (2014). Kubios HRV–heart rate variability analysis software. Comput. Methods Prog. Biomed. 113, 210–220. 10.1016/j.cmpb.2013.07.02424054542
Thayer J. F., (2007). What the heart says to the brain (and vice versa) and why we should listen. Psihologijske Teme 16, 241–250.
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. 10.1016/j.clinph.2018.01.06829486984
Tommaso M., de Navarro J., Ricci K., Lorenzo M., Lanzillotti C., Colonna F., et al. (2013). Pain in prolonged disorders of consciousness: laser evoked potentials findings in patients with vegetative and minimally conscious states. Brain Inj. 27, 962–972. 10.3109/02699052.2013.77550723789870
Turner-Stokes L., Kitzinger J., Gill-Thwaites H., Playford E. D., Wade D., Allanson J., et al. (2012). fMRI for vegetative and minimally conscious states. BMJ 345:e8045. 10.1136/bmj.e804523190911
Umetani K., Singer D. H., McCraty R., Atkinson M., (1998). Twenty-four hour time domain heart rate variability and heart rate: relations to age and gender over nine decades. J. Am. Coll. Cardiol. 31, 593–601. 10.1016/S0735-1097(97)00554-89502641
van Erp W. S., Lavrijsen J. C. M., Vos P. E., Bor H., Laureys S., Koopmans R. T. C. M., (2015). The vegetative state: prevalence, misdiagnosis, and treatment limitations. J. Am. Med. Dir. Assoc. 16, 85.e9–85.e14. 10.1016/j.jamda.2014.10.01425528282
Venturella I., (2018). EEG and autonomic responses to nociceptive stimulation in disorders of consciousness. J. Clin. Neurosci. 60, 101–106. 10.1016/j.jocn.2018.09.02030309803
Vetrugno R., Liguori R., Cortelli P., Montagna P., (2003). Sympathetic skin response. Clin. Auton. Res. 13, 256–270. 10.1007/s10286-003-0107-512955550
Voss A., Heitmann A., Schroeder R., Peters A., Perz S., (2012). Short-term heart rate variability–age dependence in healthy subjects. Physiol. Measur. 33, 1289–1311. 10.1088/0967-3334/33/8/128922813869
Yentes J. M., Hunt N., Schmid K. K., Kaipust J. P., McGrath D., Stergiou N., (2013). The appropriate use of approximate entropy and sample entropy with short data sets. Ann. Biomed. Eng. 41, 349–365. 10.1007/s10439-012-0668-323064819
Yokota T., Takahashi T., Kondo M., Fujimori B., (1959). Studies on the diphasic wave form of the galvanic skin reflex. Electroencephalogr. Clin. Neurophysiol. 11, 687–696. 10.1016/0013-4694(59)90109-913846558
Züst M. A., Ruch S., Wiest R., Henke K., (2019). Implicit vocabulary learning during sleep is bound to slow-wave peaks. Curr. Biol. 29, 541–553.e7. 10.1016/j.cub.2018.12.038