Active vision varies across the cardiac cycle

Perception and cognition oscillate with fluctuating bodily states. For example, visual processing has been shown to change with alternating cardiac phases. Here, we study the heartbeat’s role for active information sampling—testing whether humans implicitly act upon their environment so that relevant signals appear during preferred cardiac phases. During the encoding period of a visual memory experiment, participants clicked through a set of emotional pictures to memorize them for a later recognition test. By self-paced key press, they actively prompted the onset of shortly (100-ms) presented pictures. Simultaneously recorded electrocardiograms allowed us to analyse the self-initiated picture onsets relative to the heartbeat. We find that self-initiated picture onsets vary across the cardiac cycle, showing an increase during cardiac systole, while memory performance was not affected by the heartbeat. We conclude that active information sampling integrates heart-related signals, thereby extending previous findings on the association between body-brain interactions and behaviour.

[1]  H. Critchley,et al.  The influence of physiological signals on cognition , 2018, Current Opinion in Behavioral Sciences.

[2]  Deborah Badoud,et al.  Afferent cardiac signals modulate attentional engagement to low spatial frequency fearful faces , 2017, Cortex.

[3]  G. Pezzulo,et al.  Increased heart rate after exercise facilitates the processing of fearful but not disgusted faces , 2018, Scientific Reports.

[4]  Martin Rolfs,et al.  Selective enhancement of orientation tuning before saccades. , 2017, Journal of vision.

[5]  Karl J. Friston,et al.  Uncertainty and stress: Why it causes diseases and how it is mastered by the brain , 2017, Progress in Neurobiology.

[6]  Paul A. Obrist,et al.  Cardiovascular Psychophysiology: Current Issues in Response Mechanisms, Biofeedback and Methodology , 2017 .

[7]  B. Friedman,et al.  Exteroceptive stimuli override interoceptive state in reaction time control. , 2017, Psychophysiology.

[8]  Martin Rolfs,et al.  Saccadic Eye Movements Impose a Natural Bottleneck on Visual Short-Term Memory , 2017, Journal of experimental psychology. Learning, memory, and cognition.

[9]  Tirin Moore,et al.  Spatial working memory alters the efficacy of input to visual cortex , 2017, Nature Communications.

[10]  Hugo D. Critchley,et al.  Feedback from the heart: Emotional learning and memory is controlled by cardiac cycle, interoceptive accuracy and personality , 2017, Biological Psychology.

[11]  L. Davachi,et al.  Emotional brain states carry over and enhance future memory formation , 2016, Nature Neuroscience.

[12]  Catherine Tallon-Baudry,et al.  Phase-amplitude coupling at the organism level: The amplitude of spontaneous alpha rhythm fluctuations varies with the phase of the infra-slow gastric basal rhythm , 2017, NeuroImage.

[13]  Hugo D. Critchley,et al.  Cardiac afferent activity modulates the expression of racial stereotypes , 2017, Nature Communications.

[14]  Wei Ji Ma,et al.  Bayesian microsaccade detection , 2017, Journal of vision.

[15]  W. K. Simmons,et al.  Evidence for a Large-Scale Brain System Supporting Allostasis and Interoception in Humans , 2017, Nature Human Behaviour.

[16]  Nikita Arora,et al.  Nasal Respiration Entrains Human Limbic Oscillations and Modulates Cognitive Function , 2016, The Journal of Neuroscience.

[17]  Christian Frings,et al.  Cardiac cycle time effects on selection efficiency in vision. , 2016, Psychophysiology.

[18]  Hinze Hogendoorn,et al.  Voluntary Saccadic Eye Movements Ride the Attentional Rhythm , 2016, Journal of Cognitive Neuroscience.

[19]  Marisa Carrasco,et al.  Saccade Preparation Reshapes Sensory Tuning , 2016, Current Biology.

[20]  M. Morrone,et al.  Rhythmic modulation of visual contrast discrimination triggered by action , 2016, Proceedings of the Royal Society B: Biological Sciences.

[21]  O. Blanke,et al.  The Insula Mediates Access to Awareness of Visual Stimuli Presented Synchronously to the Heartbeat , 2016, The Journal of Neuroscience.

[22]  Chris M Fiacconi,et al.  Knowing by heart: Visceral feedback shapes recognition memory judgments. , 2016, Journal of experimental psychology. General.

[23]  Heiner Deubel,et al.  Oculomotor selection underlies feature retention in visual working memory. , 2016, Journal of neurophysiology.

[24]  H. Critchley,et al.  Threat and the Body: How the Heart Supports Fear Processing , 2016, Trends in Cognitive Sciences.

[25]  Reinhold Kliegl,et al.  Microsaccades Are Coupled to Heartbeat , 2016, The Journal of Neuroscience.

[26]  J. Bhattacharya,et al.  Aroused with heart: Modulation of heartbeat evoked potential by arousal induction and its oscillatory correlates , 2015, Scientific Reports.

[27]  H. Schächinger,et al.  Baroreceptor activity impacts upon controlled but not automatic distractor processing , 2015, Biological Psychology.

[28]  Tor D Wager,et al.  Brain-Body Pathways Linking Psychological Stress and Physical Health , 2015, Current directions in psychological science.

[29]  Mara Mather,et al.  Cognitive control, dynamic salience, and the imperative toward computational accounts of neuromodulatory function , 2015, Behavioral and Brain Sciences.

[30]  W. K. Simmons,et al.  Interoceptive predictions in the brain , 2015, Nature Reviews Neuroscience.

[31]  Ben Greiner,et al.  Subject pool recruitment procedures: organizing experiments with ORSEE , 2015, Journal of the Economic Science Association.

[32]  G. Sandini,et al.  Rhythmic Oscillations of Visual Contrast Sensitivity Synchronized with Action , 2015, The Journal of Neuroscience.

[33]  Kees Mulder,et al.  Circular Statistics in R , 2015 .

[34]  J. D. McGaugh Consolidating memories. , 2015, Annual review of psychology.

[35]  Charles E. Schroeder,et al.  Motor contributions to the temporal precision of auditory attention , 2014, Nature Communications.

[36]  D. Bates,et al.  Fitting Linear Mixed-Effects Models Using lme4 , 2014, 1406.5823.

[37]  H. Critchley,et al.  Fear from the Heart: Sensitivity to Fear Stimuli Depends on Individual Heartbeats , 2014, The Journal of Neuroscience.

[38]  C. Tallon-Baudry,et al.  The neural subjective frame: from bodily signals to perceptual consciousness , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[39]  Mika P. Tarvainen,et al.  Kubios HRV - Heart rate variability analysis software , 2014, Comput. Methods Programs Biomed..

[40]  A. Seth Interoceptive inference, emotion, and the embodied self , 2013, Trends in Cognitive Sciences.

[41]  D. Mcintyre,et al.  Electrocutaneous pain thresholds are higher during systole than diastole , 2013, Biological Psychology.

[42]  H. Critchley,et al.  What the heart forgets: Cardiac timing influences memory for words and is modulated by metacognition and interoceptive sensitivity. , 2013, Psychophysiology.

[43]  H. Critchley,et al.  Visceral Influences on Brain and Behavior , 2013, Neuron.

[44]  Jin Fan,et al.  Spontaneous Brain Activity Relates to Autonomic Arousal , 2012, The Journal of Neuroscience.

[45]  Tjeerd W. Boonstra,et al.  Modulation of Human Muscle Spindle Discharge by Arterial Pulsations - Functional Effects and Consequences , 2012, PloS one.

[46]  J. Thayer,et al.  eview meta-analysis of heart rate variability and neuroimaging studies : Implications or heart rate variability as a marker of stress and health , 2012 .

[47]  C. Shapiro,et al.  STOP, THAT and One Hundred Other Sleep Scales , 2012 .

[48]  Aldebaro Klautau,et al.  New approach for T-wave end detection on electrocardiogram: Performance in noisy conditions , 2011, Biomedical engineering online.

[49]  Emeran A. Mayer,et al.  Gut feelings: the emerging biology of gut–brain communication , 2011, Nature Reviews Neuroscience.

[50]  M. Mather,et al.  Arousal-Biased Competition in Perception and Memory , 2011, Perspectives on psychological science : a journal of the Association for Psychological Science.

[51]  Harjit Gill,et al.  The Timing of Onset of Mechanical Systole and Diastole in Reference to the QRS-T Complex: a Study to Determine Performance Criteria for a Non-Invasive Diastolic Timed Vibration Massage System in Treatment of Potentially Unstable Cardiac Disorders , 2010, Cardiovascular engineering.

[52]  Rhodri Cusack,et al.  Listening to Your Heart , 2010, Psychological science.

[53]  Thomas. Lewis,et al.  The Mechanism and Graphic Registration of the Heart Beat , 2010 .

[54]  Karl J. Friston The free-energy principle: a unified brain theory? , 2010, Nature Reviews Neuroscience.

[55]  T. Blumenthal,et al.  Cardiac modulation of startle: Effects on eye blink and higher cognitive processing , 2009, Brain and Cognition.

[56]  Hadley Wickham,et al.  ggplot2 - Elegant Graphics for Data Analysis (2nd Edition) , 2017 .

[57]  Caroline Di Bernardi Luft,et al.  Heart rate variability and cognitive function: Effects of physical effort , 2009, Biological Psychology.

[58]  L. S. Fridericia Die Systolendauer im Elektrokardiogramm bei normalen Menschen und bei Herzkranken , 2009 .

[59]  T. Jaeger,et al.  Categorical Data Analysis: Away from ANOVAs (transformation or not) and towards Logit Mixed Models. , 2008, Journal of memory and language.

[60]  C. Wiggers Modern Aspects of the Circulation in Health and Disease , 2008 .

[61]  D. Mcintyre,et al.  Simple reaction time as a function of the phase of the cardiac cycle in young adults at risk for hypertension. , 2008, Psychophysiology.

[62]  O. Pollatos,et al.  Emotional processing and emotional memory are modulated by interoceptive awareness , 2008 .

[63]  David McIntyre,et al.  Psychomotor speed in hypertension: effects of reaction time components, stimulus modality, and phase of the cardiac cycle. , 2007, Psychophysiology.

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

[65]  H. Lyytinen,et al.  Shot placement within cardiac cycle in junior elite rifle shooters , 2007 .

[66]  R. Gregory The Most Expensive Painting in the World , 2007, Perception.

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

[68]  Romain Meeusen,et al.  Psychomotor Speed , 2006, Sports medicine.

[69]  Daniel L Schacter,et al.  Amygdala Activity Is Associated with the Successful Encoding of Item, But Not Source, Information for Positive and Negative Stimuli , 2006, The Journal of Neuroscience.

[70]  R. Cabeza,et al.  Cognitive neuroscience of emotional memory , 2006, Nature Reviews Neuroscience.

[71]  Elizabeth A. Kensinger,et al.  Memory enhancement for emotional words: Are emotional words more vividly remembered than neutral words? , 2003, Memory & cognition.

[72]  V. Macefield Cardiovascular and Respiratory Modulation of Tactile Afferents in the Human Finger Pad , 2003, Experimental physiology.

[73]  J. Thayer,et al.  Vagal influence on working memory and attention. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[74]  A. Craig How do you feel? Interoception: the sense of the physiological condition of the body , 2002, Nature Reviews Neuroscience.

[75]  A. M. Reilly,et al.  Central Mechanisms Underlying Short‐ And Long‐Term Regulation Of The Cardiovascular System , 2002, Clinical and experimental pharmacology & physiology.

[76]  J. Meere The role of attention. , 2002 .

[77]  C. Saper The central autonomic nervous system: conscious visceral perception and autonomic pattern generation. , 2002, Annual review of neuroscience.

[78]  Hartmut Schächinger,et al.  Cardiovascular Indices of Peripheral and Central Sympathetic Activation , 2001, Psychosomatic medicine.

[79]  Stephan Hamann,et al.  Cognitive and neural mechanisms of emotional memory , 2001, Trends in Cognitive Sciences.

[80]  T. Elbert,et al.  Psychophysiology of arterial baroreceptors and the etiology of hypertension , 2001, Biological Psychology.

[81]  F. Abboud,et al.  Mechanisms Determining Sensitivity of Baroreceptor Afferents in Health and Disease , 2001, Annals of the New York Academy of Sciences.

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

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

[84]  P H Schiller,et al.  Visual representations during saccadic eye movements. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[85]  James L. McGaugh,et al.  Mechanisms of emotional arousal and lasting declarative memory , 1998, Trends in Neurosciences.

[86]  J. Kurths,et al.  Heartbeat synchronized with ventilation , 1998, Nature.

[87]  M Ito,et al.  Simple Reaction Time as a Function of Number and Similarity of Sequenced Elements in Rapid Force Production , 1997, Perceptual and motor skills.

[88]  D G Pelli,et al.  The VideoToolbox software for visual psychophysics: transforming numbers into movies. , 1997, Spatial vision.

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

[90]  H. Deubel,et al.  Saccade target selection and object recognition: Evidence for a common attentional mechanism , 1996, Vision Research.

[91]  G. Breithardt,et al.  Heart rate variability: standards of measurement, physiological interpretation and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. , 1996 .

[92]  B. Dosher,et al.  The role of attention in the programming of saccades , 1995, Vision Research.

[93]  J. Fahrenberg,et al.  Methodological guidelines for impedance cardiography. , 1990, Psychophysiology.

[94]  E. Lindholm,et al.  Cardiac-related cortical inhibition during a fixed foreperiod reaction time task. , 1986, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[95]  H. Boudoulas,et al.  Linear relationship between electrical systole, mechanical systole, and heart rate. , 1981, Chest.

[96]  R. Schandry,et al.  Heart beat perception and emotional experience. , 1981, Psychophysiology.

[97]  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.

[98]  Richard P. Lewis,et al.  REVIEWS OF CONTEMPORARY LABORATORY METHODS , 2005 .

[99]  C. C. Wood,et al.  Cardiac cycle time effects on performance, phasic cardiac responses, and their intercorrelation in choice reaction time. , 1977, Psychophysiology.

[100]  C. Sandman,et al.  Heart rate and cardiac phase influences on visual perception. , 1977, Journal of comparative and physiological psychology.

[101]  L. Salzman,et al.  Heart Rate and Cardiac Cycle Effects on Reaction Time , 1976 .

[102]  B. Pappas,et al.  Cardiac Cycle Phase and Movement and Reaction Times , 1976, Perceptual and motor skills.

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

[104]  G. Langer Heart: excitation-contraction coupling. , 1973, Annual review of physiology.

[105]  J. E. James The effects of altering mean pressure, pulse pressure and pulse frequency on the impulse activity in baroreceptor fibres from the aortic arch and right subclavian artery in the rabbit , 1971 .

[106]  J. Botwinick,et al.  Stimulation in different phases of the cardiac cycle and reaction time. , 1970, Psychophysiology.

[107]  C. Spielberger,et al.  Manual for the State-Trait Anxiety Inventory , 1970 .

[108]  A. Weissler,et al.  Bedside technics for the evaluation of ventricular function in man. , 1969, The American journal of cardiology.

[109]  A. Weissler,et al.  Systolic Time Intervals in Heart Failure in Man , 1968, Circulation.

[110]  E. Callaway,et al.  INTERACTION BETWEEN THE VISUAL EVOKED RESPONSE AND TWO SPONTANEOUS BIOLOGICAL RHYTHMS: THE EEG ALPHA CYCLE AND THE CARDIAC AROUSAL CYCLE * , 1964, Annals of the New York Academy of Sciences.

[111]  J. Mitchell,et al.  Duration of the Phases of Left Ventricular Systole , 1963, Circulation research.

[112]  J. Birren,et al.  Reaction Time as a Function of the Cardiac Cycle in Young Adults , 1963, Science.

[113]  M. I. Ferrer,et al.  THE RELATIONSHIP BETWEEN ELECTRICAL AND MECHANICAL EVENTS IN THE CARDIAC CYCLE OF MAN* , 1949, British heart journal.

[114]  Warren P. Lombard,et al.  THE DURATION OF THE SYSTOLE OF THE LEFT VENTRICLE OF MAN , 1926 .

[115]  C. Wiggers STUDIES ON THE CONSECUTIVE PHASES OF THE CARDIAC CYCLE: II. The Laws Governing the Relative Durations of Ventricular Systole and Diastole , 1921 .

[116]  Fitting linear mixed-effects models , 2022 .