Electromyographic decoding of response to command in disorders of consciousness

Article; Adolescent; Adult; Aged; Child; Cohort Studies; Consciousness Disorders; Electromyography; Female; Humans; Male; Middle Aged; Motor Activity; Muscle, Skeletal; Neuropsychological Tests; Point-of-Care Testing; Speech Perception; Upper Extremity; Young Adult

Abstract :

[en] Objective: To propose a new methodology based on single-trial analysis for detecting residual response to command with EMG in patients with disorders of consciousness (DOC), overcoming the issue of trial dependency and decreasing the influence of a patient's fluctuation of vigilance or arousal over time on diagnostic accuracy. Methods: Forty-five patients with DOC (18 with vegetative/unresponsive wakefulness syndrome [VS/UWS], 22 in a minimally conscious state [MCS], 3 who emerged from MCS [EMCS], and 2 with locked-in syndrome [LIS]) and 20 healthy controls were included in the study. Patients were randomly instructed to either move their left or right hand or listen to a control command ("It is a sunny day") while EMG activity was recorded on both arms. Results: Differential EMG activity was detected in all MCS cases displaying reproducible response to command at bedside on multiple assessments, even though only 6 of the 14 individuals presented a behavioral response to command on the day of the EMG assessment. An EMG response was also detected in all EMCS and LIS patients, and 2 MCS patients showing nonreflexive movements without command following at the bedside. None of the VS/UWS presented a response to command with this method. Conclusions: This method allowed us to reliably distinguish between different levels of consciousness and could potentially help decrease diagnostic errors in patients with motor impairment but presenting residual motor activity. © 2016 American Academy of Neurology.

Disciplines :

Neurology
Neurosciences & behavior

Author, co-author :

Lesenfants, Damien ^✱; Université de Liège - ULiège > Service administratif de la Fac. (FPLSE)

Habbal, Dina ^✱; Coma Science Group, GIGA-Research, CHU University Hospital of Liège, Belgium

Chatelle, Camille ; Université de Liège - ULiège > GIGA : Coma Group

Schnakers, Caroline ; Department of Neurosurgery, UCLA, Los Angeles, CA, United States

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

Noirhomme, Quentin ; Université de Liège - ULiège > Centre de recherches du cyclotron

^✱ These authors have contributed equally to this work.

Language :

English

Title :

Electromyographic decoding of response to command in disorders of consciousness

Publication date :

2016

Journal title :

Neurology

ISSN :

0028-3878

eISSN :

1526-632X

Publisher :

Lippincott Williams and Wilkins

Volume :

Issue :

Pages :

2099-2107

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 15 January 2019

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Bibliography

The Multi-Society Task Force on PVS. Medical aspects of the persistent vegetative state (1). N Engl J Med 1994; 330:1499-1508.
Laureys S, Celesia G, Cohadon F, et al. Unresponsive wakefulness syndrome: a new name for the vegetative state or apallic syndrome. BMC Med 2010;8:68.
von Wild K, Laureys S, Gerstenbrand F, Dolce G, Onose G. The vegetative state: a syndrome in search of a name. J Med Life 2012;5:3-15.
Giacino JT, Ashwal S, Childs N, et al. The minimally conscious state: definition and diagnostic criteria. Neurology 2002;58:349-353.
Laureys S, Perrin F, Schnakers C, Boly M, Majerus S. Residual cognitive function in comatose, vegetative and minimally conscious states. Curr Opin Neurol 2005;18:726-733.
Laureys S, Schiff ND. Coma and consciousness: paradigms (re)framed by neuroimaging. Neuroimage 2012; 61:478-491.
Lovstad M, Froslie KF, Giacino JT, Skandsen T, Anke A, Schanke AK. Reliability and diagnostic characteristics of the JFK coma recovery scale-revised: exploring the influence of rater's level of experience. J Head Trauma Rehabil 2010;25:349-356.
Noirhomme Q, Brecheisen R, Lesenfants D, Antonopoulos G, Laureys S. "Look at my classifier's result": disentangling unresponsive from (minimally) conscious patients. Neuroimage 2015;8119:01119-1122.
Bekinschtein TA, Coleman MR, Niklison J, Pickard JD, Manes FF. Can electromyography objectively detect voluntary movement in disorders of consciousness? J Neurol Neurosurg Psychiatry 2008;79:826-828.
Habbal D, Gosseries O, Noirhomme Q, et al. Volitional electromyographic responses in disorders of consciousness. Brain Inj 2014;28:1171-1179.
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;258:1373-1384.
Bruno MA, Majerus S, Boly M, et al. Functional neuroanatomy underlying the clinical subcategorization of minimally conscious state patients. J Neurol 2012; 259:1087-1098.
Giacino JT, Edlow B, Chatelle C, Schnakers C. The minimally conscious state: clinical features, pathophysiology and therapeutic implications. In: Laureys S, Tononi G, Gosseries O, eds. The Neurology of Consciousness, 2nd ed. Cambridge, MA: Academic Press; 2016.
Laureys S, Pellas F, van Eeckhout P, et al. The locked-in syndrome: what is it like to be conscious but paralyzed and voiceless? Prog Brain Res 2005;150:495-511.
Giacino JT, Kalmar K, Whyte J. The JFK Coma Recovery Scale-Revised: measurement characteristics and diagnostic utility. Arch Phys Med Rehabil 2004;85:2020-2029.
Hugger S, Schindler HJ, Kordass B, Hugger A. Clinical relevance of surface EMG of the masticatory muscles (part 1): resting activity, maximal and submaximal voluntary contraction, symmetry of EMG activity. Int J Comput Dent 2012;15:297-314.
Nöjd N, Hannula M, Narra N, Hyttinen J. Electrode position optimization for facial EMG measurements for humancomputer interface. Methods Inf Med 2008;47:192-197.
Schalk G, McFarland DJ, Hinterberger T, Birbaumer N, Wolpaw JR. BCI2000: a general-purpose brain-computer interface (BCI) system. IEEE Trans Biomed Eng 2004;51: 1034-1043.
Monti MM, Vanhaudenhuyse A, Coleman MR, et al. Willful modulation of brain activity in disorders of consciousness. N Engl J Med 2010;362:579-589.
Stender J, Gosseries O, Bruno MA, et al. Diagnostic precision of PET imaging and functional MRI in disorders of consciousness: a clinical validation study. Lancet 2014; 384:514-522.
Goldfine AM, Victor JD, Conte MM, Bardin JC, Schiff ND. Determination of awareness in patients with severe brain injury using EEG power spectral analysis. Clin Neurophysiol 2011;122:2157-2168.
Cruse D, Chennu S, Chatelle C, et al. Relationship between etiology and covert cognition in the minimally conscious state. Neurology 2012;78:816-822.
King JR, Faugeras F, Gramfort A, et al. Single-trial decoding of auditory novelty responses facilitates the detection of residual consciousness. Neuroimage 2013;83:726-738.
Lulé D, Noirhomme Q, Kleih SC, et al. Probing command following in patients with disorders of consciousness using a brain-computer interface. Clin Neurophysiol 2013;124:101-106.
Pokorny C, Klobassa DS, Pichler G, et al. The auditory P300-based single-switch brain-computer interface: paradigm transition from healthy subjects to minimally conscious patients. Artif Intell Med 2013;59:81-90.
Chatelle C, Lesenfants D, Guller Y, Laureys S, Noirhomme Q. Brain-computer interface for assessing consciousness in severely brain-injured patients. In: Rossetti AO, Laureys S, eds. Clinical Neurophysiology in Disorders of Consciousness. Vienna: Springer-Verlag Wien; 2015: 133-148.
Cruse D, Chennu S, Chatelle C, et al. Bedside detection of awareness in the vegetative state: a cohort study. Lancet 2011;378:2088-2094.
Thibaut A, Chatelle C, Ziegler E, Bruno MA, Laureys S, Gosseries O. Spasticity after stroke: physiology, assessment and treatment. Brain Inj 2013;27:1093-1105.
Nakase-Richardson R, Yablon SA, Sherer M, Nick TG, Evans CC. Emergence from minimally conscious state: insights from evaluation of post-traumatic confusion. Neurology 2009;73:1120-1126.
Schnakers C, Perrin F, Schabus M, et al. Detecting consciousness in a total locked-in syndrome: an active eventrelated paradigm. Neurocase 2009;15:271-277.
Chennu S, Finoia P, Kamau E, et al. Dissociable endogenous and exogenous attention in disorders of consciousness. Neuroimage Clin 2013;3:450-461.
Majerus S, Bruno MA, Schnakers C, Giacino JT, Laureys S. The problem of aphasia in the assessment of consciousness in brain-damaged patients. Prog Brain Res 2009;177:49-61.
Giacino JT. Disorders of consciousness: differential diagnosis and neuropathologic features. Semin Neurol 1997; 17:105-111.
Sandel ME, Mysiw WJ. The agitated brain injured patient: part 1: definitions, differential diagnosis, and assessment. Arch Phys Med Rehabil 1996;77:617-623.
Kleih SC, Nijboer F, Halder S, Kübler A. Motivation modulates the P300 amplitude during brain-computer interface use. Clin Neurophysiol 2010;121:1023-1031.
Nijboer F, Birbaumer N, Kübler A. The influence of psychological state and motivation on brain-computer interface performance in patients with amyotrophic lateral sclerosis: a longitudinal study. Front Neurosci 2010;4:55.