Ultra-low frequency neural entrainment to pain

Nervous systems exploit regularities in the sensory environment to predict sensory input and adjust behavior, and thereby maximize fitness. Entrainment of neural oscillations allows retaining temporal regularities of sensory information, a prerequisite for prediction. Entrainment has been extensively described at the frequencies of periodic inputs most commonly present in visual and auditory landscapes (e.g. >1 Hz). An open question is whether neural entrainment also occurs for regularities at much longer timescales. Here we exploited the fact that the temporal dynamics of thermal stimuli in natural environment can unfold very slowly. We show that ultra-low frequency neural oscillations preserved a long-lasting trace of sensory information through neural entrainment to periodic thermo-nociceptive input as low as 0.1 Hz. Importantly, revealing the functional significance of this phenomenon, both power and phase of the entrainment predicted individual pain sensitivity. In contrast, periodic auditory input at the same ultra-low frequency did not entrain ultra-low frequency oscillations. These results demonstrate that a functionally-significant neural entrainment can occur at temporal scales far longer than those commonly explored. The non-supramodal nature of our results suggests that ultra-low frequency entrainment might be tuned to the temporal scale of the statistical regularities characteristic of different sensory modalities.

[1]  T. Sejnowski,et al.  Removing electroencephalographic artifacts by blind source separation. , 2000, Psychophysiology.

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

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

[4]  Stefano Panzeri,et al.  Analysis of Slow (Theta) Oscillations as a Potential Temporal Reference Frame for Information Coding in Sensory Cortices , 2012, PLoS Comput. Biol..

[5]  Aniruddh D. Patel,et al.  Temporal modulations in speech and music , 2017, Neuroscience & Biobehavioral Reviews.

[6]  André Mouraux,et al.  Thermal Detection Thresholds of Aδ- and C-Fibre Afferents Activated by Brief CO2 Laser Pulses Applied onto the Human Hairy Skin , 2012, PloS one.

[7]  L. Glass Synchronization and rhythmic processes in physiology , 2001, Nature.

[8]  Evgueniy V. Lubenov,et al.  Prefrontal Phase Locking to Hippocampal Theta Oscillations , 2005, Neuron.

[9]  Satu Palva,et al.  Roles of Brain Criticality and Multiscale Oscillations in Temporal Predictions for Sensorimotor Processing , 2018, Trends in Neurosciences.

[10]  G. Kraepelin,et al.  A. T. Winfree, The Geometry of Biological Time (Biomathematics, Vol.8). 530 S., 290 Abb. Berlin‐Heidelberg‐New‐York 1980. Springer‐Verlag. DM 59,50 , 1981 .

[11]  A. Falchier,et al.  Top-down, contextual entrainment of neuronal oscillations in the auditory thalamocortical circuit , 2018, Proceedings of the National Academy of Sciences.

[12]  D. Poeppel,et al.  Mechanisms Underlying Selective Neuronal Tracking of Attended Speech at a “Cocktail Party” , 2013, Neuron.

[13]  G. Karmos,et al.  Entrainment of Neuronal Oscillations as a Mechanism of Attentional Selection , 2008, Science.

[14]  Joachim M. Buhmann,et al.  Decoding the perception of pain from fMRI using multivariate pattern analysis , 2012, NeuroImage.

[15]  G. Novembre,et al.  Tagging the musical beat: Neural entrainment or event-related potentials? , 2018, Proceedings of the National Academy of Sciences of the United States of America.

[16]  Gian Domenico Iannetti,et al.  The "Pain Matrix" in Pain-Free Individuals. , 2016, JAMA neurology.

[17]  Markus Ploner,et al.  Electroencephalography and magnetoencephalography in pain research—current state and future perspectives , 2018, Pain.

[18]  André Mouraux,et al.  EEG frequency tagging using ultra-slow periodic heat stimulation of the skin reveals cortical activity specifically related to C fiber thermonociceptors , 2017, NeuroImage.

[19]  Abbas Sohrabpour,et al.  Spectral and spatial changes of brain rhythmic activity in response to the sustained thermal pain stimulation , 2016, Human brain mapping.

[20]  D. Poeppel,et al.  Phase Patterns of Neuronal Responses Reliably Discriminate Speech in Human Auditory Cortex , 2007, Neuron.

[21]  M. Baliki,et al.  The Cortical Rhythms of Chronic Back Pain , 2011, The Journal of Neuroscience.

[22]  M. Massimini,et al.  Natural Frequencies of Human Corticothalamic Circuits , 2009, The Journal of Neuroscience.

[23]  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.

[24]  C. Schroeder,et al.  Low-frequency neuronal oscillations as instruments of sensory selection , 2009, Trends in Neurosciences.

[25]  C. Schroeder,et al.  The Spectrotemporal Filter Mechanism of Auditory Selective Attention , 2013, Neuron.

[26]  Atsuko Takashima,et al.  Neural Entrainment Determines the Words We Hear , 2017, Current Biology.

[27]  O. Jensen,et al.  Alpha Oscillations Serve to Protect Working Memory Maintenance against Anticipated Distracters , 2012, Current Biology.

[28]  D. P. Russell,et al.  Increased Synchronization of Neuromagnetic Responses during Conscious Perception , 1999, The Journal of Neuroscience.

[29]  E. Large Resonating to Musical Rhythm : Theory and Experiment , 2008 .

[30]  A. Mouraux,et al.  From the neuromatrix to the pain matrix (and back) , 2010, Experimental Brain Research.

[31]  T. Schnitzer,et al.  Shape shifting pain: chronification of back pain shifts brain representation from nociceptive to emotional circuits. , 2013, Brain : a journal of neurology.

[32]  Peter A. Tass,et al.  Phase Resetting in Medicine and Biology: Stochastic Modelling and Data Analysis , 1999 .

[33]  G. D. Iannetti,et al.  Neural indicators of perceptual variability of pain across species , 2019, Proceedings of the National Academy of Sciences.

[34]  S. Haegens,et al.  Rhythmic facilitation of sensory processing: A critical review , 2017, Neuroscience & Biobehavioral Reviews.

[35]  Jürgen Kurths,et al.  Synchronization - A Universal Concept in Nonlinear Sciences , 2001, Cambridge Nonlinear Science Series.

[36]  B. Postle,et al.  Top-down control of the phase of alpha-band oscillations as a mechanism for temporal prediction , 2015, Proceedings of the National Academy of Sciences.

[37]  Luc H. Arnal,et al.  Cortical oscillations and sensory predictions , 2012, Trends in Cognitive Sciences.

[38]  L. Deouell,et al.  Neural mechanisms of rhythm-based temporal prediction: Delta phase-locking reflects temporal predictability but not rhythmic entrainment , 2017, PLoS biology.

[39]  Michael X Cohen,et al.  Analyzing Neural Time Series Data: Theory and Practice , 2014 .

[40]  A. Apkarian,et al.  Parsing pain perception between nociceptive representation and magnitude estimation. , 2009, Journal of neurophysiology.

[41]  C. Schroeder,et al.  Tuning of the Human Neocortex to the Temporal Dynamics of Attended Events , 2011, The Journal of Neuroscience.

[42]  Gian Domenico Iannetti,et al.  Painful Issues in Pain Prediction , 2016, Trends in Neurosciences.

[43]  R. Knight,et al.  The functional role of cross-frequency coupling , 2010, Trends in Cognitive Sciences.

[44]  Joachim Gross,et al.  Brain oscillations differentially encode noxious stimulus intensity and pain intensity , 2017, NeuroImage.

[45]  Dante R Chialvo,et al.  Dynamics of pain: fractal dimension of temporal variability of spontaneous pain differentiates between pain States. , 2006, Journal of neurophysiology.

[46]  Alon Sinai,et al.  Tonic pain and continuous EEG: Prediction of subjective pain perception by alpha-1 power during stimulation and at rest , 2012, Clinical Neurophysiology.

[47]  A. Mouraux,et al.  Nociceptive laser-evoked brain potentials do not reflect nociceptive-specific neural activity. , 2009, Journal of neurophysiology.

[48]  Joachim Gross,et al.  Prefrontal Gamma Oscillations Encode Tonic Pain in Humans , 2015, Cerebral cortex.

[49]  J. Obleser,et al.  Aging affects the balance of neural entrainment and top-down neural modulation in the listening brain , 2017, Nature Communications.

[50]  A. Mouraux,et al.  Determinants of laser-evoked EEG responses: pain perception or stimulus saliency? , 2008, Journal of neurophysiology.

[51]  A. Mouraux,et al.  Nociceptive Steady-State Evoked Potentials Elicited by Rapid Periodic Thermal Stimulation of Cutaneous Nociceptors , 2011, The Journal of Neuroscience.

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

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

[54]  Yong Hu,et al.  Changes of Spontaneous Oscillatory Activity to Tonic Heat Pain , 2014, PloS one.

[55]  A. Winfree The geometry of biological time , 1991 .

[56]  D H Brainard,et al.  The Psychophysics Toolbox. , 1997, Spatial vision.

[57]  E. S. May,et al.  Electroencephalography and magnetoencephalography in pain research—current state and future perspectives , 2018, Pain.

[58]  Joachim Gross,et al.  Prefrontal gamma oscillations reflect ongoing pain intensity in chronic back pain patients , 2018, Human brain mapping.

[59]  Guillermo A. Cecchi,et al.  Predictive Dynamics of Human Pain Perception , 2012, PLoS Comput. Biol..

[60]  Gian Domenico Iannetti,et al.  A multisensory investigation of the functional significance of the “pain matrix” , 2011, NeuroImage.

[61]  Gian Domenico Iannetti,et al.  A novel approach to predict subjective pain perception from single-trial laser-evoked potentials , 2013, NeuroImage.

[62]  N. Fisher,et al.  Statistical Analysis of Circular Data , 1993 .

[63]  David Poeppel,et al.  Interpretations of Frequency Domain Analyses of Neural Entrainment: Periodicity, Fundamental Frequency, and Harmonics , 2016, Front. Hum. Neurosci..

[64]  G. Buzsáki Rhythms of the brain , 2006 .

[65]  A. Bernacchia,et al.  Characterizing the Short-Term Habituation of Event-Related Evoked Potentials , 2018, eNeuro.

[66]  Trevor Hastie,et al.  Neural mechanisms of rhythm-based temporal prediction : Delta phase-locking reflects temporal predictability but not rhythmic entrainment , 2017 .

[67]  F. Varela,et al.  Measuring phase synchrony in brain signals , 1999, Human brain mapping.

[68]  Claudia Plant,et al.  Decoding an individual's sensitivity to pain from the multivariate analysis of EEG data. , 2012, Cerebral cortex.

[69]  J. Gross,et al.  Brain Rhythms of Pain , 2017, Trends in Cognitive Sciences.

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

[71]  J. Palva,et al.  Very Slow EEG Fluctuations Predict the Dynamics of Stimulus Detection and Oscillation Amplitudes in Humans , 2008, The Journal of Neuroscience.

[72]  A. Mouraux,et al.  The pain matrix reloaded A salience detection system for the body , 2011, Progress in Neurobiology.

[73]  Hugo Merchant,et al.  Finding the beat: a neural perspective across humans and non-human primates , 2015, Philosophical Transactions of the Royal Society B: Biological Sciences.

[74]  J. Avery Critical review. , 2006, The Journal of the Arkansas Medical Society.

[75]  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..

[76]  A. Mouraux,et al.  The search for pain biomarkers in the human brain , 2018, Brain : a journal of neurology.

[77]  P. Schyns,et al.  Rhythmic TMS Causes Local Entrainment of Natural Oscillatory Signatures , 2011, Current Biology.

[78]  D. Chialvo,et al.  Chronic Pain and the Emotional Brain: Specific Brain Activity Associated with Spontaneous Fluctuations of Intensity of Chronic Back Pain , 2006, The Journal of Neuroscience.

[79]  P. Schyns,et al.  Speech Rhythms and Multiplexed Oscillatory Sensory Coding in the Human Brain , 2013, PLoS biology.