Digital filters for low-latency quantification of brain rhythms in real time

OBJECTIVE The rapidly developing paradigm of closed-loop neuroscience has extensively employed brain rhythms as the signal forming real-time neurofeedback, triggering brain stimulation, or governing stimulus selection. However, the efficacy of brain rhythm contingent paradigms suffers from significant delays related to the process of extraction of oscillatory parameters from broad-band neural signals with conventional methods. To this end, real-time algorithms are needed that would shorten the delay while maintaining an acceptable speed-accuracy trade-off. APPROACH Here we evaluated a family of techniques based on the application of the least-squares complex-valued filter (LSCF) design to real-time quantification of brain rhythms. These techniques allow for explicit optimization of the speed-accuracy trade-off when quantifying oscillatory patterns. We used EEG data collected from 10 human participants to systematically compare LSCF approach to the other commonly used algorithms. Each method being evaluated was optimized by scanning through the grid of its hyperparameters using independent data samples. MAIN RESULTS When applied to the task of estimating oscillatory envelope and phase, the LSCF techniques outperformed in speed and accuracy both conventional Fourier transform and rectification based methods as well as more advanced techniques such as those that exploit autoregressive extrapolation of narrow-band filtered signals. When operating at zero latency, the weighted LSCF approach yielded 75\% accuracy when detecting alpha-activity episodes, as defined by the amplitude crossing of the 95th-percentile threshold. SIGNIFICANCE The LSCF approaches are easily applicable to low-delay quantification of brain rhythms. As such, these methods are useful in a variety of neurofeedback, brain-computer-interface and other experimental paradigms that require rapid monitoring of brain rhythms.

[1]  G. Grice The relation of secondary reinforcement to delayed reward in visual discrimination learning. , 1948, Journal of experimental psychology.

[2]  Pascal Fries,et al.  Gamma-Rhythmic Gain Modulation , 2016, Neuron.

[3]  Jarrod A. Lewis-Peacock,et al.  Self-regulation strategy, feedback timing and hemodynamic properties modulate learning in a simulated fMRI neurofeedback environment , 2017, PLoS Comput. Biol..

[4]  Hartwig R. Siebner,et al.  Combining non-invasive transcranial brain stimulation with neuroimaging and electrophysiology: Current approaches and future perspectives , 2016, NeuroImage.

[5]  Hazhir Rahmandad,et al.  Effects of feedback delay on learning , 2009 .

[6]  B. Postle,et al.  Prestimulus alpha-band power biases visual discrimination confidence, but not accuracy , 2016, Consciousness and Cognition.

[7]  M. Nokia,et al.  Effects of Hippocampal State-Contingent Trial Presentation on Hippocampus-Dependent Nonspatial Classical Conditioning and Extinction , 2014, The Journal of Neuroscience.

[8]  E. Chang,et al.  UC San Francisco UC San Francisco Previously Published Works Title Oscillatory dynamics coordinating human frontal networks in support of goal maintenance , 2015 .

[9]  Simon Hanslmayr,et al.  Prestimulus oscillations predict visual perception performance between and within subjects , 2007, NeuroImage.

[10]  A. Nobre,et al.  Neural Oscillations: Sustained Rhythms or Transient Burst-Events? , 2018, Trends in Neurosciences.

[11]  S. Kitazawa,et al.  Effects of delayed visual information on the rate and amount of prism adaptation in the human , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[12]  A. Bruns Fourier-, Hilbert- and wavelet-based signal analysis: are they really different approaches? , 2004, Journal of Neuroscience Methods.

[13]  Sylvain Baillet,et al.  Mutual information spectrum for selection of event-related spatial components. Application to eloquent motor cortex mapping , 2014, Front. Neuroinform..

[14]  J. Schoffelen,et al.  University of Birmingham Occipital alpha activity during stimulus processing gates the information flow to object-selective cortex , 2014 .

[15]  Christoph Zrenner,et al.  Real-time EEG-defined excitability states determine efficacy of TMS-induced plasticity in human motor cortex , 2017, Brain Stimulation.

[16]  Cuntai Guan,et al.  A Randomized Controlled Trial of EEG-Based Motor Imagery Brain-Computer Interface Robotic Rehabilitation for Stroke , 2015, Clinical EEG and neuroscience.

[17]  T. Bergmann,et al.  μ-Rhythm Extracted With Personalized EEG Filters Correlates With Corticospinal Excitability in Real-Time Phase-Triggered EEG-TMS , 2018, bioRxiv.

[18]  J. Lacroix,et al.  Mechanisms of Biofeedback Control , 1986 .

[19]  Mikhail A. Lebedev,et al.  Neurofeedback learning modifies the incidence rate of alpha spindles, but not their duration and amplitude , 2017, Scientific Reports.

[20]  Jarrod A. Lewis-Peacock,et al.  Closed-loop brain training: the science of neurofeedback , 2017, Nature Reviews Neuroscience.

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

[22]  M. Arns,et al.  Neurofeedback and Basic Learning Theory: Implications for Research and Practice , 2011 .

[23]  C. Moore,et al.  Neural mechanisms of transient neocortical beta rhythms: Converging evidence from humans, computational modeling, monkeys, and mice , 2016, Proceedings of the National Academy of Sciences.

[24]  Hendrik Wöhrle,et al.  A Hybrid FPGA-Based System for EEG- and EMG-Based Online Movement Prediction , 2017, Sensors.

[25]  Roshan Cools,et al.  Region-specific modulations in oscillatory alpha activity serve to facilitate processing in the visual and auditory modalities , 2014, NeuroImage.

[26]  Benedikt Zoefel,et al.  Neurofeedback training of the upper alpha frequency band in EEG improves cognitive performance , 2011, NeuroImage.

[27]  Olaf Blanke,et al.  Visual Feedback Dominates the Sense of Agency for Brain-Machine Actions , 2015, PloS one.

[28]  Kok Lay Teo,et al.  Optimal design of complex FIR filters with arbitrary magnitude and group delay responses , 2006, IEEE Transactions on Signal Processing.

[29]  N. Busch,et al.  Single trial prestimulus oscillations predict perception of the sound-induced flash illusion , 2019, Scientific Reports.

[30]  Albert-László Barabási,et al.  Control Principles of Complex Networks , 2015, ArXiv.

[31]  Christoph Zrenner,et al.  Closed-Loop Neuroscience and Non-Invasive Brain Stimulation: A Tale of Two Loops , 2016, Front. Cell. Neurosci..

[32]  Thomas E. Myers,et al.  Neurofeedback for Autistic Spectrum Disorder: A Review of the Literature , 2010, Applied psychophysiology and biofeedback.

[33]  M. Sterman,et al.  Biofeedback Training of the Sensorimotor Electroencephalogram Rhythm in Man: Effects on Epilepsy , 1974, Epilepsia.

[34]  Moritz Grosse-Wentrup,et al.  Using brain–computer interfaces to induce neural plasticity and restore function , 2011, Journal of neural engineering.

[35]  Jonathan R. Wolpaw,et al.  Brain–Computer InterfacesPrinciples and Practice , 2012 .

[36]  Hanna-Leena Halme,et al.  Adaptive neural network classifier for decoding MEG signals , 2018, NeuroImage.

[37]  Wolfram Burgard,et al.  Deep learning with convolutional neural networks for EEG decoding and visualization , 2017, Human brain mapping.

[38]  C. Moore,et al.  The rate of transient beta frequency events predicts behavior across tasks and species , 2017, eLife.

[39]  Benjamin I. Rapoport,et al.  Real-Time Brain Oscillation Detection and Phase-Locked Stimulation Using Autoregressive Spectral Estimation and Time-Series Forward Prediction , 2013, IEEE Transactions on Biomedical Engineering.

[40]  Eric Butter,et al.  A Review of Complementary and Alternative Treatments for Autism Spectrum Disorders , 2012, Autism research and treatment.