Neural substrates of time perception and impulsivity

Several studies provide empirical evidence for the association between impulsivity and time perception. However, little is known about the neural substrates underlying this function. This investigation examined the influence of impulsivity on neural activation patterns during the encoding and reproduction of intervals with durations of 3, 9 and 18s using event-related functional magnetic resonance imaging (fMRI). Twenty-seven subjects participated in this study, including 15 high impulsive subjects that were classified based on their self-rating. FMRI activation during the duration reproduction task was correlated with measures of two self-report questionnaires related to the concept of impulsivity (Barratt Impulsiveness Scale, BIS; Zimbardo Time Perspective Inventory, ZTPI). Behaviorally, those individuals who under-reproduced temporal intervals also showed lower scores on the ZTPI future perspective subscale and higher scores on the BIS. FMRI activation revealed an accumulating pattern of neural activity peaking at the end of the 9- and 18-s intervals within right posterior insula. Activations of brain regions during the reproduction phase of the timing task, such as those related to motor execution as well as to the 'core control network' - encompassing the inferior frontal and medial frontal cortices, the anterior insula as well as the inferior parietal cortex - were significantly correlated with reproduced duration, as well as with BIS and ZTPI subscales. In particular, the greater activation in these regions the shorter were the reproduced intervals, the more impulsive was an individual and the less pronounced the future perspective. Activation in the core control network, thus, may form a biological marker for cognitive time management and for impulsiveness.

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

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

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

[4]  F. Vollenweider,et al.  Effects of varied doses of psilocybin on time interval reproduction in human subjects , 2008, Neuroscience Letters.

[5]  J. Gibbon,et al.  Timing and time perception. , 1984, Annals of the New York Academy of Sciences.

[6]  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.

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

[8]  P. Zimbardo,et al.  Putting Time in Perspective: A Valid, Reliable Individual-Differences Metric , 1999 .

[9]  W. Senn,et al.  Climbing Neuronal Activity as an Event-Based Cortical Representation of Time , 2004, The Journal of Neuroscience.

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

[11]  E T Rolls,et al.  Impulsivity, time perception, emotion and reinforcement sensitivity in patients with orbitofrontal cortex lesions. , 2004, Brain : a journal of neurology.

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

[13]  P. Zimbardo,et al.  Who's Smoking, Drinking, and Using Drugs? Time Perspective as a Predictor of Substance Use , 1999 .

[14]  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.

[15]  F. Castellanos,et al.  Temporal and probabilistic discounting of rewards in children and adolescents: Effects of age and ADHD symptoms , 2006, Neuropsychologia.

[16]  S. Lane,et al.  Relationships Among Laboratory and Psychometric Measures of Impulsivity: Implications in Substance Abuse and Dependence , 2003 .

[17]  J. Quickfall,et al.  Brain neuroimaging in cannabis use: a review. , 2006, The Journal of neuropsychiatry and clinical neurosciences.

[18]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[19]  David S. Leland,et al.  Reduced Behavioral and Neural Activation in Stimulant Users to Different Error Rates during Decision Making , 2008, Biological Psychiatry.

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

[21]  Patricia A. Reuter-Lorenz,et al.  Age differences in prefontal recruitment during verbal working memory maintenance depend on memory load , 2010, Cortex.

[22]  Carmen Santisteban,et al.  Impulsivity: a review. , 2006, Psicothema.

[23]  R. Smart Future time perspectives in alcoholics and social drinkers. , 1968, Journal of Abnormal Psychology.

[24]  P. Allen,et al.  Relation of individual differences in impulsivity to nonclinical emotional decision making , 2008, Journal of the International Neuropsychological Society.

[25]  L. Green,et al.  Area under the curve as a measure of discounting. , 2001, Journal of the experimental analysis of behavior.

[26]  H. Zelaznik,et al.  The Cerebellum and Event Timing , 2002, Annals of the New York Academy of Sciences.

[27]  L. F. Barrett,et al.  Handbook of Emotions , 1993 .

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

[29]  J. Nurnberger,et al.  A new, semi-structured psychiatric interview for use in genetic linkage studies: a report on the reliability of the SSAGA. , 1994, Journal of studies on alcohol.

[30]  Hugh Garavan,et al.  Evidence of increased activation underlying cognitive control in ecstasy and cannabis users , 2010, NeuroImage.

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

[32]  T. Robbins,et al.  Stop-signal inhibition disrupted by damage to right inferior frontal gyrus in humans , 2003, Nature Neuroscience.

[33]  Jonathan D. Cohen,et al.  Improved Assessment of Significant Activation in Functional Magnetic Resonance Imaging (fMRI): Use of a Cluster‐Size Threshold , 1995, Magnetic resonance in medicine.

[34]  B. Reynolds,et al.  Measuring state changes in human delay discounting: an experiential discounting task , 2004, Behavioural Processes.

[35]  Jeffrey R Binder,et al.  Neural systems supporting timing and chronometric counting: an FMRI study. , 2004, Brain research. Cognitive brain research.

[36]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[37]  Daniel Tranel,et al.  Right ventromedial prefrontal cortex: a neuroanatomical correlate of impulse control in boys. , 2009, Social cognitive and affective neuroscience.

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

[39]  Benjamin Morillon,et al.  Three Stages and Four Neural Systems in Time Estimation , 2009, The Journal of Neuroscience.

[40]  D. Delis,et al.  Evidence for subtle verbal fluency deficits in occasional stimulant users: quick to play loose with verbal rules. , 2011, Journal of psychiatric research.

[41]  Walter Schneider,et al.  The cognitive control network: Integrated cortical regions with dissociable functions , 2007, NeuroImage.

[42]  Robert Jech,et al.  Cumulative blood oxygenation-level-dependent signal changes support the ‘time accumulator’ hypothesis , 2005, Neuroreport.

[43]  Martin P. Paulus,et al.  Human Neuroscience , 2022 .

[44]  Franck Vidal,et al.  Timing functions of the supplementary motor area: an event-related fMRI study. , 2004, Brain research. Cognitive brain research.

[45]  Vani Pariyadath,et al.  Is subjective duration a signature of coding efficiency? , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

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

[47]  M. Carrillo-de-la-Peña,et al.  Comparison among Various Methods of Assessment of Impulsiveness , 1993, Perceptual and motor skills.

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

[49]  Ernst Pöppel,et al.  Pre-semantically defined temporal windows for cognitive processing , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[50]  R W Cox,et al.  AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. , 1996, Computers and biomedical research, an international journal.

[51]  A. D. Craig,et al.  Interoception and emotion: A neuroanatomical perspective. , 2008 .

[52]  Martin Wiener,et al.  The image of time: A voxel-wise meta-analysis , 2010, NeuroImage.

[53]  Matthew S Stanford,et al.  Impulsive and premeditated aggression: a factor analysis of self-reported acts , 1999, Psychiatry Research.

[54]  Marc Wittmann,et al.  Body signals, cardiac awareness, and the perception of time , 2011, Biological Psychology.

[55]  J. Patton,et al.  Factor structure of the Barratt impulsiveness scale. , 1995, Journal of clinical psychology.

[56]  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.

[57]  Martin Wiener,et al.  Cognitive timing: Neuropsychology and anatomic basis , 2009, Brain Research.

[58]  H. Critchley,et al.  A common role of insula in feelings, empathy and uncertainty , 2009, Trends in Cognitive Sciences.

[59]  Katya Rubia,et al.  Evidence for a pure time perception deficit in children with ADHD. , 2002, Journal of child psychology and psychiatry, and allied disciplines.

[60]  S. Samson,et al.  Is time reproduction sensitive to sensory modalities? , 2009 .

[61]  M. Shadlen,et al.  Representation of Time by Neurons in the Posterior Parietal Cortex of the Macaque , 2003, Neuron.

[62]  Dennis Velakoulis,et al.  Insular cortex volume and impulsivity in teenagers with first-presentation borderline personality disorder , 2009, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[63]  V. Walsh,et al.  The parietal cortex and the representation of time, space, number and other magnitudes , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[64]  W. Meck,et al.  How emotions colour our perception of time , 2007, Trends in Cognitive Sciences.

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

[66]  Rita Z. Goldstein,et al.  Thalamo-cortical dysfunction in cocaine abusers: Implications in attention and perception , 2007, Psychiatry Research: Neuroimaging.

[67]  E. Barratt,et al.  Psychiatric aspects of impulsivity. , 2001, The American journal of psychiatry.

[68]  Werner Ehm,et al.  The dual klepsydra model of internal time representation and time reproduction. , 2006, Journal of theoretical biology.

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

[70]  W. Reith,et al.  Impairment of fronto-striatal and parietal cerebral networks correlates with attention deficit hyperactivity disorder (ADHD) psychopathology in adults — A functional magnetic resonance imaging (fMRI) study , 2010, Psychiatry Research: Neuroimaging.

[71]  David S. Leland,et al.  Increased risk-taking decision-making but not altered response to punishment in stimulant-using young adults. , 2005, Drug and alcohol dependence.

[72]  R. Gonzalez Acute and Non-acute Effects of Cannabis on Brain Functioning and Neuropsychological Performance , 2007, Neuropsychology Review.

[73]  L. Green,et al.  Discounting of delayed rewards: Models of individual choice. , 1995, Journal of the experimental analysis of behavior.

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

[75]  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.

[76]  F. Melges,et al.  Time sense, emotions, and acute mental illness. , 1966, Journal of psychiatric research.

[77]  H. de Wit,et al.  Reward discounting as a measure of impulsive behavior in a psychiatric outpatient population. , 2000, Experimental and clinical psychopharmacology.

[78]  W. Bickel,et al.  Shortened time horizons and insensitivity to future consequences in heroin addicts. , 1998, Addiction.

[79]  W. Bickel,et al.  Heroin addicts have higher discount rates for delayed rewards than non-drug-using controls. , 1999 .

[80]  D. Heeger,et al.  Linear Systems Analysis of Functional Magnetic Resonance Imaging in Human V1 , 1996, The Journal of Neuroscience.

[81]  Martin P Paulus,et al.  Decision-Making Dysfunctions in Psychiatry—Altered Homeostatic Processing? , 2007, Science.

[82]  M. Wittmann,et al.  Temporal reproduction: further evidence for two processes. , 2007, Acta psychologica.

[83]  C. Caltagirone,et al.  Neural networks engaged in milliseconds and seconds time processing: evidence from transcranial magnetic stimulation and patients with cortical or subcortical dysfunction , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[84]  S. Droit-Volet,et al.  Counting in a time discrimination task in children and adults , 2006, Behavioural Processes.

[85]  P. A. Lewis,et al.  A right hemispheric prefrontal system for cognitive time measurement , 2006, Behavioural Processes.

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

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

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

[89]  J. Patton,et al.  Toward a Conceptualization of Impulsivity: Components across the Behavioral and Self-Report Domains. , 1987, Multivariate behavioral research.