Abstract
Purpose of Review
Diagnostic classification of patients with disorders of consciousness (DoC) is based on clinician’s observation of volitional behaviours. However, patients’ caregivers often report higher levels of responsiveness with respect to those observed during the clinical assessment. Thus, increasing efforts have been aimed at comprehending the effects of self-referential and emotional stimuli on patients’ responsiveness. Here we systematically reviewed the original experimental studies that compared behavioural and electrophysiological responses with salient vs. neutral material in patients in vegetative state/unresponsive wakefulness syndrome or in minimally conscious state.
Recent Findings
Most of the reviewed studies showed that salient stimuli (i.e. patient’s own or familiar faces, patient’s own name, and familiar voices) seem to elicit a higher amount of behavioural or electrophysiological responses with respect to neutral pictures or sounds. Importantly, a quite high percentage of patients seem to respond to salient stimuli only.
Summary
The present review could foster use of personally salient stimuli in assessing DoC. However, the low overall quality of evidence and some limitations in the general reviewing process might induce caution in transferring these suggestions into clinical practice.
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References
Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance
•• Giacino JT, Katz DI, Schiff ND, Whyte J, Ashman EJ, Ashwal S, et al. Practice guideline update recommendations summary: disorders of consciousness: report of the Guideline Development, Dissemination, and Implementation. Arch Phys Med Rehabil. 2018;99(9):1699–709. https://doi.org/10.1016/j.apmr.2018.07.001 This paper provides the most recent practice recommendations for improving diagnostic and prognostic accuracy in patients with prolonged DoC.
Multi-Society Task Force on PVS. Medical aspects of the persistent vegetative state. New Engl J Med. 1994;330(21):1499–508. https://doi.org/10.1056/nejm199507133330216.
Laureys S, Celesia GG, Cohadon F, Lavrijsen J, León-Carrión J, Sannita WG, et al. Unresponsive wakefulness syndrome: a new name for the vegetative state or apallic syndrome. BMC Med. 2010;8(1):68. https://doi.org/10.1186/1741-7015-8-68.
Giacino JT, Ashwal S, Childs N, Cranford R, Jennett B, Katz DI, et al. The minimally conscious state: definition and diagnostic criteria. Neurology. 2002;58(3):349–53. https://doi.org/10.1212/wnl.58.3.349.
Giacino JT, Kalmar K. The vegetative and minimally conscious states: a comparison of clinical features and functional outcome. J Head Trauma Rehabil. 1997;12(4):36–51.
Bernat JL. Chronic disorders of consciousness. Lancet. 2006;367(9517):1181–92. https://doi.org/10.1016/S0140-6736(06)68508-5.
Estraneo A, Trojano L. Prognosis in disorders of consciousness. In: Schnakers C, Laureys S, editors. Coma and disorders of consciousness. Cham: Springer; 2018. p. 17–36.
Schnakers C, Vanhaudenhuyse A, Giacino J, Ventura M, Boly M, Majerus S, et al. Diagnostic accuracy of the vegetative and minimally conscious state: clinical consensus versus standardized neurobehavioral assessment. BMC Neurol. 2009;9(1):35. https://doi.org/10.1186/1471-2377-9-35.
Majerus S, Gill-Thwaites H, Andrews K, Laureys S. Behavioral evaluation of consciousness in severe brain damage. Prog Brain Res. 2005;150:397–413. https://doi.org/10.1016/S0079-6123(05)50028-1.
Giacino JT, Kalmar K, Whyte J. The JFK Coma Recovery Scale-Revised: measurement characteristics and diagnostic utility. Arch Phys Med Rehabil. 2004;85(12):2020–9. https://doi.org/10.1016/j.apmr.2004.02.033.
Formisano R, Giustini M, Aloisi M, Contrada M, Schnakers C, Zasler N, et al. An International survey on diagnostic and prognostic protocols in patients with disorder of consciousness. Brain Inj. 2019:1–11. https://doi.org/10.1080/02699052.2019.1622785.
Estraneo A, Moretta P, Cardinale V, De Tanti A, Gatta G, Giacino JT, et al. A multicentre study of intentional behavioural responses measured using the Coma Recovery Scale–Revised in patients with minimally conscious state. Clin Rehabil. 2015;29(8):803–8. https://doi.org/10.1177/0269215514556002.
Estraneo A, Loreto V, Guarino I, Boemia V, Paone G, Moretta P, et al. Standard EEG in diagnostic process of prolonged disorders of consciousness. Neurophysiology. 2016;127(6):2379–85. https://doi.org/10.1016/j.clinph.2016.03.021.
Faugeras F, Rohaut B, Weiss N, Bekinschtein TA, Galanaud D, Puybasset L, et al. Probing consciousness with event-related potentials in the vegetative state. Neurology. 2011;77(3):264–8. https://doi.org/10.1212/WNL.0b013e3182217ee8.
Faugeras F, Rohaut B, Weiss N, Bekinschtein T, Galanaud D, Puybasset L, et al. Event related potentials elicited by violations of auditory regularities in patients with impaired consciousness. Neuropsychologia. 2012;50(3):403–18. https://doi.org/10.1016/j.neuropsychologia.2011.12.015.
Trojano L, Moretta P, Loreto V, Cozzolino A, Santoro L, Estraneo A. Quantitative assessment of visual behavior in disorders of consciousness. J Neurol. 2012;259(9):1888–95. https://doi.org/10.1007/s00415-012-6435-4.
Giacino JT. The vegetative and minimally conscious states: consensus-based criteria for establishing diagnosis and prognosis. Neurorehabilitation. 2004;19(4):293–8.
Estraneo A, Moretta P, De Tanti A, Gatta G, Giacino JT, Trojano L. An Italian multicentre validation study of the coma recovery scale-revised. Eur J Phys Rehabil Med. 2015;51(5):627–34.
Jox RJ, Kuehlmeyer K, Klein AM, Herzog J, Schaupp M, Nowak DA, et al. Diagnosis and decision making for patients with disorders of consciousness: a survey among family members. Arch Phys Med Rehabil. 2015;96(2):323–30. https://doi.org/10.1016/j.apmr.2014.09.030.
Moretta P, Trojano L, Masotta O, Cardinale V, Loreto V, Estraneo A. Family caregivers’ opinions about interaction with the environment in consciousness disorders. Rehabil Psychol. 2017;62(2):208. https://doi.org/10.1037/rep0000144.
Mack A, Pappas Z, Silverman M, Gay R. What we see: inattention and the capture of attention by meaning. Conscious Cogn. 2002;11(4):488–506.
Vanhaudenhuyse A, Schnakers C, Brédart S, Laureys S. Assessment of visual pursuit in post-comatose states: use a mirror. J Neurol Neurosurg Psychiatry. 2008;79(2):223–3. https://doi.org/10.1136/jnnp.2007.121624.
• Di H, Nie Y, Hu X, Tong Y, Heine L, Wannez S, et al. Assessment of visual fixation in vegetative and minimally conscious states. BMC Neurol. 2014;14(1):147. https://doi.org/10.1186/1471-2377-14-147 The authors investigated the effect of using a mirror, compared with an object or a flashing light, to elicit visual fixation, and turned out to be the study with higher methodological accuracy, as assessed by the GRADE system, in the present review.
Perrin F, Schnakers C, Schabus M, Degueldre C, Goldman S, Brédart S, et al. Brain response to one’s own name in vegetative state, minimally conscious state, and locked-in syndrome. Arch Neurol. 2006;63(4):562–9. https://doi.org/10.1001/archneur.63.4.562.
Schnakers C, Perrin F, Schabus M, Majerus S, Ledoux D, Damas P, et al. Voluntary brain processing in disorders of consciousness. Neurology. 2008;71(20):1614–20. https://doi.org/10.1212/01.wnl.0000334754.15330.69.
Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009;151(4):264–9. https://doi.org/10.1016/j.ijsu.2010.02.007.
Schünemann H. The GRADE handbook. Cochrane Collaboration; 2013.
Guyatt G, Oxman AD, Akl EA, Kunz R, Vist G, Brozek J, et al. GRADE guidelines: 1. Introduction—GRADE evidence profiles and summary of findings tables. J Clin Epidemiol. 2011;64(4):383–94. https://doi.org/10.1016/j.jclinepi.2010.04.026.
Formisano R, D’Ippolito M, Risetti M, Riccio A, Caravasso CF, Catani S, et al. Vegetative state, minimally conscious state, akinetic mutism and Parkinsonism as a continuum of recovery from disorders of consciousness: an exploratory and preliminary study. Funct Neurol. 2011;26(1):15.
Di Stefano C, Cortesi A, Masotti S, Simoncini L, Piperno R. Increased behavioural responsiveness with complex stimulation in VS and MCS: preliminary results. Brain Inj. 2012;26(10):1250–6. https://doi.org/10.3109/02699052.2012.667588.
Cheng L, Gosseries O, Ying L, Hu X, Yu D, Gao H, et al. Assessment of localisation to auditory stimulation in post-comatose states: use the patient’s own name. BMC Neurol. 2013;13(1):27. https://doi.org/10.1186/1471-2377-13-27.
Trojano L, Moretta P, Loreto V, Santoro L, Estraneo A. Affective saliency modifies visual tracking behavior in disorders of consciousness: a quantitative analysis. J Neurol. 2013;260(1):306–8. https://doi.org/10.1007/s00415-012-6717-x.
Trojano L, Moretta P, Masotta O, Loreto V, Estraneo A. Visual pursuit of one’s own face in disorders of consciousness: a quantitative analysis. Brain Inj. 2018;32(12):1549–55. https://doi.org/10.1080/02699052.2018.1504117.
• Thonnard M, Wannez S, Keen S, Brédart S, Brun MA, Gosseries O, et al. Detection of visual pursuit in patients in minimally conscious state: a matter of stimuli and visual plane? Brain Inj. 2014;28(9):1164–70. https://doi.org/10.3109/02699052.2014.920521 The authors demonstrated on a very large sample of patients with DoC the importance of using a mirror, compared with an object or a moving person, when clinically evaluating visual pursuit, a critical marker discriminating VS/UWS and MCS.
Cavinato M, Volpato C, Silvoni S, Sacchetto M, Merico A, Piccione F. Event-related brain potential modulation in patients with severe brain damage. Clin Neurophysiol. 2011;122(4):719–24. https://doi.org/10.1016/j.clinph.2010.08.024.
Del Giudice R, Blume C, Wislowska M, Lechinger J, Heib DP, Pichler G, et al. Can self-relevant stimuli help assessing patients with disorders of consciousness? Conscious Cogn. 2016;44:51–60. https://doi.org/10.1016/j.concog.2016.06.013.
Bates D. The vegetative state: guidance on diagnosis and management-a report of a working party of the Royal College of Physicians. Clin Med. 2003;3(3):249–54. https://doi.org/10.7861/clinmedicine.3-3-249.
Shiel A, Horn SA, Wilson BA, Watson MJ, Campbell MJ, McLellan DL. The Wessex Head Injury Matrix (WHIM) main scale: a preliminary report on a scale to assess and monitor patient recovery after severe head injury. Clin Rehabil. 2000;14(4):408–16. https://doi.org/10.1191/0269215500cr326oa.
Formisano R, Vinicola V, Carlesimo GA, Sabbadini M, Penta F. Assessment scale for patients with prolonged disturbances of consciousness (postcoma scale). Proceedings of the Fifth Conference of the International Association for the study of Traumatic Brain Injury and 20th Conference of the Australian Society for the Study of Brain Impairment. Melbourne: Australian Academic Press. 1996. p. 15-18.
Brédart S, Delchambre M, Laureys S. One’s own face is hard to ignore. Q J Exp Psychol. 2006;59(1):46–52. https://doi.org/10.1080/17470210500343678.
Devue C, Brédart S. Attention to self-referential stimuli: can I ignore my own face? Acta Psychol (Amst). 2008;128(2):290–7. https://doi.org/10.1016/j.actpsy.2008.02.004.
Tacikowski P, Nowicka A. Allocation of attention to self-name and self-face: an ERP study. Biol Psychol. 2010;84(2):318–24. https://doi.org/10.1016/j.biopsycho.2010.03.009.
Tong F, Nakayama K. Robust representations for faces: evidence from visual search. J Exp Psychol Hum Percept Perform. 1999;25(4):1016. https://doi.org/10.1037//0096-1523.25.4.1016.
Bruno MA, Vanhaudenhuyse A, Thibaut A, Moonen G, Laureys S. From unresponsive wakefulness to minimally conscious PLUS and functional locked-in syndromes: recent advances in our understanding of disorders of consciousness. J Neurol. 2011;258(7):1373–84. https://doi.org/10.1007/s00415-011-6114-x.
Menon DK, Owen AM, Boniface SJ, Pickard JD. Cortical processing in persistent vegetative state. Lancet. 1998;352(9134):1148–9. https://doi.org/10.1016/s0140-6736(05)77805-3.
Owen AM, Menon DK, Johnsrude IS, Bor D, Scott SK, Manly T, et al. Detecting residual cognitive function in persistent vegetative state. Neurocase. 2002;8(5):394–403. https://doi.org/10.1076/neur.8.4.394.16184.
Sharon H, Pasternak Y, Simon EB, Gruberger M, Giladi N, Krimchanski BZ, et al. Emotional processing of personally familiar faces in the vegetative state. PLoS One. 2013;8(9):e74711. https://doi.org/10.1371/journal.pone.0074711.
Grill-Spector K, Knouf N, Kanwisher N. The fusiform face area subserves face perception, not generic within-category identification. Nat Neurosci. 2004;7(5):555. https://doi.org/10.1038/nn1224.
Kanwisher N, Yovel G. The fusiform face area: a cortical region specialized for the perception of faces. Philos Trans R Soc Lond B Biol Sci. 2006;361(1476):2109–28. https://doi.org/10.1098/rstb.2006.1934.
Menon V, Uddin LQ. Saliency, switching, attention and control: a network model of insula function. Brain Struct Funct. 2010;214(5-6):655–67. https://doi.org/10.1007/s00429-010-0262-0.
Pessoa L, Adolphs R. Emotion processing and the amygdala: from a ‘low road’ to ‘many roads’ of evaluating biological significance. Nat Rev Neurosci. 2010;11(11):773. https://doi.org/10.1038/nrn2920.
Zhu J, Wu X, Gao L, Mao Y, Zhong P, Tang W, et al. Cortical activity after emotional visual stimulation in minimally conscious state patients. J Neurotrauma. 2009;26(5):677–88. https://doi.org/10.1089/neu.2008.0691.
Wannez S, Vanhaudenhuyse A, Laureys S, Brédart S. Mirror efficiency in the assessment of visual pursuit in patients in minimally conscious state. Brain Inj. 2017;31(11):1429–35. https://doi.org/10.1080/02699052.2017.1376755.
Xiao NG, Perrotta S, Quinn PC, Wang Z, Sun YHP, Lee K. On the facilitative effects of face motion on face recognition and its development. Front Psychol. 2014;5:633. https://doi.org/10.3389/fpsyg.2014.00633.
Cherry EC. Some experiments on the recognition of speech, with one and with two ears. J Acoust Soc Am. 1953;25(5):975–9.
Oswald I, Taylor AM, Treisman M. Discriminative responses to stimulation during human sleep. Brain. 1960;80:440–53. https://doi.org/10.1093/brain/83.3.440.
Kurtz D, Trapp C, Kieny MT, Wassmer JM, Mugnaioni MD, Pack A, et al. Study of recovery and the post-anaesthetic period (author’s transl). Rev Electroencephalogr Neurophysiol Clin. 1977;7(1):62–9.
Staffen W, Kronbichler M, Aichhorn M, Mair A, Ladurner G. Selective brain activity in response to one’s own name in the persistent vegetative state. J Neurol Neurosurg Psychiatry. 2006;77(12):1383–4. https://doi.org/10.1136/jnnp.2006.095166.
Bick AS, Leker RR, Ben-Hur T, Levin N. Implementing novel imaging methods for improved diagnosis of disorder of consciousness patients. J Neurol Sci. 2013;334(1-2):130–8. https://doi.org/10.1016/j.jns.2013.08.009.
Nicholas CR, McLaren DG, Gawrysiak MJ, Rogers BP, Dougherty JH, Nash MR. Functional neuroimaging of personally-relevant stimuli in a paediatric case of impaired awareness. Brain Inj. 2014;28(8):1135–8. https://doi.org/10.3109/02699052.2014.890745.
Bekinschtein T, Niklison J, Sigman L, Manes FRLJA, Leiguarda R, Armony J, et al. Emotion processing in the minimally conscious state. J Neurol Neurosurg Psychiatry. 2004;75(5):788–8. https://doi.org/10.1136/jnnp.2003.034876.
Kotchoubey B, Merz S, Lang S, Markl A, Mülle F, Yu T, et al. Global functional connectivity reveals highly significant differences between the vegetative and the minimally conscious state. J Neurol. 2013;260(4):975–83. https://doi.org/10.1007/s00415-012-6734-9.
Yu T, Lang S, Vogel D, Markl A, Müller F, Kotchoubey B. Patients with unresponsive wakefulness syndrome respond to the pain cries of other people. Neurology. 2013;80(4):345–52. https://doi.org/10.1212/WNL.0b013e31827f0846.
Harris CR, Pashler H. Attention and the processing of emotional words and names: not so special after all. Psychol Sci. 2004;15(3):171–8. https://doi.org/10.1111/j.0956-7976.2004.01503005.x.
Laureys S, Perrin F, Brédart S. Self-consciousness in non-communicative patients. Conscious Cogn. 2007;16(3):722–41. https://doi.org/10.1016/j.concog.2007.04.004.
Seel RT, Sherer M, Whyte J, Katz DI, Giacino JT, Rosenbaum AM, et al. Assessment scales for disorders of consciousness: evidence-based recommendations for clinical practice and research. Arch Phys Med Rehabil. 2010;91(12):1795–813. https://doi.org/10.1016/j.apmr.2010.07.218.
Laureys S, Perrin F, Faymonville ME, Schnakers C, Boly M, Bartsch V, et al. Cerebral processing in the minimally conscious state. Neurology. 2004;63(5):916–8. https://doi.org/10.1212/01.wnl.0000137421.30792.9b.
De Salvo S, Caminiti F, Bonanno L, De Cola MC, Corallo F, Caizzone A, et al. Neurophysiological assessment for evaluating residual cognition in vegetative and minimally conscious state patients: a pilot study. Funct Neurol. 2015;30(4):237.
Wang XY, Wu HY, Lu HT, Huang TT, Zhang H, Zhang T. Assessment of mismatch negativity and P300 response in patients with disorders of consciousness. Eur Rev Med Pharmacol Sci. 2017;21(21):4896–906.
Castro M, Tillmann B, Luauté J, Corneyllie A, Dailler F, André-Obadia N, et al. Boosting cognition with music in patients with disorders of consciousness. Neurorehab Neural Repair. 2015;29(8):734–42. https://doi.org/10.1177/1545968314565464.
Riganello F, Candelieri A, Quintieri M, Conforti D, Dolce G. Heart rate variability: an index of brain processing in vegetative state? An artificial intelligence, data mining study. Clin Neurophysiol. 2010;121(12):2024–34. https://doi.org/10.1016/j.clinph.2010.05.010.
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This work was supported by grant from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement no. 778234—DoCMA project.
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Alfonso Magliacano, Francesco De Bellis, Alejandro Galvao-Carmona, Anna Estraneo, and Luigi Trojano each declare no potential conflicts of interest.
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Magliacano, A., De Bellis, F., Galvao-Carmona, A. et al. Can Salient Stimuli Enhance Responses in Disorders of Consciousness? A Systematic Review. Curr Neurol Neurosci Rep 19, 98 (2019). https://doi.org/10.1007/s11910-019-1018-8
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DOI: https://doi.org/10.1007/s11910-019-1018-8