How to test for phasic modulation of neural and behavioural responses

Research on whether perception or other processes depend on the phase of neural oscillations is rapidly gaining popularity. However, it is unknown which methods are optimally suited to evaluate the hypothesized phase effect. Using a simulation approach, we here test the ability of different methods to detect such an effect on dichotomous (e.g., “hit” vs “miss”) and continuous (e.g., scalp potentials) response variables. We manipulated parameters that characterise the phase effect or define the experimental approach to test for this effect. For each parameter combination and response variable, we identified an optimal method. We found that methods regressing single-trial responses on circular (sine and cosine) predictors perform best for all of the simulated parameters, regardless of the nature of the response variable (dichotomous or continuous). In sum, our study lays a foundation for optimized experimental designs and analyses in future studies investigating the role of phase for neural and behavioural responses. We provide MATLAB code for the statistical methods tested.

[1]  Erich Schröger,et al.  Digital filter design for electrophysiological data – a practical approach , 2015, Journal of Neuroscience Methods.

[2]  C. Kayser Evidence for the Rhythmic Perceptual Sampling of Auditory Scenes , 2019, bioRxiv.

[3]  L. Parra,et al.  Low frequency transcranial electrical stimulation does not entrain sleep rhythms measured by human intracranial recordings , 2017, Nature Communications.

[4]  Gregory Hickok,et al.  The Rhythm of Perception , 2015, Psychological science.

[5]  E. Ziegel Permutation, Parametric, and Bootstrap Tests of Hypotheses (3rd ed.) , 2005 .

[6]  C. Miniussi,et al.  Guiding transcranial brain stimulation by EEG/MEG to interact with ongoing brain activity and associated functions: A position paper , 2017, Clinical Neurophysiology.

[7]  Rachel N. Denison,et al.  Temporal attention improves perception similarly at foveal and parafoveal locations , 2019, Journal of vision.

[8]  Myles Mc Laughlin,et al.  Analytical bias accounts for some of the reported effects of tACS on auditory perception , 2019, Brain Stimulation.

[9]  S. Dalal,et al.  Prestimulus Oscillatory Phase at 7 Hz Gates Cortical Information Flow and Visual Perception , 2013, Current Biology.

[10]  Christoph Kayser,et al.  Consistent pre-stimulus influences on auditory perception across the lifespan , 2018, NeuroImage.

[11]  J. Raaijmakers,et al.  How to deal with "The language-as-fixed-effect fallacy": Common misconceptions and alternative solutions. , 1999 .

[12]  Luis Morís Fernández,et al.  The relevance of alpha phase in human perception , 2019, Cortex.

[13]  L. Tomasevic,et al.  No trace of phase: Corticomotor excitability is not tuned by phase of pericentral mu-rhythm , 2019, bioRxiv.

[14]  Alison Moore,et al.  Making waves. , 2017, Nursing standard (Royal College of Nursing (Great Britain) : 1987).

[15]  EEG-triggered TMS reveals stronger brain state-dependent modulation of motor evoked potentials at weaker stimulation intensities , 2019, Brain Stimulation.

[16]  Lars Riecke,et al.  Endogenous Delta/Theta Sound-Brain Phase Entrainment Accelerates the Buildup of Auditory Streaming , 2015, Current Biology.

[17]  Christoph Kayser,et al.  Prestimulus influences on auditory perception from sensory representations and decision processes , 2016, Proceedings of the National Academy of Sciences.

[18]  R. VanRullen,et al.  Spontaneous EEG oscillations reveal periodic sampling of visual attention , 2010, Proceedings of the National Academy of Sciences.

[19]  Lei Ai,et al.  The phase of prestimulus alpha oscillations affects tactile perception. , 2014, Journal of neurophysiology.

[20]  R. VanRullen,et al.  The Phase of Ongoing EEG Oscillations Predicts Visual Perception , 2009, The Journal of Neuroscience.

[21]  Christoph Kayser,et al.  A Precluding But Not Ensuring Role of Entrained Low-Frequency Oscillations for Auditory Perception , 2012, The Journal of Neuroscience.

[22]  Huan Luo,et al.  Behavioral oscillation in global/local processing: Global alpha oscillations mediate global precedence effect. , 2019, Journal of vision.

[23]  Benedikt Zoefel,et al.  The Involvement of Endogenous Neural Oscillations in the Processing of Rhythmic Input: More Than a Regular Repetition of Evoked Neural Responses , 2018, Front. Neurosci..

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

[25]  The variance of d′ estimates obtained in yes—no and two-interval forced choice procedures , 2005, Perception & psychophysics.

[26]  Alejandro Lleras,et al.  Making Waves in the Stream of Consciousness: Entraining Oscillations in EEG Alpha and Fluctuations in Visual Awareness with Rhythmic Visual Stimulation , 2012, Journal of Cognitive Neuroscience.

[27]  P. Heil,et al.  Detection of Near-Threshold Sounds is Independent of EEG Phase in Common Frequency Bands , 2013, Front. Psychol..

[28]  C. Kayser,et al.  Rhythmic Auditory Cortex Activity at Multiple Timescales Shapes Stimulus–Response Gain and Background Firing , 2015, The Journal of Neuroscience.

[29]  Brian A. Nosek,et al.  The preregistration revolution , 2018, Proceedings of the National Academy of Sciences.

[30]  S. Jones When brain rhythms aren't ‘rhythmic’: implication for their mechanisms and meaning , 2016, Current Opinion in Neurobiology.

[31]  Robert Oostenveld,et al.  Neuronal Oscillations with Non-sinusoidal Morphology Produce Spurious Phase-to-Amplitude Coupling and Directionality , 2016, Front. Comput. Neurosci..

[32]  Diane M. Beck,et al.  To See or Not to See: Prestimulus α Phase Predicts Visual Awareness , 2009, The Journal of Neuroscience.

[33]  G. Buzsáki,et al.  Direct effects of transcranial electric stimulation on brain circuits in rats and humans , 2018, Nature Communications.

[34]  Matthias M. Müller,et al.  Phasic Modulation of Human Somatosensory Perception by Transcranially Applied Oscillating Currents , 2016, Brain Stimulation.

[35]  Vadim V. Nikulin,et al.  Spatial neuronal synchronization and the waveform of oscillations: implications for EEG and MEG , 2019, PLoS Comput. Biol..

[36]  G. Buzsáki,et al.  Neuronal Oscillations in Cortical Networks , 2004, Science.

[37]  Jonas Obleser,et al.  Transcranial alternating current stimulation with speech envelopes modulates speech comprehension , 2018, NeuroImage.

[38]  R. VanRullen,et al.  The Phase of Ongoing Oscillations Mediates the Causal Relation between Brain Excitation and Visual Perception , 2011, The Journal of Neuroscience.

[39]  Jonathan Miller,et al.  Phase-tuned neuronal firing encodes human contextual representations for navigational goals , 2017, bioRxiv.

[40]  Matthew H. Davis,et al.  Transcranial electric stimulation for the investigation of speech perception and comprehension , 2016, Language, cognition and neuroscience.

[41]  R. VanRullen How to Evaluate Phase Differences between Trial Groups in Ongoing Electrophysiological Signals , 2016, bioRxiv.

[42]  Andreas Wutz,et al.  Temporal Integration Windows in Neural Processing and Perception Aligned to Saccadic Eye Movements , 2016, Current Biology.

[43]  Rufin VanRullen,et al.  Selective Perceptual Phase Entrainment to Speech Rhythm in the Absence of Spectral Energy Fluctuations , 2015, The Journal of Neuroscience.

[44]  P. Good Permutation, Parametric, and Bootstrap Tests of Hypotheses , 2005 .

[45]  V. Romei,et al.  Information-Based Approaches of Noninvasive Transcranial Brain Stimulation , 2016, Trends in Neurosciences.

[46]  Rufin VanRullen,et al.  What goes up must come down: EEG phase modulates auditory perception in both directions , 2013, Front. Psychology.

[47]  Carsten H. Wolters,et al.  Good vibrations: Oscillatory phase shapes perception , 2012, NeuroImage.

[48]  Alison Ledgerwood,et al.  The preregistration revolution needs to distinguish between predictions and analyses , 2018, Proceedings of the National Academy of Sciences.

[49]  David Poeppel,et al.  An oscillator model better predicts cortical entrainment to music , 2019, Proceedings of the National Academy of Sciences.

[50]  M. Morrone,et al.  Rhythmic modulation of visual contrast discrimination triggered by action , 2016, Proceedings of the Royal Society B: Biological Sciences.

[51]  R. VanRullen,et al.  Oscillatory Mechanisms of Stimulus Processing and Selection in the Visual and Auditory Systems: State-of-the-Art, Speculations and Suggestions , 2017, Front. Neurosci..

[52]  David Melcher,et al.  Multiple oscillatory rhythms determine the temporal organization of perception , 2017, Proceedings of the National Academy of Sciences.

[53]  J. Obleser,et al.  Entrained neural oscillations in multiple frequency bands comodulate behavior , 2014, Proceedings of the National Academy of Sciences.

[54]  Robert T. Knight,et al.  Parameterizing neural power spectra , 2018, bioRxiv.

[55]  R. VanRullen,et al.  Conscious updating is a rhythmic process , 2012, Proceedings of the National Academy of Sciences.

[56]  C. Herrmann,et al.  Transcranial alternating current stimulation: a review of the underlying mechanisms and modulation of cognitive processes , 2013, Front. Hum. Neurosci..

[57]  Alain de Cheveigné,et al.  Filters: When, Why, and How (Not) to Use Them , 2019, Neuron.

[58]  A. de Cheveigné,et al.  Scanning for oscillations , 2015, Journal of neural engineering.

[59]  Gregor Thut,et al.  Frequency and power of human alpha oscillations drift systematically with time-on-task , 2018, NeuroImage.

[60]  Jonas Obleser,et al.  Alpha Phase Determines Successful Lexical Decision in Noise , 2015, The Journal of Neuroscience.

[61]  Y. Saalmann,et al.  Rhythmic Sampling within and between Objects despite Sustained Attention at a Cued Location , 2013, Current Biology.

[62]  M. Kendall Statistical Methods for Research Workers , 1937, Nature.

[63]  Matthew H. Davis,et al.  Neural Oscillations Carry Speech Rhythm through to Comprehension , 2012, Front. Psychology.

[64]  W. Klimesch Alpha-band oscillations, attention, and controlled access to stored information , 2012, Trends in Cognitive Sciences.

[65]  R. VanRullen,et al.  Ongoing EEG Phase as a Trial-by-Trial Predictor of Perceptual and Attentional Variability , 2011, Front. Psychology.

[66]  Christopher W. Pleydell-Pearce,et al.  The phase of pre-stimulus alpha oscillations influences the visual perception of stimulus timing , 2016, NeuroImage.

[67]  Bradley Voytek,et al.  Cycle-by-cycle analysis of neural oscillations , 2018, bioRxiv.

[68]  P. Fries,et al.  Attention Samples Stimuli Rhythmically , 2012, Current Biology.

[69]  Lars Riecke,et al.  4-Hz Transcranial Alternating Current Stimulation Phase Modulates Hearing , 2015, Brain Stimulation.

[70]  Praveen K. Pilly,et al.  Transcranial alternating current stimulation entrains single-neuron activity in the primate brain , 2019, Proceedings of the National Academy of Sciences.

[71]  M. Leek Adaptive procedures in psychophysical research , 2001, Perception & psychophysics.

[72]  Lucas C. Parra,et al.  Joint decorrelation, a versatile tool for multichannel data analysis , 2014, NeuroImage.

[73]  Bettina Sorger,et al.  Neural Entrainment to Speech Modulates Speech Intelligibility , 2017, Current Biology.

[74]  E. Maris,et al.  Theta oscillations locked to intended actions rhythmically modulate perception , 2017, eLife.

[75]  R. VanRullen,et al.  Different responses of spontaneous and stimulus‐related alpha activity to ambient luminance changes , 2018, The European journal of neuroscience.

[76]  T. Zaehle,et al.  Sailing in a sea of disbelief: In vivo measurements of transcranial electric stimulation in human subcortical structures , 2018, Brain Stimulation.

[77]  John-Dylan Haynes,et al.  Valid population inference for information-based imaging: From the second-level t-test to prevalence inference , 2015, NeuroImage.

[78]  Lars Riecke,et al.  Conveying Temporal Information to the Auditory System via Transcranial Current Stimulation , 2018, Acta Acustica united with Acustica.

[79]  Nachum Ulanovsky,et al.  Nonoscillatory Phase Coding and Synchronization in the Bat Hippocampal Formation , 2018, Cell.

[80]  Matthew H. Davis,et al.  Phase Entrainment of Brain Oscillations Causally Modulates Neural Responses to Intelligible Speech , 2018, Current Biology.

[81]  Ankoor S. Shah,et al.  An oscillatory hierarchy controlling neuronal excitability and stimulus processing in the auditory cortex. , 2005, Journal of neurophysiology.

[82]  Alexander T Sack,et al.  Oscillatory phase shapes syllable perception , 2015, Proceedings of the National Academy of Sciences.

[83]  Floris P. de Lange,et al.  Local Entrainment of Alpha Oscillations by Visual Stimuli Causes Cyclic Modulation of Perception , 2014, The Journal of Neuroscience.

[84]  Joachim Lange,et al.  Beta oscillations define discrete perceptual cycles in the somatosensory domain , 2015, Proceedings of the National Academy of Sciences.

[85]  Gregor Thut,et al.  Visual cortex responses reflect temporal structure of continuous quasi-rhythmic sensory stimulation , 2017, NeuroImage.

[86]  Yi Chen,et al.  Statistical inference and multiple testing correction in classification-based multi-voxel pattern analysis (MVPA): Random permutations and cluster size control , 2011, NeuroImage.

[87]  Anthony M. Harris,et al.  Detecting Unattended Stimuli Depends on the Phase of Prestimulus Neural Oscillations , 2018, The Journal of Neuroscience.

[88]  J. Obleser,et al.  Frequency modulation entrains slow neural oscillations and optimizes human listening behavior , 2012, Proceedings of the National Academy of Sciences.