Occipital tACS bursts during a visual task impact ongoing neural oscillation power, coherence and LZW complexity

Little is known about the precise neural mechanisms by which tACS affects the human cortex. Current hypothesis suggest that transcranial current stimulation (tCS) can directly enhance ongoing brain oscillations and induce long - lasting effects through the activation of synaptic plasticity mechanisms [1]. Entrainment has been demonstrated in in - vitro studies, but its presence in non-invasive human studies is still under debate [2,3]. Here, we aim to investigate the immediate and short-term effects of tACS bursts on the occipital cortex of participants engaged in a change – of - speed detection task, a task that has previously reported to have a clear physiology - behavior relationship, where trials with faster responses also have increased power in γ - oscillations (50 - 80 Hz) [4]. The dominant brain oscillations related to the visual task are modulated using multichannel tACS at 10 and 70 Hz within occipital cortex. We found that tACS stimulation at 10 Hz (tACS 10) enhanced both α (8 - 13 Hz) and γ oscillations, in hand with an increase in reaction time (RT) in the change – of - speed detection visual task. On the other hand, tACS at 70Hz desynchronized visual cortices, impairing both phase - locked and endogenous γ - power while increasing RT. While both tACS protocols seem to revert the relationship reported in [4], we argue that tACS produces a shift in attentional resources within visual cortex while leaving unaltered the resources required to conduct the task. This theory is supported by the fact that the correlation between fast RT and high γ- power trials is maintained for tACS sessions too. Finally, we measured cortical excitability by analyzing Event – Related - Potentials (ERP) Lempel – Ziv - Welch Complexity (LZW). In control sessions we observe that lower γ - LZW complexity correlates to faster reaction times. Both metrics are altered by tACS stimulation, as tACS 10 decreased amplitude of the P300 peak, while increasing γ- LZW complexity. To this end, our study highlights the nonlinear cross - frequency interaction between exogenous stimulation and endogenous brain dynamics, and proposes the use of complexity metrics, as LZW, to characterize excitability patterns of cortical areas in a behaviorally relevant timescale. These insights will hopefully contribute to the design of adaptive and personalized tACS protocols where cortical excitability can be characterized through complexity metrics. Additional Title Page Footnotes: We introduce a bursting tACS protocol to study semi-concurrent tACS effects in the visual system and their impact on behavior as measured by reaction time. Burst 10 Hz tACS (tACS10) applied to the visual cortex entrained γ-oscillations and increased RTs in a change-of-speed detection visual task more than 70 Hz tACS (tACS70) or Control conditions. Burst tACS10 also decreased amplitude of the P300 peak, while increasing α-power and γ-LZW complexity. Physiological and behavioral impact of occipital tACS10 and tACS70 was frequency-specific. tACS70 reduced γ-oscillations after 20min of tACS stimulation. Cognitive task may determine cortical excitation levels as measured by complexity metrics, as lower γ-LZW complexity correlates to faster reaction times.

[1]  A. Antal,et al.  Transcranial alternating current stimulation (tACS) , 2013, Front. Hum. Neurosci..

[2]  Robert Oostenveld,et al.  Visually induced gamma-band activity predicts speed of change detection in humans , 2010, NeuroImage.

[3]  R. Hornero,et al.  Entropy and Complexity Analyses in Alzheimer’s Disease: An MEG Study , 2010, The open biomedical engineering journal.

[4]  Roi Cohen Kadosh,et al.  Not all brains are created equal: the relevance of individual differences in responsiveness to transcranial electrical stimulation , 2014, Front. Syst. Neurosci..

[5]  Robert Oostenveld,et al.  FieldTrip: Open Source Software for Advanced Analysis of MEG, EEG, and Invasive Electrophysiological Data , 2010, Comput. Intell. Neurosci..

[6]  Giulio Ruffini,et al.  The electric field in the cortex during transcranial current stimulation , 2013, NeuroImage.

[7]  F. Wendling,et al.  Transcranial Current Brain Stimulation (tCS): Models and Technologies , 2013, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[8]  Emiliano Santarnecchi,et al.  State-Dependent Effects of Transcranial Oscillatory Currents on the Motor System: What You Think Matters , 2013, The Journal of Neuroscience.

[9]  Walter Paulus,et al.  Noninvasively Decoding the Contents of Visual Working Memory in the Human Prefrontal Cortex within High-gamma Oscillatory Patterns , 2012, Journal of Cognitive Neuroscience.

[10]  C. Herrmann,et al.  Orchestrating neuronal networks: sustained after-effects of transcranial alternating current stimulation depend upon brain states , 2013, Front. Hum. Neurosci..

[11]  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.

[12]  Guillaume A. Rousselet,et al.  Modeling Single-Trial ERP Reveals Modulation of Bottom-Up Face Visual Processing by Top-Down Task Constraints (in Some Subjects) , 2011, Frontiers in psychology.

[13]  C. Herrmann,et al.  Sustained Aftereffect of α-tACS Lasts Up to 70 min after Stimulation , 2016, Front. Hum. Neurosci..

[14]  Thomas M. Cover,et al.  Elements of Information Theory , 2005 .

[15]  Abraham Lempel,et al.  On the Complexity of Finite Sequences , 1976, IEEE Trans. Inf. Theory.

[16]  S. Muthukumaraswamy High-frequency brain activity and muscle artifacts in MEG/EEG: a review and recommendations , 2013, Front. Hum. Neurosci..

[17]  Paul B. Fitzgerald,et al.  TDCS increases cortical excitability: Direct evidence from TMS-EEG , 2016, Cortex.

[18]  M. Murray,et al.  Shaping Intrinsic Neural Oscillations with Periodic Stimulation , 2016, The Journal of Neuroscience.

[19]  T. Sejnowski,et al.  Network Oscillations: Emerging Computational Principles , 2006, The Journal of Neuroscience.

[20]  Roberto Hornero,et al.  Lempel–Ziv complexity in schizophrenia: A MEG study , 2011, Clinical Neurophysiology.

[21]  E. Boersma,et al.  Prevention of Catheter-Related Bacteremia with a Daily Ethanol Lock in Patients with Tunnelled Catheters: A Randomized, Placebo-Controlled Trial , 2010, PloS one.

[22]  Stephen Darling,et al.  Intraindividual reaction time variability affects P300 amplitude rather than latency , 2014, Front. Hum. Neurosci..

[23]  A. Engel,et al.  Entrainment of Brain Oscillations by Transcranial Alternating Current Stimulation , 2014, Current Biology.

[24]  Robert Oostenveld,et al.  Localizing human visual gamma-band activity in frequency, time and space , 2006, NeuroImage.

[25]  Giulio Ruffini,et al.  An algorithmic information theory of consciousness , 2017, Neuroscience of consciousness.

[26]  Sylvia Vitello,et al.  Transcranial Magnetic Stimulation for Investigating Causal Brain-behavioral Relationships and their Time Course , 2014, Journal of visualized experiments : JoVE.

[27]  C. Herrmann,et al.  Transcranial Alternating Current Stimulation Enhances Individual Alpha Activity in Human EEG , 2010, PloS one.

[28]  M. Hallett,et al.  Modeling the current distribution during transcranial direct current stimulation , 2006, Clinical Neurophysiology.

[29]  Gordon Pipa,et al.  Neuronal oscillations form parietal/frontal networks during contour integration , 2014, Front. Integr. Neurosci..

[30]  S. Tong,et al.  Abnormal EEG complexity in patients with schizophrenia and depression , 2008, Clinical Neurophysiology.

[31]  Todd C. Handy,et al.  Event-related potentials : a methods handbook , 2005 .

[32]  Flavio Fröhlich,et al.  Endogenous Cortical Oscillations Constrain Neuromodulation by Weak Electric Fields , 2014, Brain Stimulation.

[33]  Christoph S. Herrmann,et al.  Transcranial Alternating Current Stimulation (tACS) Enhances Mental Rotation Performance during and after Stimulation , 2017, Front. Hum. Neurosci..

[34]  Giulio Ruffini,et al.  Optimization of multifocal transcranial current stimulation for weighted cortical pattern targeting from realistic modeling of electric fields , 2014, NeuroImage.

[35]  G. Tononi,et al.  Lempel-Ziv complexity of cortical activity during sleep and waking in rats , 2015, Journal of neurophysiology.

[36]  H. Kennedy,et al.  Alpha-Beta and Gamma Rhythms Subserve Feedback and Feedforward Influences among Human Visual Cortical Areas , 2016, Neuron.

[37]  Thomas M. Cover,et al.  Elements of Information Theory: Cover/Elements of Information Theory, Second Edition , 2005 .

[38]  C. Herrmann,et al.  On the possible role of stimulation duration for after-effects of transcranial alternating current stimulation , 2015, Front. Cell. Neurosci..

[39]  N. Yeung,et al.  The roles of cortical oscillations in sustained attention , 2015, Trends in Cognitive Sciences.

[40]  A. Antal,et al.  Safety aspects of transcranial direct current stimulation concerning healthy subjects and patients , 2007, Brain Research Bulletin.

[41]  Richard Gao,et al.  Field Potential Reflects the Balance of Synaptic Excitation and Inhibition , 2016 .

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

[43]  Roberto Hornero,et al.  Complexity analysis of spontaneous brain activity: effects of depression and antidepressant treatment , 2012, Journal of psychopharmacology.

[44]  A. Seth,et al.  Increased spontaneous MEG signal diversity for psychoactive doses of ketamine, LSD and psilocybin , 2017, Scientific Reports.

[45]  C. Herrmann,et al.  Eyes wide shut: Transcranial alternating current stimulation drives alpha rhythm in a state dependent manner , 2016, Scientific Reports.

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

[47]  M. Nitsche,et al.  Excitability changes induced in the human primary visual cortex by transcranial direct current stimulation: direct electrophysiological evidence. , 2004, Investigative ophthalmology & visual science.

[48]  Yuan Bo Peng,et al.  The anterior cingulate cortex and pain processing , 2014, Front. Integr. Neurosci..

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

[50]  Timothy H. Muller,et al.  Individual differences and specificity of prefrontal gamma frequency-tACS on fluid intelligence capabilities , 2016, Cortex.

[51]  G. Tononi,et al.  A Theoretically Based Index of Consciousness Independent of Sensory Processing and Behavior , 2013, Science Translational Medicine.

[52]  D. Abásolo,et al.  Brain oscillatory complexity across the life span , 2012, Clinical Neurophysiology.

[53]  S. Rossi,et al.  Evidence-based guidelines on the therapeutic use of transcranial direct current stimulation (tDCS) , 2017, Clinical Neurophysiology.

[54]  S. Treue,et al.  Transcranial alternating stimulation in a high gamma frequency range applied over V1 improves contrast perception but does not modulate spatial attention , 2012, Brain Stimulation.

[55]  Debora Brignani,et al.  Is Transcranial Alternating Current Stimulation Effective in Modulating Brain Oscillations? , 2013, PloS one.

[56]  F. Fregni,et al.  A systematic review on reporting and assessment of adverse effects associated with transcranial direct current stimulation. , 2011, The international journal of neuropsychopharmacology.

[57]  J. Delgado-García,et al.  Effects of transcranial Direct Current Stimulation (tDCS) on cortical activity: A computational modeling study , 2013, Brain Stimulation.

[58]  Glyn Humphreys,et al.  Mu rhythm desynchronization reveals motoric influences of hand action on object recognition , 2013, Front. Hum. Neurosci..

[59]  P. König,et al.  Top-down processing mediated by interareal synchronization. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[60]  Gregor Thut,et al.  Alpha Power Increase After Transcranial Alternating Current Stimulation at Alpha Frequency (α-tACS) Reflects Plastic Changes Rather Than Entrainment , 2015, Brain Stimulation.

[61]  Jan Born,et al.  Transcranial Electrical Currents to Probe EEG Brain Rhythms and Memory Consolidation during Sleep in Humans , 2011, PloS one.

[62]  Tom Verguts,et al.  The P3 Event-Related Potential is a Biomarker for the Efficacy of Vagus Nerve Stimulation in Patients with Epilepsy , 2014, Neurotherapeutics.

[63]  A. Kok Event-related-potential (ERP) reflections of mental resource̊s: a review and synthesis , 1997, Biological Psychology.

[64]  Kristin K Sellers,et al.  Targeting the neurophysiology of cognitive systems with transcranial alternating current stimulation , 2015, Expert review of neurotherapeutics.

[65]  P. Schyns,et al.  Entrainment of Perceptually Relevant Brain Oscillations by Non-Invasive Rhythmic Stimulation of the Human Brain , 2011, Front. Psychology.

[66]  W. Singer,et al.  Neural Synchrony in Cortical Networks: History, Concept and Current Status , 2009, Front. Integr. Neurosci..