Brain–heart coupling at the P300 latency is linked to anterior cingulate cortex and insula—A cardio-electroencephalographic covariance tracing study

Prior work on the coupling of cortical and cardiac responses to feedback demonstrated that feedback-evoked single-trial EEG magnitudes 300 ms post-stimulus predict the degree of subsequent cardiac acceleration. The main goal of the current study was to explore the neural sources of this phenomenon using (a) independent component analysis in conjunction with dipole fitting and (b) low resolution electromagnetic tomography (LORETA) in N=14 participants who performed a gambling task with feedback presented after each trial. It was shown that independent components localized near anterior cingulate cortex produced robust within-subjects correlations with feedback-evoked heart-period, suggesting that anterior cingulate cortex activity 300ms after feedback presentation predicts the strength of subsequent cardiac acceleration. Moreover, interindividual differences in evoked left insular cortex LORETA-estimated activity at around 300ms moderated within-subjects EEG-heart period correlations. These results suggest that key regions of central autonomic control are involved in cortico-cardiac coupling evoked by feedback stimuli.

[1]  A. Craig,et al.  How do you feel — now? The anterior insula and human awareness , 2009, Nature Reviews Neuroscience.

[2]  A. Ramage Central cardiovascular regulation and 5-hydroxytryptamine receptors , 2001, Brain Research Bulletin.

[3]  Jacob Cohen Statistical Power Analysis for the Behavioral Sciences , 1969, The SAGE Encyclopedia of Research Design.

[4]  A. Verberne,et al.  Cortical Modulation of theCardiovascular System , 1998, Progress in Neurobiology.

[5]  K. R. Ridderinkhof,et al.  Conscious perception of errors and its relation to the anterior insula , 2010, Brain Structure and Function.

[6]  Monika Althaus,et al.  Physiological correlates of learning by performance feedback in children: a study of EEG event-related potentials and evoked heart rate , 2007, Biological Psychology.

[7]  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.

[8]  R. Barry,et al.  Cognitive processing effects on auditory event-related potentials and the evoked cardiac response. , 2010, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[9]  J. Jennings,et al.  Regional cerebral blood flow correlates with heart period and high-frequency heart period variability during working-memory tasks: Implications for the cortical and subcortical regulation of cardiac autonomic activity. , 2004, Psychophysiology.

[10]  G. Stemmler,et al.  Single-trial electroencephalogram predicts cardiac acceleration: a time-lagged P-correlation approach for studying neurovisceral connectivity , 2010, Neuroscience.

[11]  T. Sejnowski,et al.  Dynamic Brain Sources of Visual Evoked Responses , 2002, Science.

[12]  A. Sanfey,et al.  Independent Coding of Reward Magnitude and Valence in the Human Brain , 2004, The Journal of Neuroscience.

[13]  S. Makeig,et al.  Dopamine Effects on Human Error Processing Depend on Catechol-O-Methyltransferase VAL158MET Genotype , 2011, The Journal of Neuroscience.

[14]  E. Evers,et al.  Acute tryptophan depletion attenuates brain-heart coupling following external feedback , 2012, Front. Hum. Neurosci..

[15]  Berrin Maraşligil,et al.  İnsanlarda Yenilik N2 Yanıtı Hedef Uyaranların Zamansal Sınıflamasını Yansıtır , 2011 .

[16]  R. Simons,et al.  To err is autonomic: error-related brain potentials, ANS activity, and post-error compensatory behavior. , 2003, Psychophysiology.

[17]  S. Nieuwenhuis,et al.  The anatomical and functional relationship between the P3 and autonomic components of the orienting response. , 2011, Psychophysiology.

[18]  Folkert Postema,et al.  Forebrain parasympathetic control of heart activity: retrograde transneuronal viral labeling in rats. , 1997, American journal of physiology. Heart and circulatory physiology.

[19]  John W. Tukey,et al.  Statistical Methods for Research Workers , 1930, Nature.

[20]  C. Wientjes,et al.  The relation between event-related brain potential, heart rate, and blood pressure responses in an S1-S2 paradigm , 1995, Biological Psychology.

[21]  Jonathan D. Cohen,et al.  Decision making, the P3, and the locus coeruleus-norepinephrine system. , 2005, Psychological bulletin.

[22]  D. Lehmann,et al.  Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain. , 1994, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[23]  Ryan Bogdan,et al.  Serotonin Transporter Genotype and Action Monitoring Dysfunction: A Possible Substrate Underlying Increased Vulnerability to Depression , 2010, Neuropsychopharmacology.

[24]  J. Polich Updating P300: An integrative theory of P3a and P3b , 2007, Clinical Neurophysiology.

[25]  M. W. Molen,et al.  Cardiac and electrophysiological responses to valid and invalid feedback in a time-estimation task , 2011 .

[26]  S Makeig,et al.  Blind separation of auditory event-related brain responses into independent components. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Martin P Paulus,et al.  Functional subdivisions within anterior cingulate cortex and their relationship to autonomic nervous system function , 2004, NeuroImage.

[28]  Beatrice C. Lacey,et al.  Change in heart period: A function of sensorimotor event timing within the cardiac cycle , 1977 .

[29]  Input and central processing expressed in ERP and heart rate changes to rare target and rare nontarget stimuli. , 1998, Psychophysiology.

[30]  R. Lane,et al.  Claude Bernard and the heart–brain connection: Further elaboration of a model of neurovisceral integration , 2009, Neuroscience & Biobehavioral Reviews.

[31]  M. Posner,et al.  Cognitive and emotional influences in anterior cingulate cortex , 2000, Trends in Cognitive Sciences.

[32]  H. Critchley Neural mechanisms of autonomic, affective, and cognitive integration , 2005, The Journal of comparative neurology.

[33]  Peter S Talbot,et al.  Anterior Cingulate and Subgenual Prefrontal Blood Flow Changes Following Tryptophan Depletion in Healthy Males , 2006, Neuropsychopharmacology.

[34]  Atsushi Sato,et al.  Effects of value and reward magnitude on feedback negativity and P300 , 2005, Neuroreport.

[35]  Aad van der Lugt,et al.  Remedial action and feedback processing in a time-estimation task: Evidence for a role of the rostral cingulate zone in behavioral adjustments without learning , 2011, NeuroImage.

[36]  D. Jordan Vagal control of the heart: central serotonergic (5‐HT) mechanisms , 2005, Experimental physiology.

[37]  D. Linden The P300: Where in the Brain Is It Produced and What Does It Tell Us? , 2005, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[38]  D. Tranel The effects of monetary incentive and frustrative nonreward on heart rate and electrodermal activity. , 1983, Psychophysiology.

[39]  C. Braun,et al.  Event-Related Brain Potentials Following Incorrect Feedback in a Time-Estimation Task: Evidence for a Generic Neural System for Error Detection , 1997, Journal of Cognitive Neuroscience.

[40]  Eveline A. Crone,et al.  Phasic heart rate responses to performance feedback in a time production task: effects of information versus valence , 2004, Biological Psychology.

[41]  C. Villalón,et al.  5-hydroxytryptamine and cardiovascular regulation. , 2008, Trends in pharmacological sciences.

[42]  M. Coles,et al.  The influence of the magnitude, probability, and valence of potential wins and losses on the amplitude of the feedback negativity. , 2012, Psychophysiology.

[43]  H. Nagaraja,et al.  Heart rate variability: origins, methods, and interpretive caveats. , 1997, Psychophysiology.

[44]  P. Lang,et al.  Electro-cortical and cardiac rate correlates of psychophysical judgment. , 1975, Psychophysiology.

[45]  M. W. van der Molen,et al.  A psychophysiological investigation of cognitive-energetic relations in human information processing: a heart rate/additive factors approach. , 1987, Acta psychologica.

[46]  M. Behbehani Functional characteristics of the midbrain periaqueductal gray , 1995, Progress in Neurobiology.

[47]  D. Tranel,et al.  The heart beats to reward: the effect of monetary incentive on heart rate. , 1982, Psychophysiology.

[48]  T. Robbins,et al.  Serotoninergic regulation of emotional and behavioural control processes , 2008, Trends in Cognitive Sciences.

[49]  Eveline A. Crone,et al.  Cardiac concomitants of feedback processing , 2003, Biological Psychology.

[50]  M. Weinand,et al.  Heart Rate and Heart Rate Variability Changes in the Intracarotid Sodium Amobarbital Test , 2001, Epilepsia.

[51]  Kewei Chen,et al.  Neural correlates of heart rate variability during emotion , 2009, NeuroImage.

[52]  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.

[53]  W. J. Meyers The influence of stimulus intensity and repetition on the mean evoked heart rate response. , 1969, Psychophysiology.

[54]  A. Beitz,et al.  Immunocytochemical localization of serotonin in the rat periaqueductal gray: A quantitative light and electron microscopic study , 1985, The Journal of comparative neurology.

[55]  H. Critchley,et al.  Cerebral correlates of autonomic cardiovascular arousal: a functional neuroimaging investigation in humans , 2000, The Journal of physiology.

[56]  J F Thayer,et al.  Phasic heart period reactions to cued threat and nonthreat stimuli in generalized anxiety disorder. , 2000, Psychophysiology.

[57]  Noriaki Kanayama,et al.  Brain and autonomic association accompanying stochastic decision-making , 2010, NeuroImage.

[58]  G. Stemmler,et al.  5-HTTLPR and anxiety modulate brain-heart covariation. , 2013, Psychophysiology.