Heart cycle-related effects on event-related potentials, spectral power changes, and connectivity patterns in the human ECoG

The perception of one's own heartbeat is a fundamental interoceptive process that involves cortical and subcortical structures. Yet, the precise spatiotemporal neuronal activity patterns underlying the cortical information processing have remained largely elusive. Although the high temporal and spatial resolution of electrocorticographic (ECoG) recordings is increasingly being exploited in functional neuroimaging, it has not been used to study heart cycle-related effects. Here, we addressed the capacity of ECoG to characterize neuronal signals within the cardiac cycle, as well as to disentangle them from heart cycle-related artifacts. Based on topographical distribution and latency, we identified a biphasic potential within the primary somatosensory cortex, which likely constitutes a heartbeat-evoked potential (HEP) of neuronal origin. We also found two different types of artifacts: i) oscillatory potential changes with a frequency identical to the heart pulse rate, which probably represent pulsatility artifacts and ii) sharp potentials synchronized to the R-peak, corresponding to the onset of ventricular contraction and the cardiac field artifact (CFA) in EEG. Finally, we show that heart cycle-related effects induce pronounced phase-synchrony patterns in the ECoG and that this kind of correlation patterns, which may confound ECoG connectivity studies, can be reduced by a suitable correction algorithm. The present study is, to our knowledge, the first one to show a focally localized cortical HEP that could be clearly and consistently observed over subjects, suggesting a basic role of primary sensory cortex in processing of heart-related sensory inputs. We also conclude that taking into account and reducing heart cycle-related effects may be advantageous for many ECoG studies, and are of crucial importance, particularly for ECoG-based connectivity studies. Thus, in summary, although ECoG poses new challenges, it opens up new possibilities for the investigation of heartbeat-related viscerosensory processing in the human brain.

[1]  D. Auer,et al.  Brain structures mediating cardiovascular arousal and interoceptive awareness , 2007, Brain Research.

[2]  John M. Stern,et al.  Atlas of EEG Patterns , 2004 .

[3]  N. Crone,et al.  High-frequency gamma oscillations and human brain mapping with electrocorticography. , 2006, Progress in brain research.

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

[5]  O. Mecarelli,et al.  Clinical Electroencephalography , 2019 .

[6]  Ernst Fernando Lopes Da Silva Niedermeyer,et al.  Electroencephalography, basic principles, clinical applications, and related fields , 1982 .

[7]  A. Bechara,et al.  Listening to your heart: interoceptive awareness as a gateway to feeling , 2004, Nature Neuroscience.

[8]  G Dirlich,et al.  Topography and morphology of heart action-related EEG potentials. , 1998, Electroencephalography and clinical neurophysiology.

[9]  P. Montoya,et al.  Event-related brain potentials and the processing of cardiac activity , 1996, Biological Psychology.

[10]  Jeffrey G. Ojemann,et al.  Power-Law Scaling in the Brain Surface Electric Potential , 2009, PLoS Comput. Biol..

[11]  Hugo D. Critchley,et al.  Activity in the human brain predicting differential heart rate responses to emotional facial expressions , 2005, NeuroImage.

[12]  Richard P. Brenner,et al.  Atlas of EEG in critical care , 2010 .

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

[14]  N. Barbaro,et al.  Spatiotemporal Dynamics of Word Processing in the Human Brain , 2007, Front. Neurosci..

[15]  U. Klose,et al.  Cerebrospinal fluid flow , 2004, Neuroradiology.

[16]  J. Wolpaw,et al.  Decoding two-dimensional movement trajectories using electrocorticographic signals in humans , 2007, Journal of neural engineering.

[17]  Satoshi Minoshima,et al.  Regional Brain Activation Due to Pharmacologically Induced Adrenergic Interoceptive Stimulation in Humans , 2002, Psychosomatic medicine.

[18]  P. Montoya,et al.  Heartbeat evoked potentials (HEP): topography and influence of cardiac awareness and focus of attention. , 1993, Electroencephalography and clinical neurophysiology.

[19]  Andreas Schulze-Bonhage,et al.  Movement related activity in the high gamma range of the human EEG , 2008, NeuroImage.

[20]  Kaiquan Shen,et al.  Effect of pain perception on the heartbeat evoked potential , 2011, Clinical Neurophysiology.

[21]  B. Saltin,et al.  Maximal oxygen uptake and heart rate in various types of muscular activity. , 1961, Journal of applied physiology.

[22]  D. Spence,et al.  Cardiac Change as a Function of Attention to and Awareness of Continuous Verbal Text , 1972, Science.

[23]  H. Critchley,et al.  Neural systems supporting interoceptive awareness , 2004, Nature Neuroscience.

[24]  A. Burgess,et al.  Paradox lost? Exploring the role of alpha oscillations during externally vs. internally directed attention and the implications for idling and inhibition hypotheses. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[25]  Todd R. Ogden,et al.  Wavelet Methods for Time Series Analysis , 2002 .

[26]  P Kahane,et al.  Intracranial EEG and human brain mapping , 2003, Journal of Physiology-Paris.

[27]  O. Pollatos,et al.  Accuracy of heartbeat perception is reflected in the amplitude of the heartbeat-evoked brain potential. , 2004, Psychophysiology.

[28]  David Rudrauf,et al.  The pathways of interoceptive awareness , 2009, Nature Neuroscience.

[29]  M G Bleichner,et al.  The effects of blood vessels on electrocorticography , 2011, Journal of neural engineering.

[30]  Catie Chang,et al.  Influence of heart rate on the BOLD signal: The cardiac response function , 2009, NeuroImage.

[31]  B C Lacey,et al.  Two-way communication between the heart and the brain. Significance of time within the cardiac cycle. , 1978, The American psychologist.

[32]  Dimitrios Pantazis,et al.  Behavioral states may be associated with distinct spatial patterns in electrocorticogram , 2010, Cognitive Neurodynamics.

[33]  Ayako Ochi,et al.  High-frequency oscillations of ictal muscle activity and epileptogenic discharges on intracranial EEG in a temporal lobe epilepsy patient , 2008, Clinical Neurophysiology.

[34]  B. Macgillivray EEG Technology , 1982 .

[35]  Philippe Kahane,et al.  Saccade Related Gamma-Band Activity in Intracerebral EEG: Dissociating Neural from Ocular Muscle Activity , 2009, Brain Topography.

[36]  N. Pelc,et al.  Brain motion: measurement with phase-contrast MR imaging. , 1992, Radiology.

[37]  C. Crainiceanu,et al.  Electrocorticographic high gamma activity versus electrical cortical stimulation mapping of naming. , 2005, Brain : a journal of neurology.

[38]  C. Mehring,et al.  Differential Representation of Arm Movement Direction in Relation to Cortical Anatomy and Function , 2008 .

[39]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. I. Alpha and beta event-related desynchronization. , 1998, Brain : a journal of neurology.

[40]  Andreas Schulze-Bonhage,et al.  Signal quality of simultaneously recorded invasive and non-invasive EEG , 2009, NeuroImage.

[41]  C. D. Binnie,et al.  EEG, paediatric neurophysiology, special techniques and applications , 2003 .

[42]  J. Lacey Psychophysiological approaches to the evaluation of psychotherapeutic process and outcome. , 1959 .

[43]  Beatrice C. Lacey,et al.  Studies of heart rate and other bodily processes in sensorimotor behavior. , 1974 .

[44]  Satoshi Umeda,et al.  Association between interoception and empathy: evidence from heartbeat-evoked brain potential. , 2011, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[45]  M. Berger,et al.  High Gamma Power Is Phase-Locked to Theta Oscillations in Human Neocortex , 2006, Science.

[46]  R. Weitkunat,et al.  Enhancement of heartbeat-related brain potentials through cardiac awareness training. , 1990, The International journal of neuroscience.

[47]  Andreas Schulze-Bonhage,et al.  Decoding natural grasp types from human ECoG , 2012, NeuroImage.

[48]  J. S. Barlow,et al.  EKG-artifact minimization in referential EEG recordings by computer subtraction. , 1980, Electroencephalography and clinical neurophysiology.

[49]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. , 1998, Brain : a journal of neurology.

[50]  O. Pollatos,et al.  Brain structures involved in interoceptive awareness and cardioafferent signal processing: A dipole source localization study , 2005, Human brain mapping.

[51]  Gerwin Schalk,et al.  A brain–computer interface using electrocorticographic signals in humans , 2004, Journal of neural engineering.

[52]  E. Guijarro,et al.  Suppression of the cardiac electric field artifact from the heart action evoked potential , 2006, Medical and Biological Engineering and Computing.

[53]  Adam Flanders,et al.  Functional Magnetic Resonance Imaging Analysis of Attention to One’s Heartbeat , 2007, Psychosomatic medicine.

[54]  Eric Leuthardt,et al.  Real-time detection of event-related brain activity , 2008, NeuroImage.

[55]  Naotaka Fujii,et al.  Decoding continuous three-dimensional hand trajectories from epidural electrocorticographic signals in Japanese macaques , 2012, Journal of neural engineering.

[56]  Catherine Tallon-Baudry,et al.  The many faces of the gamma band response to complex visual stimuli , 2005, NeuroImage.

[57]  G. Dirlich,et al.  Cardiac field effects on the EEG. , 1997, Electroencephalography and clinical neurophysiology.

[58]  R. Weitkunat,et al.  From the heart to the brain: a study of heartbeat contingent scalp potentials. , 1986, The International journal of neuroscience.

[59]  A. Engel,et al.  Invasive recordings from the human brain: clinical insights and beyond , 2005, Nature Reviews Neuroscience.

[60]  R. Schandry,et al.  The heartbeat-evoked brain potential in patients suffering from diabetic neuropathy and in healthy control persons , 2001, Clinical Neurophysiology.

[61]  B. Ekblom,et al.  Maximal oxygen uptake during exercise with various combinations of arm and leg work. , 1976, Journal of applied physiology.

[62]  Y. Benjamini,et al.  Controlling the false discovery rate in behavior genetics research , 2001, Behavioural Brain Research.

[63]  Tonio Ball,et al.  Towards an implantable brain-machine interface based on epicortical field potentials , 2004 .

[64]  F. Ståhlberg,et al.  Pulsatile brain movement and associated hydrodynamics studied by magnetic resonance phase imaging , 2004, Neuroradiology.

[65]  L W Thompson,et al.  Heart rate changes in a reaction time experiment with young and aged subjects. , 1969, Journal of gerontology.

[66]  Hui Yuan 袁辉,et al.  Effect of heartbeat perception on heartbeat evoked potential waves , 2007, Neuroscience Bulletin.

[67]  L Beyer,et al.  Dynamics of central nervous activation during motor imagination. , 1990, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[68]  J. Madsen,et al.  The pulsating brain: A review of experimental and clinical studies of intracranial pulsatility , 2011, Fluids and Barriers of the CNS.

[69]  U Klose,et al.  Cerebrospinal fluid flow , 2004, Neuroradiology.

[70]  H. Critchley,et al.  A cortical potential reflecting cardiac function , 2007, Proceedings of the National Academy of Sciences.

[71]  Christopher K. Kovach,et al.  Manifestation of ocular-muscle EMG contamination in human intracranial recordings , 2011, NeuroImage.