MMN and Novelty P3 in Coma and Other Altered States of Consciousness: A Review

In recent decades, there has been a growing interest in the assessment of patients in altered states of consciousness. There is a need for accurate and early prediction of awakening and recovery from coma. Neurophysiological assessment of coma was once restricted to brainstem auditory and primary cortex somatosensory evoked potentials elicited in the 30 ms range, which have both shown good predictive value for poor coma outcome only. In this paper, we review how passive auditory oddball paradigms including deviant and novel sounds have proved their efficiency in assessing brain function at a higher level, without requiring the patient’s active involvement, thus providing an enhanced tool for the prediction of coma outcome. The presence of an MMN in response to deviant stimuli highlights preserved automatic sensory memory processes. Recorded during coma, MMN has shown high specificity as a predictor of recovery of consciousness. The presence of a novelty P3 in response to the subject’s own first name presented as a novel (rare) stimulus has shown a good correlation with coma awakening. There is now a growing interest in the search for markers of consciousness, if there are any, in unresponsive patients (chronic vegetative or minimally conscious states). We discuss the different ERP patterns observed in these patients. The presence of novelty P3, including parietal components and possibly followed by a late parietal positivity, raises the possibility that some awareness processes are at work in these unresponsive patients.

[1]  R. Näätänen,et al.  The mismatch negativity (MMN) – A unique window to disturbed central auditory processing in ageing and different clinical conditions , 2012, Clinical Neurophysiology.

[2]  Multi-Society Task Force on Pvs Medical aspects of the persistent vegetative state (1). , 1994, The New England journal of medicine.

[3]  Foss Mv MANAGEMENT OF VIRUS HEPATITIS. , 1964 .

[4]  T. Picton,et al.  The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. , 1987, Psychophysiology.

[5]  Dominique Morlet,et al.  Late auditory and event-related potentials can be useful to predict good functional outcome after coma. , 2005, Archives of physical medicine and rehabilitation.

[6]  T. Lewis,et al.  Event-related potentials — neurophysiological tools for predicting emergence and early outcome from traumatic coma , 2005, Intensive Care Medicine.

[7]  C. Delpuech,et al.  Subject's own name as a novel in a MMN design: A combined ERP and PET study , 2008, Brain Research.

[8]  AH Chowdhury,et al.  Assessment of coma and impaired consciousness : A critical review , 2009 .

[9]  O. Bertrand,et al.  Brain reactivity differentiates subjects with high and low dream recall frequencies during both sleep and wakefulness. , 2014, Cerebral cortex.

[10]  F. Angeleri,et al.  Eliciting P300 in comatose patients , 1995, The Lancet.

[11]  Dominique Morlet,et al.  Novelty P3 elicited by the subject’s own name in comatose patients , 2008, Clinical Neurophysiology.

[12]  N. Birbaumer,et al.  Stimulus complexity enhances auditory discrimination in patients with extremely severe brain injuries , 2003, Neuroscience Letters.

[13]  Henry L. Lew,et al.  Predictive value of somatosensory evoked potentials for awakening from coma* , 2003, Critical care medicine.

[14]  B. Jennett,et al.  Assessment of coma and impaired consciousness. A practical scale. , 1974, Lancet.

[15]  T. Curran Effects of attention and confidence on the hypothesized ERP correlates of recollection and familiarity , 2004, Neuropsychologia.

[16]  L. Garcia-Larrea,et al.  P3, positive slow wave and working memory load: a study on the functional correlates of slow wave activity. , 1998, Electroencephalography and clinical neurophysiology.

[17]  E Donchin,et al.  A new method for off-line removal of ocular artifact. , 1983, Electroencephalography and clinical neurophysiology.

[18]  C. Fischer,et al.  Evoked potentials for the prediction of vegetative state in the acute stage of coma , 2005, Neuropsychological Rehabilitation.

[19]  Karl J. Friston,et al.  Preserved Feedforward But Impaired Top-Down Processes in the Vegetative State , 2011, Science.

[20]  Ewout W Steyerberg,et al.  A systematic review finds methodological improvements necessary for prognostic models in determining traumatic brain injury outcomes. , 2008, Journal of clinical epidemiology.

[21]  C. Fischer,et al.  Improved prediction of awakening or nonawakening from severe anoxic coma using tree-based classification analysis* , 2006, Critical care medicine.

[22]  J. Connolly,et al.  Finding a way in: A review and practical evaluation of fMRI and EEG for detection and assessment in disorders of consciousness , 2013, Neuroscience & Biobehavioral Reviews.

[23]  P. Alku,et al.  Event-related potentials associated with sound discrimination versus novelty detection in children. , 2004, Psychophysiology.

[24]  J. Bernat Chronic disorders of consciousness , 2006, The Lancet.

[25]  R. Näätänen,et al.  Early selective-attention effect on evoked potential reinterpreted. , 1978, Acta psychologica.

[26]  E. John,et al.  Evoked-Potential Correlates of Stimulus Uncertainty , 1965, Science.

[27]  J. Connolly,et al.  Assessment of working memory abilities using an event-related brain potential (ERP)-compatible digit span backward task , 2005, Clinical Neurophysiology.

[28]  S. R. Butler,et al.  Electrophysiological indicator of awakening from coma , 1993, The Lancet.

[29]  J. Giacino,et al.  The JFK Coma Recovery Scale-Revised: measurement characteristics and diagnostic utility. , 2004, Archives of physical medicine and rehabilitation.

[30]  Claude Delpuech,et al.  Brain responses to a subject's own name uttered by a familiar voice , 2006, Brain Research.

[31]  K. Alho,et al.  Separate Time Behaviors of the Temporal and Frontal Mismatch Negativity Sources , 2000, NeuroImage.

[32]  J. Hohnsbein,et al.  Effects of choice complexity on different subcomponents of the late positive complex of the event-related potential. , 1994, Electroencephalography and clinical neurophysiology.

[33]  Walter G Sannita,et al.  Unresponsive wakefulness syndrome: a new name for the vegetative state or apallic syndrome , 2010, BMC medicine.

[34]  C. Stoutenbeek,et al.  Systematic review of early prediction of poor outcome in anoxicischaemic coma , 1998, The Lancet.

[35]  B Jennett,et al.  Assessment of outcome after severe brain damage. , 1975, Lancet.

[36]  F. Perrin,et al.  Separate Representation of Stimulus Frequency, Intensity, and Duration in Auditory Sensory Memory: An Event-Related Potential and Dipole-Model Analysis , 1995, Journal of Cognitive Neuroscience.

[37]  D. Guthrie,et al.  Significance testing of difference potentials. , 1991, Psychophysiology.

[38]  R. Näätänen,et al.  Auditory frequency discrimination and event-related potentials. , 1985, Electroencephalography and clinical neurophysiology.

[39]  M. Kronbichler,et al.  Preserved oscillatory response but lack of mismatch negativity in patients with disorders of consciousness , 2011, Clinical Neurophysiology.

[40]  D. Jolley,et al.  Accuracy of clinical signs, SEP, and EEG in predicting outcome of hypoxic coma , 2010, Neurology.

[41]  Lucas Spierer,et al.  Progression of auditory discrimination based on neural decoding predicts awakening from coma. , 2013, Brain : a journal of neurology.

[42]  D Morlet,et al.  Mismatch negativity and late auditory evoked potentials in comatose patients , 1999, Clinical Neurophysiology.

[43]  B. Efron Bootstrap Methods: Another Look at the Jackknife , 1979 .

[44]  J. Bernat Questions remaining about the minimally conscious state. , 2002, Neurology.

[45]  Carles Escera,et al.  Spatiotemporal dynamics of the auditory novelty-P3 event-related brain potential. , 2003, Brain research. Cognitive brain research.

[46]  C. Fischer,et al.  Event-related potentials (MMN and novelty P3) in permanent vegetative or minimally conscious states , 2010, Clinical Neurophysiology.

[47]  David Hinkley,et al.  Bootstrap Methods: Another Look at the Jackknife , 2008 .

[48]  D. Friedman,et al.  The novelty P3: an event-related brain potential (ERP) sign of the brain's evaluation of novelty , 2001, Neuroscience & Biobehavioral Reviews.

[49]  Henry L. Lew,et al.  Prognostic Value of Evoked and Event‐related Potentials in Moderate to Severe Brain Injury , 2006, The Journal of head trauma rehabilitation.

[50]  B. Kotchoubey,et al.  Predicting coma and other low responsive patients outcome using event-related brain potentials: A meta-analysis , 2007, Clinical Neurophysiology.

[51]  B. Jennett,et al.  ASSESSMENT OF OUTCOME AFTER SEVERE BRAIN DAMAGE A Practical Scale , 1975, The Lancet.

[52]  S. Dehaene,et al.  Neural signature of the conscious processing of auditory regularities , 2009, Proceedings of the National Academy of Sciences.

[53]  J. Giacino,et al.  The minimally conscious state: Definition and diagnostic criteria , 2002, Neurology.

[54]  N. Birbaumer,et al.  Information processing in severe disorders of consciousness: Vegetative state and minimally conscious state , 2005, Clinical Neurophysiology.

[55]  Dominique Morlet,et al.  Predictive value of sensory and cognitive evoked potentials for awakening from coma , 2004, Neurology.

[56]  Perrine Ruby,et al.  What is the specificity of the response to the own first-name when presented as a novel in a passive oddball paradigm? An ERP study , 2012, Brain Research.

[57]  C. Zauner,et al.  Detection of nontraumatic comatose patients with no benefit of intensive care treatment by recording of sensory evoked potentials. , 1996, Archives of neurology.

[58]  Multi-Society Task Force on Pvs Medical aspects of the persistent vegetative state (2). , 1994, The New England journal of medicine.

[59]  David Friedman,et al.  Stimulus characteristics and task category dissociate the anterior and posterior aspects of the novelty P3. , 2003, Psychophysiology.

[60]  Perrine Ruby,et al.  Odd Sound Processing in the Sleeping Brain , 2008, Journal of Cognitive Neuroscience.

[61]  J. R. King,et al.  Single-trial decoding of auditory novelty responses facilitates the detection of residual consciousness , 2013, NeuroImage.

[62]  R. Ilmoniemi,et al.  Test–retest reliability of mismatch negativity for duration, frequency and intensity changes , 1999, Clinical Neurophysiology.

[63]  B. de Gelder,et al.  Mismatch negativity predicts recovery from the vegetative state , 2007, Clinical Neurophysiology.

[64]  Juan Lu,et al.  Prognostic value of the Glasgow Coma Scale and pupil reactivity in traumatic brain injury assessed pre-hospital and on enrollment: an IMPACT analysis. , 2007, Journal of neurotrauma.