Cortical source of blink‐related delta oscillations and their correlation with levels of consciousness

Recently, blink‐related delta oscillations (delta BROs) have been observed in healthy subjects during spontaneous blinking at rest. Delta BROs have been linked with continuous gathering of information from the surrounding environment, which is classically attributed to the precuneus. Furthermore, fMRI studies have shown that precuneal activity is reduced or missing when consciousness is low or absent. We therefore hypothesized that the source of delta BROs in healthy subjects could be located in the precuneus and that delta BROs could be absent or reduced in patients with disorders of consciousness (DOC). To test these hypotheses, electroencephalographic (EEG) activity at rest was recorded in 12 healthy controls and nine patients with DOC (four vegetative states, and five minimally conscious states). Three‐second‐lasting EEG epochs centred on each blink instance were analyzed in both time‐ (BROs) and frequency domains (event‐related spectral perturbation or ERSP and intertrial coherence or ITC). Cortical sources of the maximum blink‐related delta power, corresponding to the positive peak of the delta BROs, were estimated by standardized Low Resolution Electromagnetic Tomography. In control subjects, as expected, the source of delta BROs was located in the precuneus, whereas in DOC patients, delta BROs were not recognizable and no precuneal localization was possible. Furthermore, we observed a direct relationship between spectral indexes and levels of cognitive functioning in all subjects participating in the study. This reinforces the hypothesis that delta BROs reflect neural processes linked with awareness of the self and of the environment. Hum Brain Mapp 34:2178–2189, 2013. © 2012 Wiley Periodicals, Inc.

[1]  G. Karmos,et al.  Entrainment of Neuronal Oscillations as a Mechanism of Attentional Selection , 2008, Science.

[2]  M. Boly,et al.  Diagnostic accuracy of the vegetative and minimally conscious state: Clinical consensus versus standardized neurobehavioral assessment , 2009, BMC neurology.

[3]  B. Jennett.  The vegetative state , 2002, Journal of neurology, neurosurgery, and psychiatry.

[4]  Jürgen Kayser,et al.  In search of the Rosetta Stone for scalp EEG: Converging on reference-free techniques , 2010, Clinical Neurophysiology.

[5]  D. Schacter,et al.  The Brain's Default Network , 2008, Annals of the New York Academy of Sciences.

[6]  C. Phillips,et al.  Impaired Effective Cortical Connectivity in Vegetative State: Preliminary Investigation Using PET , 1999, NeuroImage.

[7]  Luca Bonfiglio,et al.  Reciprocal dynamics of EEG alpha and delta oscillations during spontaneous blinking at rest: a survey on a default mode-based visuo-spatial awareness. , 2011, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[8]  I. Fekete,et al.  Theta EEG source localization using LORETA in partial epilepsy patients with and without medication , 2010, Clinical Neurophysiology.

[9]  F. Chollet,et al.  Wakefulness and loss of awareness , 2010, Neurology.

[10]  I. Selesnick,et al.  Conjugate eye movements and gamma power modulation of the EEG in persistent vegetative state , 2006, Journal of the Neurological Sciences.

[11]  P. Goldman-Rakic.  Topography of cognition: parallel distributed networks in primate association cortex. , 1988, Annual review of neuroscience.

[12]  B. Rossi,et al.  Spontaneous blinking behaviour in persistent vegetative and minimally conscious states: Relationships with evolution and outcome , 2005, Brain Research Bulletin.

[13]  Steven Laureys,et al.  Brain function in coma, vegetative state, and related disorders , 2004, The Lancet Neurology.

[14]  R. Malach,et al.  Reaching across the abyss: recent advances in functional magnetic resonance imaging and their potential relevance to disorders of consciousness. , 2009, Progress in brain research.

[15]  Geraint Rees,et al.  Two distinct neural effects of blinking on human visual processing , 2005, NeuroImage.

[16]  Steven Laureys,et al.  Posterior cingulate, precuneal and retrosplenial cortices: cytology and components of the neural network correlates of consciousness. , 2005, Progress in brain research.

[17]  J. J. Roseman.  Phragmen-Lindelof theorems for some nonlinear elliptic partial differential equations , 1973 .

[18]  S Laureys,et al.  Intrinsic Brain Activity in Altered States of Consciousness , 2008, Annals of the New York Academy of Sciences.

[19]  E. Basar,et al.  Event‐related delta oscillatory responses of Alzheimer patients , 2008, European journal of neurology.

[20]  A. Cavanna,et al.  The precuneus: a review of its functional anatomy and behavioural correlates. , 2006, Brain : a journal of neurology.

[21]  Calixto Machado,et al.  WAKEFULNESS AND LOSS OF AWARENESS: BRAIN AND BRAINSTEM INTERACTION IN THE VEGETATIVE STATE , 2010, Neurology.

[22]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[23]  N. Schiff.  Modeling the minimally conscious state: measurements of brain function and therapeutic possibilities. , 2005, Progress in brain research.

[24]  M. Boly,et al.  Functional connectivity in the default network during resting state is preserved in a vegetative but not in a brain dead patient , 2009, Human brain mapping.

[25]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[26]  Steve Majerus,et al.  Visual fixation in the vegetative state: an observational case series PET study , 2010, BMC neurology.

[27]  W. Klimesch.  EEG alpha and theta oscillations reflect cognitive and memory performance: a review and analysis , 1999, Brain Research Reviews.

[28]  Patrick Berg,et al.  Eyeblinks evoke potentials in the occipital brain region , 1992, Neuroscience Letters.

[29]  M. Boly,et al.  Default network connectivity reflects the level of consciousness in non-communicative brain-damaged patients. , 2010, Brain : a journal of neurology.

[30]  Maurizio Corbetta,et al.  The human brain is intrinsically organized into dynamic, anticorrelated functional networks. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[31]  M. Boly,et al.  Tracking the recovery of consciousness from coma. , 2006, The Journal of clinical investigation.

[32]  H. Petsche,et al.  Synchronization between prefrontal and posterior association cortex during human working memory. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[33]  D. Lehmann,et al.  Functional imaging with low-resolution brain electromagnetic tomography (LORETA): a review. , 2002, Methods and findings in experimental and clinical pharmacology.

[34]  Bruce D. McCandliss,et al.  Possible axonal regrowth in late recovery from the minimally conscious state. , 2006, The Journal of clinical investigation.

[35]  A. Cavanna.  The Precuneus and Consciousness , 2007, CNS Spectrums.

[36]  C. Koch,et al.  Some reflections on visual awareness. , 1990, Cold Spring Harbor symposia on quantitative biology.

[37]  Steven Laureys,et al.  Automated EEG entropy measurements in coma, vegetative state/unresponsive wakefulness syndrome and minimally conscious state. , 2011, Functional neurology.

[38]  A. von Stein,et al.  Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[40]  V. Virsu,et al.  Visual stability during eyeblinks , 1994, Nature.

[41]  Alan C. Evans,et al.  Enhancement of MR Images Using Registration for Signal Averaging , 1998, Journal of Computer Assisted Tomography.

[42]  K. K. Tan,et al.  The spatial location of EEG electrodes: locating the best-fitting sphere relative to cortical anatomy. , 1993, Electroencephalography and clinical neurophysiology.

[43]  Peng Xu,et al.  A comparative study of different references for EEG default mode network: The use of the infinity reference , 2010, Clinical Neurophysiology.

[44]  Luca Bonfiglio,et al.  Blink-related delta oscillations in the resting-state EEG: A wavelet analysis , 2009, Neuroscience Letters.

[45]  Steven Laureys.  The neural correlate of (un)awareness: lessons from the vegetative state , 2005, Trends in Cognitive Sciences.

[46]  Gui Cai,et al.  Application of nonlinear dynamics analysis in assessing unconsciousness: A preliminary study , 2011, Clinical Neurophysiology.

[47]  Peter Fransson,et al.  The precuneus/posterior cingulate cortex plays a pivotal role in the default mode network: Evidence from a partial correlation network analysis , 2008, NeuroImage.

[48]  Erol Başar,et al.  The genesis of human event-related responses explained through the theory of oscillatory neural assemblies , 2000, Neuroscience Letters.

[49]  C. Torrence,et al.  A Practical Guide to Wavelet Analysis. , 1998 .

[50]  D. Lehmann,et al.  Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain. , 1994, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[51]  E. Kirino.  MISMATCH NEGATIVITY CORRELATES WITH DELTA AND THETA EEG POWER IN SCHIZOPHRENIA , 2007, The International journal of neuroscience.

[52]  F. Castellanos,et al.  Spontaneous attentional fluctuations in impaired states and pathological conditions: A neurobiological hypothesis , 2007, Neuroscience & Biobehavioral Reviews.

[53]  Steven Laureys,et al.  The vegetative state , 2010, BMJ : British Medical Journal.

[54]  Justin L. Vincent,et al.  Precuneus shares intrinsic functional architecture in humans and monkeys , 2009, Proceedings of the National Academy of Sciences.

[55]  J. Connolly,et al.  Improving the clinical assessment of consciousness with advances in electrophysiological and neuroimaging techniques , 2010, BMC neurology.

[56]  E. Stein,et al.  Cingulate activation increases dynamically with response speed under stimulus unpredictability. , 2007, Cerebral cortex.

[57]  O. Sporns,et al.  Mapping the Structural Core of Human Cerebral Cortex , 2008, PLoS biology.

[58]  P. Eling,et al.  Brain perfusion and VEP reactivity in occipital and parietal areas are associated to recovery from hypoxic vegetative state , 2007, Journal of the Neurological Sciences.

[59]  Nicola Neumann,et al.  Assessment of cognitive functions in severely paralysed and severely brain-damaged patients: neuropsychological and electrophysiological methods. , 2004, Brain research. Brain research protocols.

[60]  P. Welch.  The use of fast Fourier transform for the estimation of power spectra: A method based on time averaging over short, modified periodograms , 1967 .

[61]  M. Raichle,et al.  Searching for a baseline: Functional imaging and the resting human brain , 2001, Nature Reviews Neuroscience.

[62]  Peter F. Liddle,et al.  Low-frequency EEG oscillations associated with information processing in schizophrenia , 2009, Schizophrenia Research.

[63]  María del Rosario Domínguez-Morales,et al.  Brain function in the minimally conscious state: A quantitative neurophysiological study , 2008, Clinical Neurophysiology.

[64]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[65]  Tzyy-Ping Jung,et al.  Independent Component Analysis of Electroencephalographic Data , 1995, NIPS.

[66]  A. Bol,et al.  Brain glucose metabolism in postanoxic syndrome. Positron emission tomographic study. , 1990, Archives of neurology.

[67]  B. Baars,et al.  Brain, conscious experience and the observing self , 2003, Trends in Neurosciences.

[68]  P Berg,et al.  Eyeblink-related potentials. , 1988, Electroencephalography and clinical neurophysiology.