Estimation of overlapped Eye Fixation Related Potentials: The General Linear Model, a more flexible framework than the ADJAR algorithm

The Eye Fixation Related Potential (EFRP) estimation is the average of EEG signals across epochs at ocular fixation onset. Its main limitation is the overlapping issue. Inter Fixation Intervals (IFI) - typically around 300 ms in the case of unrestricted eye movement- depend on participants’ oculomotor patterns, and can be shorter than the latency of the components of the evoked potential. If the duration of an epoch is longer than the IFI value, more than one fixation can occur, and some overlapping between adjacent neural responses ensues. The classical average does not take into account either the presence of several fixations during an epoch or overlapping. The Adjacent Response algorithm (ADJAR), which is popular for event-related potential estimation, was compared to the General Linear Model (GLM) on a real dataset from a conjoint EEG and eye-tracking experiment to address the overlapping issue. The results showed that the ADJAR algorithm was based on assumptions that were too restrictive for EFRP estimation. The General Linear Model appeared to be more robust and efficient. Different configurations of this model were compared to estimate the potential elicited at image onset, as well as EFRP at the beginning of exploration. These configurations took into account the overlap between the event-related potential at stimulus presentation and the following EFRP, and the distinction between the potential elicited by the first fixation onset and subsequent ones. The choice of the General Linear Model configuration was a tradeoff between assumptions about expected behavior and the quality of the EFRP estimation: the number of different potentials estimated by a given model must be controlled to avoid erroneous estimations with large variances.

[1]  A. Yagi Visual signal detection and lambda responses. , 1981, Electroencephalography and clinical neurophysiology.

[2]  Anthony J. Ries,et al.  Automatic Versus Contingent Mechanisms of Sensory-Driven Neural Biasing and Reflexive Attention , 2005, Journal of Cognitive Neuroscience.

[3]  S. Klein,et al.  Neural saccadic response estimation during natural viewing. , 2012, Journal of neurophysiology.

[4]  S Kanaya,et al.  Brain potentials associated with eye fixations during visual tasks under different lighting systems. , 1998, Ergonomics.

[5]  H. Jasper,et al.  The ten-twenty electrode system of the International Federation. The International Federation of Clinical Neurophysiology. , 1999, Electroencephalography and clinical neurophysiology. Supplement.

[6]  H. Abdi The General Linear Model , 2009 .

[7]  Jacek P Dmochowski,et al.  EEG precursors of detected and missed targets during free-viewing search. , 2013, Journal of vision.

[8]  Barak A. Pearlmutter,et al.  The VESPA: A method for the rapid estimation of a visual evoked potential , 2006, NeuroImage.

[9]  Cees van Leeuwen,et al.  Combining EEG and eye movement recording in free viewing: Pitfalls and possibilities , 2016, Brain and Cognition.

[10]  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.

[11]  G. Thickbroom,et al.  Saccade onset and offset lambda waves: relation to pattern movement visually evoked potentials , 1991, Brain Research.

[12]  M. Woldorff,et al.  Distortion of ERP averages due to overlap from temporally adjacent ERPs: analysis and correction. , 2007, Psychophysiology.

[13]  Lambda response as an index of visual perception research , 1982 .

[14]  Guillaume Gibert,et al.  xDAWN Algorithm to Enhance Evoked Potentials: Application to Brain–Computer Interface , 2009, IEEE Transactions on Biomedical Engineering.

[15]  Nathalie Guyader,et al.  The P300 potential for fixations onto target object when exploring natural scenes during a visual task after denoising overlapped EFRP , 2015, 2015 7th International IEEE/EMBS Conference on Neural Engineering (NER).

[16]  A M Dale,et al.  Optimal experimental design for event‐related fMRI , 1999, Human brain mapping.

[17]  A. Jacobs,et al.  Coregistration of eye movements and EEG in natural reading: analyses and review. , 2011, Journal of experimental psychology. General.

[18]  Bertrand Rivet,et al.  Regularization and a general linear model for event-related potential estimation , 2017, Behavior Research Methods.

[19]  R G Bickford,et al.  Lambda responses in the human electroencephalogram , 1967, Neurology.

[20]  Kenneth Kreutz-Delgado,et al.  Comparison of averaging and regression techniques for estimating Event Related Potentials , 2013, 2013 35th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).

[21]  Mariano Sigman,et al.  Fixation-related potentials in visual search: a combined EEG and eye tracking study. , 2012, Journal of vision.

[22]  Thom Carney,et al.  The Fixation and Saccade P3 , 2012, PloS one.

[23]  Marty G. Woldorff,et al.  Selective Attention and Multisensory Integration: Multiple Phases of Effects on the Evoked Brain Activity , 2005, Journal of Cognitive Neuroscience.

[24]  Shlomit Yuval-Greenberg,et al.  Saccadic spike potentials in gamma-band EEG: Characterization, detection and suppression , 2010, NeuroImage.

[25]  Boris Reuderink,et al.  Distinguishing between target and nontarget fixations in a visual search task using fixation-related potentials. , 2013, Journal of vision.

[26]  J C ARMINGTON,et al.  Averaged Brain Activity Following Saccadic Eye Movement , 1964, Science.

[27]  Jon Touryan,et al.  The Impact of Task Demands on Fixation-Related Brain Potentials during Guided Search , 2016, PloS one.

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

[29]  Marco Congedo,et al.  Spatio-temporal common pattern: A companion method for ERP analysis in the time domain , 2016, Journal of Neuroscience Methods.

[30]  L Cigánek,et al.  Lambda responses in relation to visual evoked responses in man. , 1969, Electroencephalography and clinical neurophysiology.

[31]  Mariano Sigman,et al.  Looking for a face in the crowd: Fixation-related potentials in an eye-movement visual search task , 2014, NeuroImage.

[32]  B. Velichkovsky,et al.  Attentional dynamics during free picture viewing: Evidence from oculomotor behavior and electrocortical activity , 2013, Front. Syst. Neurosci..

[33]  Harvey Dillon,et al.  Least-squares deconvolution of evoked potentials and sequence optimization for multiple stimuli under low-jitter conditions , 2014, Clinical Neurophysiology.

[34]  R. J. van Beers,et al.  The Sources of Variability in Saccadic Eye Movements , 2007, The Journal of Neuroscience.

[35]  Thierry Baccino,et al.  Decision-making in information seeking on texts: an eye-fixation-related potentials investigation , 2013, Front. Syst. Neurosci..

[36]  Akihiro Yagi,et al.  Saccade size and lambda complex in man , 1979 .

[37]  Nathalie Guyader,et al.  An eye fixation-related potentials analysis of the P300 potential for fixations onto a target object when exploring natural scenes. , 2015, Journal of vision.

[38]  Benjamin W Tatler,et al.  The central fixation bias in scene viewing: selecting an optimal viewing position independently of motor biases and image feature distributions. , 2007, Journal of vision.

[39]  Cees van Leeuwen,et al.  Eye fixation-related potentials in free viewing identify encoding failures in change detection , 2011, NeuroImage.

[40]  A. Newman,et al.  Modeling nonlinear relationships in ERP data using mixed-effects regression with R examples. , 2015, Psychophysiology.

[41]  P. Maldonado,et al.  Superposition Model Predicts EEG Occipital Activity during Free Viewing of Natural Scenes , 2010, The Journal of Neuroscience.

[42]  Thierry Baccino,et al.  Eye movements and concurrent event-related potentials: Eye fixation-related potential investigations in reading , 2011 .