EEG Alpha and Gamma Modulators Mediate Motion Sickness-Related Spectral Responses

Motion sickness (MS) is a common experience of travelers. To provide insights into brain dynamics associated with MS, this study recruited 19 subjects to participate in an electroencephalogram (EEG) experiment in a virtual-reality driving environment. When riding on consecutive winding roads, subjects experienced postural instability and sensory conflict between visual and vestibular stimuli. Meanwhile, subjects rated their level of MS on a six-point scale. Independent component analysis (ICA) was used to separate the filtered EEG signals into maximally temporally independent components (ICs). Then, reduced logarithmic spectra of ICs of interest, using principal component analysis, were decomposed by ICA again to find spectrally fixed and temporally independent modulators (IMs). Results demonstrated that a higher degree of MS accompanied increased activation of alpha (r = 0.421) and gamma (r =0.478) IMs across remote-independent brain processes, covering motor, parietal and occipital areas. This co-modulatory spectral change in alpha and gamma bands revealed the neurophysiological demand to regulate conflicts among multi-modal sensory systems during MS.

[1]  Scott Makeig,et al.  High-frequency Broadband Modulations of Electroencephalographic Spectra , 2009, Front. Hum. Neurosci..

[2]  Hojjat Adeli,et al.  Fuzzy Synchronization Likelihood with Application to Attention-Deficit/Hyperactivity Disorder , 2011, Clinical EEG and neuroscience.

[3]  W Singer,et al.  Visual feature integration and the temporal correlation hypothesis. , 1995, Annual review of neuroscience.

[4]  Hojjat Adeli,et al.  Probabilistic neural networks for diagnosis of Alzheimer's disease using conventional and wavelet coherence , 2011, Journal of Neuroscience Methods.

[5]  Fiona E. N. LeBeau,et al.  Multiple origins of the cortical gamma rhythm , 2011, Developmental neurobiology.

[6]  Hojjat Adeli,et al.  Fractality and a Wavelet-Chaos-Neural Network Methodology for EEG-Based Diagnosis of Autistic Spectrum Disorder , 2010, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[7]  Hojjat Adeli,et al.  Functional community analysis of brain: A new approach for EEG-based investigation of the brain pathology , 2011, NeuroImage.

[8]  Robert Oostenveld,et al.  Enhanced EEG gamma-band activity reflects multisensory semantic matching in visual-to-auditory object priming , 2008, NeuroImage.

[9]  Juha Karhunen,et al.  Local Linear Independent Component Analysis Based on Clustering , 2000, Int. J. Neural Syst..

[10]  A. Burgess,et al.  Functional connectivity of gamma EEG activity is modulated at low frequency during conscious recollection. , 2002, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[11]  Chin-Teng Lin,et al.  EEG-Based Learning System for Online Motion Sickness Level Estimation in a Dynamic Vehicle Environment , 2013, IEEE Transactions on Neural Networks and Learning Systems.

[12]  J. Kaiser,et al.  Human gamma-frequency oscillations associated with attention and memory , 2007, Trends in Neurosciences.

[13]  P. Fries Neuronal gamma-band synchronization as a fundamental process in cortical computation. , 2009, Annual review of neuroscience.

[14]  T. Stoffregen,et al.  Postural instability precedes motion sickness , 1998, Brain Research Bulletin.

[15]  E. Basar,et al.  Time and frequency analysis of the brain's distributed gamma-band system , 1995 .

[16]  Robert S. Kennedy,et al.  Simulator Sickness Questionnaire: An enhanced method for quantifying simulator sickness. , 1993 .

[17]  A. Engel,et al.  Cognitive functions of gamma-band activity: memory match and utilization , 2004, Trends in Cognitive Sciences.

[18]  Tzyy-Ping Jung,et al.  Tonic and phasic electroencephalographic dynamics during continuous compensatory tracking , 2008, NeuroImage.

[19]  Paul Ferrari,et al.  Self-paced movements induce high-frequency gamma oscillations in primary motor cortex , 2008, NeuroImage.

[20]  R. Oostenveld,et al.  Validating the boundary element method for forward and inverse EEG computations in the presence of a hole in the skull , 2002, Human brain mapping.

[21]  F. L. D. Silva,et al.  Event-related EEG/MEG synchronization and desynchronization: basic principles , 1999, Clinical Neurophysiology.

[22]  E. Basar,et al.  Distributed gamma band responses in the brain studied in cortex, reticular formation, hippocampus and cerebellum. , 1996, The International journal of neuroscience.

[23]  Matthias M. Müller,et al.  Effects of emotional arousal in the cerebral hemispheres: a study of oscillatory brain activity and event-related potentials , 2001, Clinical Neurophysiology.

[24]  Erkki Oja,et al.  An Experimental Comparison of Neural Algorithms for Independent Component Analysis and Blind Separation , 1999, Int. J. Neural Syst..

[25]  T. Stoffregen,et al.  An ecological Theory of Motion Sickness and Postural Instability , 1991 .

[26]  H. Adeli,et al.  Fractality and a Wavelet-chaos-Methodology for EEG-based Diagnosis of Alzheimer Disease , 2011, Alzheimer disease and associated disorders.

[27]  T. Yokoi,et al.  Effects of virtual body motion on visually-induced motion sickness , 2004, The 26th Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[28]  Yuan-Pin Lin,et al.  Co-modulatory spectral changes in independent brain processes are correlated with task performance , 2012, NeuroImage.

[29]  I. Nelken,et al.  Transient Induced Gamma-Band Response in EEG as a Manifestation of Miniature Saccades , 2008, Neuron.

[30]  Senqi Hu,et al.  Correlation of Phasic and Tonic Skin-Conductance Responses with Severity of Motion Sickness Induced by Viewing an Optokinetic Rotating Drum , 2003, Perceptual and motor skills.

[31]  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.

[32]  H. Adeli,et al.  Improved visibility graph fractality with application for the diagnosis of Autism Spectrum Disorder , 2012 .

[33]  P. Fries,et al.  Is synchronized neuronal gamma activity relevant for selective attention? , 2003, Brain Research Reviews.

[34]  H. Adeli,et al.  Intrahemispheric, interhemispheric, and distal EEG coherence in Alzheimer’s disease , 2011, Clinical Neurophysiology.

[35]  R. Stern,et al.  The contribution of expectations to motion sickness symptoms and gastric activity. , 2004, Journal of psychosomatic research.

[36]  L. M. Ward,et al.  Theta modulation of inter-regional gamma synchronization during auditory attention control , 2012, Brain Research.

[37]  E. Basar,et al.  A possible role of evoked alpha in primary sensory processing: common properties of cat intracranial recordings and human EEG and MEG. , 1997, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[38]  Scott J. Wood,et al.  Human otolith–ocular reflexes during off-vertical axis rotation: effect of frequency on tilt–translation ambiguity and motion sickness , 2002, Neuroscience Letters.

[39]  Yoon-Ki Min,et al.  Psychophysiological evaluation of simulator sickness evoked by a graphic simulator. , 2004, Applied ergonomics.

[40]  Miguel Castelo-Branco,et al.  Neural correlates of visual integration in Williams syndrome: Gamma oscillation patterns in a model of impaired coherence , 2013, Neuropsychologia.

[41]  M. Tervaniemi,et al.  Binding symbols and sounds: evidence from event-related oscillatory gamma-band activity. , 2007, Cerebral cortex.

[42]  H. Adeli,et al.  of Depressive Women and Men Spatiotemporal Analysis of Relative Convergence of EEGs Reveals Differences Between Brain Dynamics , 2013 .

[43]  Angelo Gemignani,et al.  The dynamics of EEG gamma responses to unpleasant visual stimuli: From local activity to functional connectivity , 2012, NeuroImage.

[44]  J T Reason,et al.  Motion Sickness Adaptation: A Neural Mismatch Model 1 , 1978, Journal of the Royal Society of Medicine.

[45]  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.

[46]  Tzyy-Ping Jung,et al.  Independent Component Analysis of Electroencephalographic and Event-Related Potential Data , 1998 .

[47]  Tzyy-Ping Jung,et al.  Spatial and temporal EEG dynamics of motion sickness , 2010, NeuroImage.

[48]  M. Volkmer Theoretical analysis of a time-frequency-pcnn auditory cortex model , 2005, Int. J. Neural Syst..

[49]  R. Oostenveld,et al.  Theta and Gamma Oscillations Predict Encoding and Retrieval of Declarative Memory , 2006, The Journal of Neuroscience.

[50]  S. Hu,et al.  Systematic investigation of physiological correlates of motion sickness induced by viewing an optokinetic rotating drum. , 1999, Aviation, space, and environmental medicine.

[51]  H. Adeli,et al.  Fractality analysis of frontal brain in major depressive disorder. , 2012, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[52]  S Makeig,et al.  Blind separation of auditory event-related brain responses into independent components. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[53]  Colin Fyfe,et al.  Stochastic ICA Contrast Maximisation Using Oja's Nonlinear PCA Algorithm , 1997, Int. J. Neural Syst..

[54]  M. Hallett,et al.  Neural correlates of cross-modal binding , 2003, Nature Neuroscience.

[55]  Terrence J. Sejnowski,et al.  An Information-Maximization Approach to Blind Separation and Blind Deconvolution , 1995, Neural Computation.

[56]  Juha Karhunen,et al.  Advances in blind source separation (BSS) and independent component analysis (ICA) for nonlinear mixtures , 2004, Int. J. Neural Syst..

[57]  Bob Cheung,et al.  Perspectives of electrogastrography and motion sickness , 1998, Brain Research Bulletin.

[58]  Hojjat Adeli,et al.  New diagnostic EEG markers of the Alzheimer’s disease using visibility graph , 2010, Journal of Neural Transmission.

[59]  W. Freeman Mass action in the nervous system : examination of the neurophysiological basis of adaptive behavior through the EEG , 1975 .

[60]  Andreas Schulze-Bonhage,et al.  Movement related activity in the high gamma range of the human EEG , 2008, NeuroImage.

[61]  A. Angrilli,et al.  Language-related gamma EEG frontal reduction is associated with positive symptoms in schizophrenia patients , 2015, Schizophrenia Research.

[62]  Hojjat Adeli,et al.  Principal Component Analysis-Enhanced Cosine Radial Basis Function Neural Network for Robust Epilepsy and Seizure Detection , 2008, IEEE Transactions on Biomedical Engineering.

[63]  Hojjat Adeli,et al.  Wavelet-Synchronization Methodology: A New Approach for EEG-Based Diagnosis of ADHD , 2010, Clinical EEG and neuroscience.

[64]  T. Russomano,et al.  Development and validation of an electrically controlled rotatory chair to be used as a simulator for spatial disorientation and motion sickness , 2003, Proceedings of the 25th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (IEEE Cat. No.03CH37439).

[65]  Walter J. Freeman,et al.  A neurobiological theory of meaning in perception , 2003, Proceedings of the International Joint Conference on Neural Networks, 2003..

[66]  H. Adeli,et al.  Visibility graph similarity: A new measure of generalized synchronization in coupled dynamic systems , 2012 .

[67]  H. Adeli,et al.  Graph Theoretical Analysis of Organization of Functional Brain Networks in ADHD , 2012, Clinical EEG and neuroscience.

[68]  Tzyy-Ping Jung,et al.  Neural Correlates of Mathematical Problem Solving , 2015, Int. J. Neural Syst..

[69]  D. Senkowski,et al.  Effects of task difficulty on evoked gamma activity and ERPs in a visual discrimination task , 2002, Clinical Neurophysiology.

[70]  E. Basar,et al.  Gamma, alpha, delta, and theta oscillations govern cognitive processes. , 2001, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[71]  E. Basar,et al.  Alpha oscillations in brain functioning: an integrative theory. , 1997, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[73]  M. Benedek,et al.  EEG alpha synchronization is related to top-down processing in convergent and divergent thinking , 2011, Neuropsychologia.

[74]  K. R. Ridderinkhof,et al.  EEG Source Reconstruction Reveals Frontal-Parietal Dynamics of Spatial Conflict Processing , 2013, PloS one.

[75]  T. Sejnowski,et al.  Analysis and visualization of single‐trial event‐related potentials , 2001, Human brain mapping.

[76]  W. Klimesch,et al.  EEG alpha oscillations: The inhibition–timing hypothesis , 2007, Brain Research Reviews.