Diagnosis; Disorders of consciousness; Electrooculography; Language; Linguistic learning; Humans; Male; Female; Adult; Middle Aged; Young Adult; Learning/physiology; Electroencephalography/methods; Aged; Consciousness Disorders/physiopathology; Consciousness Disorders/diagnosis; Consciousness Disorders; Electroencephalography; Learning; Neurology; Cognitive Neuroscience
Abstract :
[en] For patients with disorders of consciousness (DoC), accurate assessment of residual consciousness levels and cognitive abilities is critical for developing appropriate rehabilitation interventions. In this study, we investigated the potential of electrooculography (EOG) in assessing language processing abilities and consciousness levels. Patients' EOG data and related electrophysiological data were analysed before and after explicit language learning. The results showed distinct differences in vocabulary learning patterns among patients with varying levels of consciousness. While minimally conscious patients showed significant neural tracking of artificial words and notable learning effects similar to those observed in healthy controls, whereas patients with unresponsive wakefulness syndrome did not show such effects. Correlation analysis further indicated that EOG detected vocabulary learning effects with comparable validity to electroencephalography, reinforcing the credibility of EOG indicator as a diagnostic tool. Critically, EOG also revealed significant correlations between individual patients' linguistic learning performance and their Oromotor/verbal function as assessed through behavioural scales. In conclusion, this study explored the differences in language processing abilities among patients with varying consciousness levels. By demonstrating the utility of EOG in evaluating consciousness and detecting vocabulary learning effects, as well as its potential to guide personalised rehabilitation, our findings indicate that EOG indicators show promise as a rapid, accurate and effective additional tool for diagnosing and managing patients with DoC.
Disciplines :
Neurosciences & behavior
Author, co-author :
Xiao, Xiangyue; International Unresponsive Wakefulness Syndrome and Consciousness Science Institute, Hangzhou Normal University, Hangzhou 311121, China, Key Laboratory of Ageing and Cancer Biology of Zhejiang Province, School of Basic Medical Sciences, Hangzhou Normal University, Hangzhou 311121, China
Ding, Junhua ; Department of Psychology, University of Edinburgh, Edinburgh EH8 9YL, UK
Yu, Mingyan; International Unresponsive Wakefulness Syndrome and Consciousness Science Institute, Hangzhou Normal University, Hangzhou 311121, China, Key Laboratory of Ageing and Cancer Biology of Zhejiang Province, School of Basic Medical Sciences, Hangzhou Normal University, Hangzhou 311121, China
Dong, Zhicai; International Unresponsive Wakefulness Syndrome and Consciousness Science Institute, Hangzhou Normal University, Hangzhou 311121, China, Key Laboratory of Ageing and Cancer Biology of Zhejiang Province, School of Basic Medical Sciences, Hangzhou Normal University, Hangzhou 311121, China
Cruz, Sara ; The Psychology for Development Research Centre, Lusiada University Porto, Porto 4100-348, Portugal
Ding, Nai; Key Laboratory for Biomedical Engineering of Ministry of Education, College of Biomedical Engineering and Instrument Sciences, Zhejiang University, Hangzhou 310027, China
Aubinet, Charlène ; Université de Liège - ULiège > GIGA > GIGA Neurosciences - Coma Science Group
Laureys, Steven ; Université de Liège - ULiège > Département des sciences cliniques
Di, Haibo; International Unresponsive Wakefulness Syndrome and Consciousness Science Institute, Hangzhou Normal University, Hangzhou 311121, China, Key Laboratory of Ageing and Cancer Biology of Zhejiang Province, School of Basic Medical Sciences, Hangzhou Normal University, Hangzhou 311121, China. Electronic address: dihaibo19@aliyun.com
Chen, Yan ; International Unresponsive Wakefulness Syndrome and Consciousness Science Institute, Hangzhou Normal University, Hangzhou 311121, China, Key Laboratory of Ageing and Cancer Biology of Zhejiang Province, School of Basic Medical Sciences, Hangzhou Normal University, Hangzhou 311121, China. Electronic address: chen_yan@hznu.edu.cn
Language :
English
Title :
Exploring the clinical diagnostic value of linguistic learning ability in patients with disorders of consciousness using electrooculography.
Zhejiang Provincial Natural Science Foundation NSCF - National Natural Science Foundation of China
Funding text :
This study was supported by the National Natural Science Foundation of China [82201332], the Natural Science Foundation of Zhejiang Province [LQ22H090002], and the National Key Research and Development Program of China [2022YFC3601200]. SC was supported by national funds through the FCT \u2013 The Portuguese Foundation for Science and Technology, I.P., under the Project UIDB/04375/2020.
Aubinet, C., Chatelle, C., Gosseries, O., et al. Residual implicit and explicit language abilities in patients with disorders of consciousness: a systematic review. Neurosci. Biobehav. Rev. 132 (2022), 391–409, 10.1016/j.neubiorev.2021.12.001.
Balconi, M., Arangio, R., The relationship between coma near coma, disability ratings, and event-related potentials in patients with disorders of consciousness: a semantic association task. Appl. Psychophysiol. Biofeedb. 40 (2015), 327–337, 10.1007/s10484-015-9304-y.
Batterink, L., Syllables in sync form a link: neural phase-locking reflects word knowledge during language learning. J. Cogn. Neurosci. 32 (2020), 1735–1748, 10.1162/jocn_a_01581.
Bekinschtein, T.A., Shalom, D.E., Forcato, C., et al. Classical conditioning in the vegetative and minimally conscious state. Nat. Neurosci. 12 (2009), 1343–1349, 10.1038/nn.2391.
Beukema, S., Gonzalez-Lara, L.E., Finoia, P., et al. A hierarchy of event-related potential markers of auditory processing in disorders of consciousness. Neuroimage: Clin. 12 (2016), 359–371, 10.1016/j.nicl.2016.08.003.
Boly, M., Faymonville, M.-E., Peigneux, P., et al. Auditory processing in severely brain injured patients: differences between the minimally conscious state and the persistent vegetative state. Arch. Neurol. 61 (2004), 233–238, 10.1001/archneur.61.2.233.
Bormann, T., Seyboth, M., Machleb, F., Weiller, C., Learning of novel compound nouns – A variant of lexical learning that requires intact verbal short-term memory. Cortex 124 (2020), 23–32, 10.1016/j.cortex.2019.08.024.
Brainard, D.H., The Psychophysics toolbox. Spat. Vis. 10 (1997), 433–436.
Chen, Y., Jin, P., Ding, N., The influence of linguistic information on cortical tracking of words. Neuropsychologia, 148, 2020, 107640, 10.1016/j.neuropsychologia.2020.107640.
Childs, N.L., Mercer, W.N., Childs, H.W., Accuracy of diagnosis of persistent vegetative state. Neurology, 43, 1993, 1465, 10.1212/WNL.43.8.1465.
deJong, B., Willemsen, A., Paans, A., Regional cerebral blood flow changes related to affective speech presentation in persistent vegetative state. Clin. Neurol. Neurosurg. 99 (1997), 213–216, 10.1016/S0303-8467(97)00024-3.
Demertzi, A., Antonopoulos, G., Heine, L., et al. Intrinsic functional connectivity differentiates minimally conscious from unresponsive patients. Brain 138 (2015), 2619–2631, 10.1093/brain/awv169.
Ding, N., Melloni, L., Zhang, H., et al. Cortical tracking of hierarchical linguistic structures in connected speech. Nat. Neurosci. 19 (2016), 158–164, 10.1038/nn.4186.
Ding, N., Pan, X., Luo, C., et al. Attention is required for knowledge-based sequential grouping: insights from the integration of syllables into words. J. Neurosci. 38 (2018), 1178–1188, 10.1523/JNEUROSCI.2606-17.2017.
Edlow, B., Claassen, J., Schiff, N., Dm, G., Recovery from disorders of consciousness: mechanisms, prognosis and emerging therapies. Nat. Rev. Neurol. 17 (2021), 135–156, 10.1038/s41582-020-00428-x.
Getz, H., Ding, N., Newport, E.L., Poeppel, D., Cortical tracking of constituent structure in language acquisition. Cognition 181 (2018), 135–140, 10.1016/j.cognition.2018.08.019.
Giacino, J.T., Fins, J.J., Laureys, S., Schiff, N.D., Disorders of consciousness after acquired brain injury: the state of the science. Nat. Rev. Neurol. 10 (2014), 99–114, 10.1038/nrneurol.2013.279.
Giacino, J.T., Kalmar, K., Whyte, J., The JFK coma recovery scale-revised: measurement characteristics and diagnostic utility. Arch. Phys. Med. Rehabil. 85 (2004), 2020–2029, 10.1016/j.apmr.2004.02.033.
Giacino, J.T., Schnakers, C., Rodriguez-Moreno, D., et al. Behavioral assessment in patients with disorders of consciousness: gold standard or fool's gold?. Prog. Brain Res. 177 (2009), 33–48, 10.1016/S0079-6123(09)17704-X.
Golkowski, D., Merz, K., Mlynarcik, C., et al. Simultaneous EEG-PET-fMRI measurements in disorders of consciousness: an exploratory study on diagnosis and prognosis. J. Neurol. 264 (2017), 1986–1995, 10.1007/s00415-017-8591-z.
Gui, P., Jiang, Y., Zang, D., et al. Assessing the depth of language processing in patients with disorders of consciousness. Nat. Neurosci. 23 (2020), 761–770, 10.1038/s41593-020-0639-1.
Kerlin, J.R., Shahin, A.J., Miller, L.M., Attentional gain control of ongoing cortical speech representations in a “cocktail party”. J. Neurosci. 30 (2010), 620–628, 10.1523/JNEUROSCI.3631-09.2010.
Kim, E.J., Park, J.M., Kim, W.H., et al. A learning set up for detecting minimally conscious state (MCS). Ann. Rehabil. Med. 36 (2012), 428–431, 10.5535/arm.2012.36.3.428.
Koelsch, S., Heinke, W., Sammler, D., Olthoff, D., Auditory processing during deep propofol sedation and recovery from unconsciousness. Clin. Neurophysiol.: Offic. J. Int. Federat. Clin. Neurophysiol. 117 (2006), 1746–1759, 10.1016/j.clinph.2006.05.009.
Kondziella, D., Bender, A., Diserens, K., et al. European academy of neurology guideline on the diagnosis of coma and other disorders of consciousness. Eur. J. Neurol. 27 (2020), 741–756, 10.1111/ene.14151.
Kondziella, D., Friberg, C.K., Frokjaer, V.G., et al. Preserved consciousness in vegetative and minimal conscious states: systematic review and meta-analysis. J. Neurol. Neurosurg. Psychiatr. 87 (2016), 485–492, 10.1136/jnnp-2015-310958.
Kotchoubey, B., Yu, T., Mueller, F., et al. True or false? Activations of language-related areas in patients with disorders of consciousness. Curr. Pharm. Des. 20 (2014), 4239–4247.
Kroenke, K.-M., Kraft, I., Regenbrecht, F., Obrig, H., Lexical learning in mild aphasia: gesture benefit depends on patholinguistic profile and lesion pattern. Cortex 49 (2013), 2637–2649, 10.1016/j.cortex.2013.07.012.
Kubanek, J., Brunner, P., Gunduz, A., et al. The tracking of speech envelope in the human cortex. PLoS ONE, 8, 2013, e53398, 10.1371/journal.pone.0053398.
Kujawa, K., Żurek, A., Gorączko, A., Zurek, G., Application of high-tech solution for memory assessment in patients with disorders of consciousness. Front. Neurol., 13, 2022, 841095, 10.3389/fneur.2022.841095.
Kwiatkowska, A., Lech, M., Odya, P., Czyżewski, A., Post-comatose patients with minimal consciousness tend to preserve reading comprehension skills but neglect syntax and spelling. Sci. Rep., 9, 2019, 19929, 10.1038/s41598-019-56443-6.
Laforge, G., Gonzalez-Lara, L.E., Owen, A.M., Stojanoski, B., Individualized assessment of residual cognition in patients with disorders of consciousness. Neuroimage: Clin., 28, 2020, 102472, 10.1016/j.nicl.2020.102472.
Lalor, E.C., Foxe, J.J., Neural responses to uninterrupted natural speech can be extracted with precise temporal resolution. Eur. J. Neurosci. 31 (2010), 189–193, 10.1111/j.1460-9568.2009.07055.x.
Lancioni, G.E., Bosco, A., Olivetti Belardinelli, M., et al. Assessing learning as a possible sign of consciousness in post-coma persons with minimal responsiveness. Front. Hum. Neurosci., 8, 2014, 25, 10.3389/fnhum.2014.00025.
Laureys, S., Faymonville, M.-E., Degueldre, C., et al. Auditory processing in the vegetative state. Brain 123 (2000), 1589–1601, 10.1093/brain/123.8.1589.
Li, X., Shao, X., Xia, J., Xu, X., The cognitive and neural oscillatory mechanisms underlying the facilitating effect of rhythm regularity on speech comprehension. J. Neuroling. 49 (2019), 155–167, 10.1016/j.jneuroling.2018.05.004.
Marino, S., Bonanno, L., Giorgio, A., Functional connectivity in disorders of consciousness: methodological aspects and clinical relevance. Brain Imaging Behav. 10 (2016), 604–608, 10.1007/s11682-015-9417-1.
Nigri, A., Catricalà, E., Ferraro, S., et al. The neural correlates of lexical processing in disorders of consciousness. Brain Imaging Behav. 11 (2017), 1526–1537, 10.1007/s11682-016-9613-7.
Owen, A.M., Coleman, M.R., Boly, M., et al. Detecting awareness in the vegetative state. Science, 313, 2006, 1402, 10.1126/science.1130197.
Owen, A.M., Coleman, M.R., Menon, D.K., et al. Residual auditory function in persistent vegetative state: a combined PET and fMRI study. Neuropsychol. Rehabil. 15 (2005), 290–306, 10.1080/09602010443000579.
Peñaloza, C., Martin, N., Laine, M., Rodríguez-Fornells, A., Language learning in aphasia: a narrative review and critical analysis of the literature with implications for language therapy. Neurosci. Biobehav. Rev., 141, 2022, 104825, 10.1016/j.neubiorev.2022.104825.
Prinsloo, K.D., Lalor, E.C., General auditory and speech-specific contributions to cortical envelope tracking revealed using auditory chimeras. J. Neurosci. 42 (2022), 7782–7798, 10.1523/JNEUROSCI.2735-20.2022.
Rohaut, B., Faugeras, F., Chausson, N., et al. Probing ERP correlates of verbal semantic processing in patients with impaired consciousness. Neuropsychologia 66 (2015), 279–292, 10.1016/j.neuropsychologia.2014.10.014.
Schiff, N.D., Rodriguez-Moreno, D., Kamal, A., et al. fMRI reveals large-scale network activation in minimally conscious patients. Neurology 64 (2005), 514–523, 10.1212/01.WNL.0000150883.10285.44.
Schnakers, C., Clinical assessment of patients with disorders of consciousness. Arch. Ital. Biol. 150 (2012), 36–43, 10.4449/aib.v150i2.1371.
Snider, S.B., Edlow, B.L., MRI in disorders of consciousness. Curr. Opin. Neurol. 33 (2020), 676–683, 10.1097/WCO.0000000000000873.
Sokoliuk, R., Degano, G., Banellis, L., et al. Covert speech comprehension predicts recovery from acute unresponsive states. Ann. Neurol. 89 (2021), 646–656, 10.1002/ana.25995.
Stender, J., Gosseries, O., Bruno, M.-A., et al. Diagnostic precision of PET imaging and functional MRI in disorders of consciousness: a clinical validation study. Lancet 384 (2014), 514–522, 10.1016/S0140-6736(14)60042-8.
Tuomiranta, L., Grönroos, A.-M., Martin, N., Laine, M., Vocabulary acquisition in aphasia: modality can matter. J. Neuroling. 32 (2014), 42–58, 10.1016/j.jneuroling.2014.08.006.
Vanden Bosch der Nederlanden, C.M., Joanisse, M.F., Grahn, J.A., et al. Familiarity modulates neural tracking of sung and spoken utterances. Neuroimage, 252, 2022, 119049, 10.1016/j.neuroimage.2022.119049.
Vogel, D., Markl, A., Yu, T., et al. Can mental imagery functional magnetic resonance imaging predict recovery in patients with disorders of consciousness?. Arch. Phys. Med. Rehabil. 94 (2013), 1891–1898, 10.1016/j.apmr.2012.11.053.
Wannez, S., Heine, L., Thonnard, M., et al. The repetition of behavioral assessments in diagnosis of disorders of consciousness. Ann. Neurol. 81 (2017), 883–889, 10.1002/ana.24962.
Xu, C., Li, H., Gao, J., et al. Statistical learning in patients in the minimally conscious state. Cereb. Cortex 33 (2023), 2507–2516, 10.1093/cercor/bhac222.
Zou, J., Feng, J., Xu, T., et al. Auditory and language contributions to neural encoding of speech features in noisy environments. Neuroimage 192 (2019), 66–75, 10.1016/j.neuroimage.2019.02.047.
