Body signals, cardiac awareness, and the perception of time

Recent research suggests that our sense of time intervals in the range of seconds is directly related to activity in the insular cortex, which contains the primary sensory area for interoception. We therefore investigated whether performance in a duration reproduction task might correlate with individual interoceptive awareness and with measurable changes in autonomic activity during the task. Thirty-one healthy volunteers participated in an interoceptive (heartbeat) perception task and in repeated temporal reproduction trials using intervals of 8, 14, and 20s duration while skin conductance levels and cardiac and respiratory periods were recorded. We observed progressive increases in cardiac periods and decreases in skin conductance level during the encoding and (less reliably) the reproduction of these intervals. Notably, individuals' duration reproduction accuracy correlated positively both with the slope of cardiac slowing during the encoding intervals and with individual heartbeat perception scores. These results support the view that autonomic function and interoceptive awareness underpin our perception of time intervals in the range of seconds.

[1]  H. Critchley Review: Electrodermal Responses: What Happens in the Brain , 2002 .

[2]  A. Ehlers,et al.  Psychological and Perceptual Factors Associated With Arrhythmias and Benign Palpitations , 2000, Psychosomatic medicine.

[3]  E. Ravussin,et al.  Neuroanatomical correlates of hunger and satiation in humans using positron emission tomography. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Katya Rubia,et al.  The neural correlates of cognitive time management: a review. , 2004, Acta neurobiologiae experimentalis.

[5]  J. Staddon Interval timing: memory, not a clock , 2005, Trends in Cognitive Sciences.

[6]  A. Lawrence,et al.  Heartbeat perception in depression. , 2007, Behaviour research and therapy.

[7]  Mingxiong Huang,et al.  Neural representation of interval encoding and decision making. , 2004, Brain research. Cognitive brain research.

[8]  Edmund T Rolls,et al.  Time perception, impulsivity, emotionality, and personality in self-harming borderline personality disorder patients. , 2004, Journal of personality disorders.

[9]  A. Angrilli,et al.  The influence of affective factors on time perception , 1997, Perception & psychophysics.

[10]  Virginie van Wassenhove,et al.  The experience of time: neural mechanisms and the interplay of emotion, cognition and embodiment , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[11]  W. Roth,et al.  Marijuana and ethanol: Differential effects on time perception, heart rate, and subjective response , 1976, Psychopharmacology.

[12]  G. Hawkes,et al.  Autonomic effects on estimates of time: evidence for a physiological correlate of temporal experience. , 1961, Report. Army Medical Research Laboratory.

[13]  R. Barkley,et al.  Executive Functioning, Temporal Discounting, and Sense of Time in Adolescents with Attention Deficit Hyperactivity Disorder (ADHD) and Oppositional Defiant Disorder (ODD) , 2001, Journal of abnormal child psychology.

[14]  R. Barkley,et al.  Time perception and reproduction in young adults with attention deficit hyperactivity disorder. , 2001, Neuropsychology.

[15]  J E Tong,et al.  Effects of Heart-Rate Increase on Temporal Discrimination and Time Judgment by Two Groups of Delinquents , 1972, Perceptual and motor skills.

[16]  Martin P. Paulus,et al.  Accumulation of neural activity in the posterior insula encodes the passage of time , 2008, Neuropsychologia.

[17]  U. Karmarkar,et al.  Timing in the Absence of Clocks: Encoding Time in Neural Network States , 2007, Neuron.

[18]  A. Ehlers,et al.  Increased cardiac awareness in panic disorder. , 1992, Journal of abnormal psychology.

[19]  P. Tse,et al.  Time and the Brain: How Subjective Time Relates to Neural Time , 2005 .

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

[21]  Q. Aziz,et al.  Exploring relationships for visceral and somatic pain with autonomic control and personality , 2009, PAIN®.

[22]  Martin P. Paulus,et al.  Temporal horizons in decision making. , 2009 .

[23]  B Burle,et al.  Dissociation between activation and attention effects in time estimation: implications for internal clock models. , 2001, Journal of experimental psychology. Human perception and performance.

[24]  H. Eisler,et al.  Time perception: effects of sex and sound intensity on scales of subjective duration. , 1992, Scandinavian journal of psychology.

[25]  T. F. Sawyer,et al.  Contrasting task demands alter the perceived duration of brief time intervals , 1994, Perception & psychophysics.

[26]  S. Lane,et al.  Measurement of delay discounting using trial-by-trial consequences , 2003, Behavioural Processes.

[27]  J. Gibbon,et al.  Annals of the New York Academy of Sciences. Volume 423. Timing and Time Perception Held at New York on 10-13 May 1983, , 1984 .

[28]  Martin P Paulus,et al.  Now or later? Striatum and insula activation to immediate versus delayed rewards. , 2010, Journal of neuroscience, psychology, and economics.

[29]  Catalin V. Buhusi,et al.  What makes us tick? Functional and neural mechanisms of interval timing , 2005, Nature Reviews Neuroscience.

[30]  S. Droit-Volet,et al.  The time–emotion paradox , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[31]  Stuart D. Rosen,et al.  Breathlessness in humans activates insular cortex , 2000, Neuroreport.

[32]  Stephen W. Porges,et al.  Research methods for measurement of heart rate and respiration , 1992, Biological Psychology.

[33]  J. Gybels,et al.  Positron emission tomography study of a chronic pain patient successfully treated with somatosensory thalamic stimulation , 2000, Pain.

[34]  Scott W. Brown Attentional resources in timing: Interference effects in concurrent temporal and nontemporal working memory tasks , 1997, Perception & psychophysics.

[35]  Vladimir Hachinski,et al.  Human forebrain activation by visceral stimuli , 1999, The Journal of comparative neurology.

[36]  T. McCormack,et al.  Duration judgements in patients with schizophrenia , 2003, Psychological Medicine.

[37]  S. Porges Orienting in a defensive world: mammalian modifications of our evolutionary heritage. A Polyvagal Theory. , 1995, Psychophysiology.

[38]  P. Julu,et al.  A linear scale for measuring vagal tone in man. , 1992, Journal of autonomic pharmacology.

[39]  W. Meck Neuropharmacology of timing and time perception. , 1996, Brain research. Cognitive brain research.

[40]  J. B. Carter,et al.  Effect of Endurance Exercise on Autonomic Control of Heart Rate , 2003, Sports medicine.

[41]  Frank Munz,et al.  Central activation by histamine-induced itch: analogies to pain processing: a correlational analysis of O-15 H2O positron emission tomography studies , 2001, Pain.

[42]  A. Blewett Abnormal Subjective Time Experience in Depression , 1992, British Journal of Psychiatry.

[43]  W. Meck,et al.  Cortico-striatal circuits and interval timing: coincidence detection of oscillatory processes. , 2004, Brain research. Cognitive brain research.

[44]  M. Kisley,et al.  Deficits in auditory and visual temporal perception in schizophrenia , 2002, Cognitive neuropsychiatry.

[45]  H. Critchley Electrodermal responses: what happens in the brain. , 2002, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[46]  K. A. Provins,et al.  RELATION BETWEEN PHYSIOLOGICAL RESPONSES TO ENVIRONMENTAL HEAT AND TIME JUDGMENTS. , 1963, Journal of experimental psychology.

[47]  E. Osato,et al.  Relations among Heart Rate, Immediate Memory, and Time Estimation under Two Different Instructions , 1995, Perceptual and motor skills.

[48]  M. Bradley Natural selective attention: orienting and emotion. , 2009, Psychophysiology.

[49]  Laurent Hugueville,et al.  Neural network involved in time perception: An fMRI study comparing long and short interval estimation , 2005, Human brain mapping.

[50]  U. Scherrer,et al.  Stimulation of skin sympathetic nerve discharge by central command. Differential control of sympathetic outflow to skin and skeletal muscle during static exercise. , 1991, Circulation research.

[51]  David S. Leland,et al.  Impaired time perception and motor timing in stimulant-dependent subjects. , 2007, Drug and alcohol dependence.

[52]  K. Lesch,et al.  Neural Hyporesponsiveness and Hyperresponsiveness During Immediate and Delayed Reward Processing in Adult Attention-Deficit/Hyperactivity Disorder , 2009, Biological Psychiatry.

[53]  M. Bradley,et al.  Emotion and the motivational brain , 2010, Biological Psychology.

[54]  M. Craske,et al.  Interoceptive accuracy and panic. , 1999, Behaviour research and therapy.

[55]  W. Hiddemann,et al.  The relation between the experience of time and psychological distress in patients with hematological malignancies , 2006, Palliative and Supportive Care.

[56]  The relation of time estimation to certain physiological changes. , 1938 .

[57]  M. Wittmann The inner experience of time , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[58]  R. Halari,et al.  Impulsiveness as a timing disturbance: neurocognitive abnormalities in attention-deficit hyperactivity disorder during temporal processes and normalization with methylphenidate , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[59]  M. Paulus,et al.  Decision making, impulsivity and time perception , 2008, Trends in Cognitive Sciences.

[60]  M. Wittmann Die Neuropsychologie der Zeit – Kognitive und emotionale Modulatoren der zeitlichen Erfahrung , 2009 .

[61]  S. Hansen,et al.  Discordant mental and physical efforts in an autistic patient , 2004, Brain and Development.

[62]  F. Mauguière,et al.  Parietal and cingulate processes in central pain. A combined positron emission tomography (PET) and functional magnetic resonance imaging (fMRI) study of an unusual case , 2000, Pain.

[63]  M. Craske,et al.  Reactivity to interoceptive cues in nocturnal panic. , 2001, Journal of behavior therapy and experimental psychiatry.

[64]  Christian Kaufmann,et al.  Interoceptive awareness, anxiety and cardiovascular reactivity to isometric exercise. , 2007, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[65]  R. Miall,et al.  Distinct systems for automatic and cognitively controlled time measurement: evidence from neuroimaging , 2003, Current Opinion in Neurobiology.

[66]  R M Church,et al.  Properties of the Internal Clock a , 1984, Annals of the New York Academy of Sciences.

[67]  V. Hodapp,et al.  A comparison between two methods for assessing heartbeat perception. , 1992, Psychophysiology.

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

[69]  M. Treisman,et al.  The Internal Clock: Evidence for a Temporal Oscillator Underlying Time Perception with Some Estimates of its Characteristic Frequency , 1990, Perception.

[70]  M. Bauer,et al.  Time experience and time judgment in major depression, mania and healthy subjects. A controlled study of 93 subjects , 2004, Acta psychiatrica Scandinavica.

[71]  Johan Wessberg,et al.  Somatotopic Organization of Gentle Touch Processing in the Posterior Insular Cortex , 2009, The Journal of Neuroscience.

[72]  Maurizio Codispoti,et al.  Watching emotional movies: affective reactions and gender differences. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[73]  A. Craig,et al.  Emotional moments across time: a possible neural basis for time perception in the anterior insula , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[74]  Matthew B. Wall,et al.  Time perception: Manipulation of task difficulty dissociates clock functions from other cognitive demands , 2007, Neuropsychologia.

[75]  R M Church,et al.  Scalar Timing in Memory , 1984, Annals of the New York Academy of Sciences.

[76]  M. Craske,et al.  Accuracy of heartbeat perception in panic disorder, social phobia, and nonanxious subjects , 1995 .