Unraveling nonlinear electrophysiologic processes in the human visual system with full dimension spectral analysis

Natural sensory signals have nonlinear structures dynamically composed of the carrier frequencies and the variation of the amplitude (i.e., envelope). How the human brain processes the envelope information is still poorly understood, largely due to the conventional analysis failing to quantify it directly. Here, we used a recently developed method, Holo-Hilbert spectral analysis, and steady-state visually evoked potential collected using electroencephalography (EEG) recordings to investigate how the human visual system processes the envelope of amplitude-modulated signals, in this case with a 14 Hz carrier and a 2 Hz envelope. The EEG results demonstrated that in addition to the fundamental stimulus frequencies, 4 Hz amplitude modulation residing in 14 Hz carrier and a broad range of carrier frequencies covering from 8 to 32 Hz modulated by 2 Hz amplitude modulation are also found in the two-dimensional frequency spectrum, which have not yet been recognized before. The envelope of the stimulus is also found to dominantly modulate the response to the incoming signal. The findings thus reveal that the electrophysiological response to amplitude-modulated stimuli is more complex than could be revealed by, for example, Fourier analysis. This highlights the dynamics of neural processes in the visual system.

[1]  Leontios J. Hadjileontiadis,et al.  Swarm decomposition: A novel signal analysis using swarm intelligence , 2017, Signal Process..

[2]  A Stefanovska,et al.  Detecting the harmonics of oscillations with time-variable frequencies. , 2011, Physical review. E, Statistical, nonlinear, and soft matter physics.

[3]  E. Harth,et al.  Electric Fields of the Brain: The Neurophysics of Eeg , 2005 .

[4]  M. Breakspear.  Dynamic models of large-scale brain activity , 2017, Nature Neuroscience.

[5]  ILONA KOVÁCS,et al.  Non-Fourier Information in Bandpass Noise Patterns , 1997, Vision Research.

[6]  R. Blake.  A Neural Theory of Binocular Rivalry , 1989 .

[7]  M. P. Regan,et al.  Objective Investigation of Visual Function Using a Nondestructive Zoom-FFT Technique for Evoked Potential Analysis , 1989, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[8]  H. Spekreijse,et al.  Interocular sustained suppression: correlations with evoked potential amplitude and distribution. , 1972, Vision research.

[9]  Dick Reits,et al.  SEQUENTIAL ANALYSIS OF THE VISUAL EVOKED POTENTIAL SYSTEM IN MAN; NONLINEAR ANALYSIS OF A SANDWICH SYSTEM * , 1980, Annals of the New York Academy of Sciences.

[10]  C. Baker,et al.  Temporal and spatial response to second-order stimuli in cat area 18. , 1998, Journal of neurophysiology.

[11]  Aneta Stefanovska,et al.  Reconstructing Time-Dependent Dynamics , 2016, Proceedings of the IEEE.

[12]  G. Lennerstrand.  BINOCULAR INTERACTION STUDIED WITH VISUAL EVOKED RESPONSES (VER) IN HUMANS WITH NORMAL OR IMPAIRED BINOCULAR VISION , 1978, Acta ophthalmologica.

[13]  V Zemon,et al.  Electrophysiological tests of neural models: evidence for nonlinear binocular interactions in humans. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[14]  N. Huang,et al.  The empirical mode decomposition and the Hilbert spectrum for nonlinear and non-stationary time series analysis , 1998, Proceedings of the Royal Society of London. Series A: Mathematical, Physical and Engineering Sciences.

[15]  D. Spinelli,et al.  Spatiotemporal analysis of the cortical sources of the steady‐state visual evoked potential , 2007, Human brain mapping.

[16]  E. Spaak,et al.  Discriminating Valid from Spurious Indices of Phase-Amplitude Coupling , 2016, eNeuro.

[17]  R. Srinivasan,et al.  Nonlinear SSVEP responses are sensitive to the perceptual binding of visual hemifields during conventional ‘eye’ rivalry and interocular ‘percept’ rivalry , 2009, Brain Research.

[18]  N. Issa,et al.  Subcortical Representation of Non-Fourier Image Features , 2010, The Journal of Neuroscience.

[19]  Steven A. Hillyard,et al.  Global Facilitation of Attended Features Is Obligatory and Restricts Divided Attention , 2013, The Journal of Neuroscience.

[20]  André Longtin,et al.  Contrast coding in the electrosensory system: parallels with visual computation , 2015, Nature Reviews Neuroscience.

[21]  G. Buzsáki,et al.  The log-dynamic brain: how skewed distributions affect network operations , 2014, Nature Reviews Neuroscience.

[22]  A. Cichocki,et al.  Steady-state visually evoked potentials: Focus on essential paradigms and future perspectives , 2010, Progress in Neurobiology.

[23]  A. Cowey,et al.  Perception of first‐ and second‐order motion: Separable neurological mechanisms? , 1999, Human brain mapping.

[24]  A. Norcia,et al.  A method for investigating binocular rivalry in real-time with the steady-state VEP , 1997, Vision Research.

[25]  Justin M. Ales,et al.  The steady-state visual evoked potential in vision research: A review. , 2015, Journal of vision.

[26]  D. Regan.  Some characteristics of average steady-state and transient responses evoked by modulated light. , 1966, Electroencephalography and clinical neurophysiology.

[27]  W. Miles.  Ocular dominance in human adults. , 1930 .

[28]  N. Huang,et al.  On Holo-Hilbert spectral analysis: a full informational spectral representation for nonlinear and non-stationary data , 2016, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[29]  C. Stam,et al.  Nonlinear dynamical analysis of EEG and MEG: Review of an emerging field , 2005, Clinical Neurophysiology.

[30]  Søren K. Andersen,et al.  Driving steady-state visual evoked potentials at arbitrary frequencies using temporal interpolation of stimulus presentation , 2015, BMC Neuroscience.

[31]  C. Baker,et al.  First- and second-order information in natural images: a filter-based approach to image statistics. , 2004, Journal of the Optical Society of America. A, Optics, image science, and vision.

[32]  D. Regan,et al.  Objective evidence for phase-independent spatial frequency analysis in the human visual pathway , 1988, Vision Research.

[33]  Floyd Ratliff,et al.  Intermodulation components of the visual evoked potential: Responses to lateral and superimposed stimuli , 2004, Biological Cybernetics.

[34]  R. Blake,et al.  Temporal perturbations of binocular rivalry , 1990, Perception & psychophysics.

[35]  Ari Rosenberg,et al.  The Y Cell Visual Pathway Implements a Demodulating Nonlinearity , 2011, Neuron.

[36]  André Longtin,et al.  The cellular basis for parallel neural transmission of a high-frequency stimulus and its low-frequency envelope , 2006, Proceedings of the National Academy of Sciences.

[37]  M. R. Harter,et al.  An objective indicant of binocular vision in humans: size-specific interocular suppression of visual evoked potentials. , 1977, Electroencephalography and clinical neurophysiology.

[38]  D. Hubel,et al.  Receptive fields, binocular interaction and functional architecture in the cat's visual cortex , 1962, The Journal of physiology.

[39]  Peng Zhang,et al.  Binocular Rivalry Requires Visual Attention , 2011, Neuron.

[40]  J V Odom,et al.  Models of binocular luminance interaction evaluated using visually evoked potential and psychophysical measures: a tribute to M. Russell Harter. , 1995, The International journal of neuroscience.

[41]  C. Baker,et al.  Processing of second-order stimuli in the visual cortex. , 2001, Progress in brain research.

[42]  M. Bianciardi,et al.  Single-epoch analysis of interleaved evoked potentials and fMRI responses during steady-state visual stimulation , 2009, Clinical Neurophysiology.

[43]  L. H. Tweel,et al.  Linearization of Evoked Responses to Sine Wave-modulated Light by Noise , 1965, Nature.

[44]  P. Müller-Preuss,et al.  Auditory responsive cortex in the squirrel monkey: neural responses to amplitude-modulated sounds , 1996, Experimental Brain Research.

[45]  H Spekreijse,et al.  Flicker responses in monkey lateral geniculate nucleus and human perception of flicker. , 1971, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Aneta Stefanovska,et al.  Chronotaxic systems: a new class of self-sustained nonautonomous oscillators. , 2013, Physical review letters.

[47]  S. Cole,et al.  Brain Oscillations and the Importance of Waveform Shape , 2017, Trends in Cognitive Sciences.

[48]  R. Oostenveld,et al.  Nonparametric statistical testing of EEG- and MEG-data , 2007, Journal of Neuroscience Methods.

[49]  G. Zanette,et al.  Binocular interaction in normal vision studied by pattern-reversal visual evoked potentials (PR-VEPS) , 1997, The Italian Journal of Neurological Sciences.

[50]  G. Trick,et al.  Interocular luminance differences and the binocular pattern-reversal visual-evoked response. , 1982, Investigative ophthalmology & visual science.

[51]  E. Adachi-Usami,et al.  Binocular interaction reflected in visually evoked cortical potentials as studied with pseudorandom stimuli. , 2002, Investigative ophthalmology & visual science.

[52]  R. C. Macridis.  A review , 1963 .

[53]  J. B. Demb,et al.  Cellular Basis for the Response to Second-Order Motion Cues in Y Retinal Ganglion Cells , 2001, Neuron.

[54]  D. Levi,et al.  Evidence for nonlinear binocular interactions in human visual cortex , 1988, Vision Research.

[55]  C L Baker,et al.  A processing stream in mammalian visual cortex neurons for non-Fourier responses. , 1993, Science.

[56]  Daniel H Baker,et al.  Binocular Summation Revisited: Beyond √2 , 2018, Psychological bulletin.

[57]  Aneta Stefanovska,et al.  Nonlinear mode decomposition: a noise-robust, adaptive decomposition method. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[58]  S. Nakagawa,et al.  Visual sensitivity and cortical response to the temporal envelope of amplitude-modulated flicker. , 2009, Journal of the Optical Society of America. A, Optics, image science, and vision.

[59]  G. Sperling,et al.  Drift-balanced random stimuli: a general basis for studying non-Fourier motion perception. , 1988, Journal of the Optical Society of America. A, Optics and image science.

[60]  Eero P. Simoncelli,et al.  Natural signal statistics and sensory gain control , 2001, Nature Neuroscience.