Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Opinion
  • Published:

The inner sense of time: how the brain creates a representation of duration

Abstract

A large number of competing models exist for how the brain creates a representation of time. However, several human and animal studies point to 'climbing neural activation' as a potential neural mechanism for the representation of duration. Neurophysiological recordings in animals have revealed how climbing neural activation that peaks at the end of a timed interval underlies the processing of duration, and, in humans, climbing neural activity in the insular cortex, which is associated with feeling states of the body and emotions, may be related to the cumulative representation of time.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1: The dual klepsydra model.
Figure 2: Mean cardiac periods during interval timing.

Similar content being viewed by others

References

  1. Wittmann, M. & Paulus, M. P. Decision making, impulsivity and time perception. Trends Cogn. Sci. 12, 7–12 (2008).

    Article  PubMed  Google Scholar 

  2. Wittmann, M. & Paulus, M. P. Temporal horizons in decision making. J. Neurosci. Psychol. Econ. 2, 1–11 (2009).

    Article  Google Scholar 

  3. Wittmann, M. & van Wassenhove, V. The experience of time: neural mechanisms and the interplay of emotion, cognition and embodiment. Phil. Trans. R. Soc. B 364, 1809–1813 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  4. Ivry, R. B. & Schlerf, J. E. Dedicated and intrinsic models of time perception. Trends Cogn. Sci. 12, 273–280 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  5. Treisman, M. Temporal discrimination and the difference interval: implications for a model of the “internal clock”. Psychol. Monogr. 77, 1–31 (1963).

    Article  CAS  PubMed  Google Scholar 

  6. Gibbon, J., Church, R. M. & Meck, W. H. in Timing and Time Perception. Vol. 423 (eds Gibbon, J. & Allan, L.) 52–77 (New York Academy of Sciences, 1984).

    Google Scholar 

  7. Zakay, D. & Block, R. A. Temporal cognition. Curr. Dir. Psychol. Sci. 6, 12–16 (1997).

    Article  Google Scholar 

  8. Taatgen, N. A., van Rijn, H. & Anderson, J. R. An integrated theory of prospective time interval estimation: the role of cognition, attention and learning. Psychol. Rev. 114, 577–598 (2007).

    Article  PubMed  Google Scholar 

  9. van Wassenhove, V. Minding time in an amodal representational space. Phil. Trans. R. Soc. B 364, 1815–1830 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  10. Staddon, J. E. R. Interval timing: memory, not a clock. Trends Cogn. Sci. 9, 312–314 (2005).

    Article  CAS  PubMed  Google Scholar 

  11. Marchetti, G. Studies on time: a proposal on how to get out of circularity. Cogn. Process 10, 7–40 (2009).

    Article  PubMed  Google Scholar 

  12. Eagleman, D. & Pariyadath, V. Is subjective duration a signature for coding efficiency? Phil. Trans. R. Soc. B 364, 1841–1852 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  13. Buonomano, D. V. & Maass, W. State-dependent computations: spatiotemporal processing in cortical networks. Nature Rev. Neurosci. 10, 113–125 (2009).

    Article  CAS  Google Scholar 

  14. Wackermann, J. & Ehm, W. The dual klepsydra model of internal time representation and time reproduction. J. Theor. Biol. 239, 482–493 (2006).

    Article  PubMed  Google Scholar 

  15. Buhusi, C. V. & Meck, W. H. What makes us tick? Functional and neural mechanisms of interval timing. Nature Rev. Neurosci. 6, 755–765 (2005).

    Article  CAS  Google Scholar 

  16. Bueti, D. & Walsh, V. The parietal cortex and the respresentation of time, space, number and other magnitudes. Phil. Trans. R. Soc. B 364, 1831–1840 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  17. Ivry, R. B., Spencer, R. M., Zelaznik, H. N. & Diedrichsen, J. The cerebellum and event timing. Ann. NY Acad. Sci. 978, 302–317 (2002).

    Article  PubMed  Google Scholar 

  18. Lewis, P. A. & Miall, R. C. Remembering the time: a continuous clock. Trends Cogn. Sci. 10, 401–406 (2006).

    Article  PubMed  Google Scholar 

  19. Craig, A. D. Emotional moments across time: a possible neural basis for time perception in the anterior insula. Phil. Trans. R. Soc. B 364, 1933–1942 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  20. Lebedev, M. A., O'Doherty, J. E. & Nicolelis, M. A. L. Decoding of temporal intervals from cortical ensemble activity. J. Neurophysiol. 99, 166–186 (2008).

    Article  PubMed  Google Scholar 

  21. Mita, A., Mushiake, H., Shima, K., Matsuzaka, Y. & Tanji, J. Interval time coding by neurons in the presupplementary motor areas. Nature Neurosci. 12, 502–507 (2009).

    Article  CAS  PubMed  Google Scholar 

  22. Merchant, H., Zarco, W., Pérez, O., Prado, L. & Bartolo, R. Measuring time with different neural chronometers during a synchronization-continuation task. Proc. Natl Acad. Sci. USA 108, 19784–19789 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Casini, L. & Vidal, F. The SMAs: neural substrate of the temporal accumulator? Front. Integr. Neurosci. 5, 35 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  24. Pouthas, V. & Perbal, S. Time perception depends on accurate clock mechanisms as well as unimpaired attention and memory processes. Acta Neurobiol. Exp. 64, 367–385 (2004).

    Google Scholar 

  25. Meck, W. Neuropsychology of timing and time perception. Brain Cog. 58, 1–8 (2005).

    Article  Google Scholar 

  26. Lewis, P. A. & Miall, R. C. Distinct systems for automatic and cognitively controlled time measurement: evidence from neuroimaging. Curr. Opin. Neurobiol. 13, 250–255 (2003).

    Article  CAS  PubMed  Google Scholar 

  27. Wiener, M., Turkeltaub, P. & Coslett, H. B. The image of time: a voxel-wise meta-analysis. NeuroImage 49, 1728–1740 (2010).

    Article  PubMed  Google Scholar 

  28. Koch, G., Oliveri, M. & Caltagirone, C. Neural networks engaged in milliseconds and seconds time processing: evidence from transcranial magnetic stimulation and patients with cortical or subcortical dysfunction. Phil. Trans. R. Soc. B 364, 1907–1918 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  29. Harrington, D. L. & Haaland, K. Y. Neural underpinnings of temporal processing: a review of focal lesion, pharmacological, and functional imaging research. Rev. Neurosci. 10, 91–116 (1999).

    Article  CAS  PubMed  Google Scholar 

  30. Coslett, H. B., Shenton, J., Dyer, T. & Wiener, M. Cognitive timing: neuropsychology and anatomic basis. Brain Res. 1254, 38–48 (2009).

    Article  CAS  PubMed  Google Scholar 

  31. Coull, J. T., Nazarian, B. & Vidal, F. Timing, storage, and comparison of stimulus duration engage discrete anatomical components of a perceptual timing network. J. Cogn. Neurosci. 20, 2185–2197 (2008).

    Article  PubMed  Google Scholar 

  32. Buonomano, D. V., Bramen, J. & Khodadadifar, M. Influence of the interstimulus interval on temporal processing and learning: testing the state-dependent network model. Phil. Trans. R. Soc. B 364, 1865–1874 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  33. Spencer, R. M. C., Karmarkar, U. & Ivry, R. B. Evaluating dedicated and intrinsic models of temporal encoding by varying context. Phil. Trans. R. Soc. B 364, 1853–1864 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  34. Rammsayer, T. H. Neuropharmacological evidence for different timing mechanisms in humans. Q. J. Exp. Psychol. B 52, 273–286 (1999).

    Article  CAS  PubMed  Google Scholar 

  35. Rammsayer, T. H. Differences in duration discrimination of filled and empty auditory intervals as a function of base duration. Atten. Percept. Psychophys. 72, 1591–1600 (2010).

    Article  PubMed  Google Scholar 

  36. Fraisse, P. Perception and estimation of time. Ann. Rev. Psychol. 35, 1–36 (1984).

    Article  CAS  Google Scholar 

  37. Pöppel, E. A hierarchical model of temporal perception. Trends Cogn. Sci. 1, 56–61 (1997).

    Article  PubMed  Google Scholar 

  38. Wittmann, M. Moments in time. Front. Integr. Neurosci. 5, 66 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  39. Nakajima, Y., Shimojo, S. & Sugita, Y. On the perception of two successive sound bursts. Psychol. Res. 41, 335–344 (1980).

    Article  CAS  PubMed  Google Scholar 

  40. Getty, D. J. Discrimination of short temporal intervals: a comparison of two models. Percept. Psychophys. 18, 1–8 (1975).

    Article  Google Scholar 

  41. Ulbrich, P., Churan, J., Fink, M. & Wittmann. M. Temporal reproduction: further evidence for two processes. Acta Psychol. 125, 51–65 (2007).

    Article  Google Scholar 

  42. Lejeune, H. & Wearden, J. H. Vierordt's The Experimental Study Of The Time Sense (1868) and its legacy. Eur. J. Cogn. Psychol. 21, 941–960 (2009).

    Article  Google Scholar 

  43. Noulhiane, M., Pouthas, V. & Samson, S. Is time reproduction sensitive to sensory modalities? Eur. J. Cogn. Psychol. 21, 18–34 (2009).

    Article  Google Scholar 

  44. Morillon, B., Kell, C. A. & Giraud, A. L. Three stages and four neural systems in time estimation. J. Neurosci. 29, 14803–14811 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Droit-Volet, S. & Gil, S. The time-emotion paradox. Phil. Trans. R. Soc. B 364, 1943–1954 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  46. Wittmann, M. The inner sense of time. Phil. Trans. R. Soc. B 364, 1955–1967 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  47. Schirmer, A. How emotions change time. Front. Integr. Neurosci. 5, 58 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  48. Noulhiane, M., Mella, N., Samson, S., Ragot, R. & Pouthas, V. How emotional auditory stimuli modulate time perception. Emotion 7, 697–704 (2007).

    Article  PubMed  Google Scholar 

  49. Droit-Volet, S. & Meck, W. H. How emotions colour our perception of time. Trends Cogn. Sci. 11, 504–513 (2007).

    Article  PubMed  Google Scholar 

  50. Angrilli, A., Cherubini, P., Pavese, A. & Manfredini, S. The influence of affective factors on time perception. Percept. Psychophys. 59, 972–982 (1997).

    Article  CAS  PubMed  Google Scholar 

  51. Effron, D. A., Niedenthal, P. M., Gil, S. & Droit-Volet, S. Embodied temporal perception of emotion. Emotion 6, 1–9 (2006).

    Article  PubMed  Google Scholar 

  52. Falk, J. L. & Bindra, D. Judgment of time as a function of serial position and stress. J. Exp. Psychol. 47, 279–282 (1954).

    Article  CAS  PubMed  Google Scholar 

  53. Watts, F. N. & Sharrock, R. Fear and time estimation. Percept. Mot. Skills 59, 597–598 (1984).

    Article  CAS  PubMed  Google Scholar 

  54. Wearden, J. H. & Penton-Voak, I. S. Feeling the heat: body temperature and the rate of subjective time, revisited. Q. J. Exp. Psychol. B 48, 129–141 (1995).

    CAS  PubMed  Google Scholar 

  55. Somov, P. G. Time perception as a measure of pain intensity and pain type. J. Back Muscoloskelet. Rehabil. 14, 111–121 (2000).

    Article  Google Scholar 

  56. Craig, A. D. How do you feel — now? The anterior insula and human awareness. Nature Rev. Neurosci. 10, 59–70 (2009).

    Article  CAS  Google Scholar 

  57. Wittmann, M., Simmons, A. N., Aron, J. & Paulus, M. P. Accumulation of neural activity in the posterior insula encodes the passage of time. Neuropsychologia 48, 3110–3120 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  58. Wittmann, M. et al. Neural substrates of time perception and impulsivity. Brain Res. 1406, 43–58 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Kosillo, P. & Smith, A. T. The role of the human anterior insular cortex in time processing Brain Struct. Funct. 214, 623–628 (2010).

    Article  CAS  PubMed  Google Scholar 

  60. Meissner, K. & Wittmann, M. Body signals, cardiac awareness, and the perception of time. Biol. Psychol. 86, 289–297 (2011).

    Article  PubMed  Google Scholar 

  61. Sysoeva, O. V., Wittmann, M. & Wackermann, J. Neural representation of temporal duration: coherent findings obtained with the 'lossy integration' model. Front. Integr. Neurosci. 5, 37 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  62. Pollatos, O., Herbert, B. M., Kaufmann, C., Auer, D. P. & Schandry, R. Interoceptive awareness, anxiety and cardiovascular reactivity to isometric exercise. Int. J. Psychophysiol. 65, 167–173 (2007).

    Article  PubMed  Google Scholar 

  63. Coull, J. T. & Nobre, A. C. Dissociating explicit timing from temporal expectation with fMRI. Curr. Opin. Neurobiol. 18, 137–144 (2008).

    Article  CAS  PubMed  Google Scholar 

  64. Jin, D. Z., Fujii, N. & Graybiel, A. M. Neural representation of time in cortico-basal ganglia circuits. Proc. Natl Acad. Sci. USA 106, 19156–19161 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Matell, M. S., Shea-Brown, E., Gooch, C., Wilson, A. G. & Rinzel, J. A heterogeneous population code for elapsed time in rat medial agranular cortex. Behav. Neurosci. 125, 54–73 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  66. Niki, H. & Watanabe, M. Prefrontal and cingulate unit activity during timing behavior in the monkey. Brain Res. 171, 213–224 (1979).

    Article  CAS  PubMed  Google Scholar 

  67. Leon, M. I. & Shadlen, M. N. Representation of time by neurons in the posterior parietal cortex of the macaque. Neuron 38, 317–327 (2003).

    Article  CAS  PubMed  Google Scholar 

  68. Janssen, P. & Shadlen, M. N. A representation of the hazard rate of elapsed time in macaque are LIP. Nature Neurosci. 8, 234–241 (2005).

    Article  CAS  PubMed  Google Scholar 

  69. Kalenscher, T., Ohmann, T., Windmann, S., Freund, N. & Güntürkün, O. Single forebrain neurons represent interval timing and reward amount during response scheduling. Eur. J. Neurosci. 24, 2923–2931 (2006).

    Article  PubMed  Google Scholar 

  70. Renoult, L., Roux, S. & Riehle, A. Time is a rubberhand: neural activity in monkey motor cortex in relation to time estimation. Eur. J. Neurosci. 23, 3098–3108 (2006).

    Article  PubMed  Google Scholar 

  71. Durstewitz, D. Self-organizing neural integrator predicts interval times through climbing activity. J. Neurosci. 23, 5342–5353 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Reutimann, J., Yakovlev, V., Fusi, S. & Senn, W. Climbing neural activity as an event-based cortical representation of time. J. Neurosci. 23, 3295–3303 (2004).

    Article  CAS  Google Scholar 

  73. Simen, P., Balci, F., deSouza, L. Cohen, J. D. & Holmes, P. A model of internal timing by neural integration. J. Neurosci. 31, 9238–9253 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Pfeuty, M., Ragot, R. & Pouthas, V. Relationship between CNV and timing of an upcoming event. Neurosci. Lett. 382, 106–111 (2005).

    Article  CAS  PubMed  Google Scholar 

  75. Praamstra, P. in Attention and Time (eds Nobre, A. C., Coull, J. T.) 331–344 (Oxford Univ. Press, 2010).

    Book  Google Scholar 

  76. Kononowicz, T. W. & Van Rijn, H. Slow potentials in time estimation: the role of temporal accumulation and habituation. Front. Integr. Neurosci. 5, 48 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  77. Van Rijn, H., Kononowicz, T. W., Meck, W. H., Ng, K. K. & Penney, T. B. A critical evaluation of the theoretical interpretations of the contingent negative variation and its relation to time estimation. Front. Integr. Neurosci. 5, 91 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  78. Cui, X., Stetson, C., Montague, P. R. & Eagleman, D. M. Ready...go: amplitude of the fMRI signal encodes expectation of cue arrival time. PLoS Biol. 7, e1000167 (2009).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  79. Wang, X. J. Decision making in recurrent neuronal circuits. Neuron 60, 215–234 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Heekeren, H. R., Marrett, S. & Ungerleider, L. G. The neural systems that mediate human perceptual decision making. Nature Rev. Neurosci. 9, 467–479 (2008).

    Article  CAS  Google Scholar 

  81. Rammsayer, T. Effects of pharmacological induced dopamine-receptor stimulation on human temporal information processing. Neuroquantology 7, 103–113 (2009).

    Article  Google Scholar 

  82. Coull, J. T., Cheng, R.-K. & Meck, W. H. Neuroanatomical and neurochemical substrates of timing. Neuropsychopharmacology 36, 3–25 (2011).

    Article  PubMed  Google Scholar 

  83. Wiener, M., Lohoff, F. W. & Coslett, H. B. Double dissociation of dopamine genes and timing in humans. J. Cogn. Neurosci. 23, 2811–2821 (2011).

    Article  PubMed  Google Scholar 

  84. Reuter, M. et al. The influence of the dopaminergic system on cognitive functioning: a molecular genetic approach. Behav. Brain Res. 164, 93–99 (2005).

    Article  CAS  PubMed  Google Scholar 

  85. Wittmann, M. et al. Effects of psilocybin on time perception and temporal control of behaviour in humans. J. Psychopharmacol. 21, 50–64 (2007).

    Article  CAS  PubMed  Google Scholar 

  86. Wackermann, J., Wittmann, M., Hasler, F. & Vollenweider, F. X. Effects of varied doses of psilocybin on time interval reproduction in human subjects. Neurosci. Lett. 435, 51–55 (2008).

    Article  CAS  PubMed  Google Scholar 

  87. Sysoeva, O. V., Tonevitsky, A. & Wackermann, J. Genetic determinants of time perception mediated by the serotonergic system. PLoS ONE 5, e12650 (2010).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. Craig, A. D. How do you feel? Interoception: the sense of the physiological condition of the body. Nature Rev. Neurosci. 3, 655–666 (2002).

    Article  CAS  Google Scholar 

  89. Critchley, H. D., Wiens, S., Rotshtein, P., Öhman, A. & Dolan, R. J. Neural systems supporting interoceptive awareness. Nature Neurosci. 7, 189–195 (2004).

    Article  CAS  PubMed  Google Scholar 

  90. Singer, T., Critchley, H. D. & Preuschoff, K. A common role of insula in feelings, empathy and uncertainty. Trends Cogn. Sci. 13, 334–340 (2009).

    Article  PubMed  Google Scholar 

  91. Picard, F. & Craig, A. D. Ecstatic epileptic seizures: a potential window on the neural basis of self-awareness. Epilepsy Behav. 16, 539–546 (2009).

    Article  CAS  PubMed  Google Scholar 

  92. Wackermann, J. in Multidisciplinary Aspects of Time and Time Perception (eds Vatakis, A., Esposito, A., Giagkou, M., Cummins, F. & Papadelis, G.) 246–257 (Springer, 2011).

    Book  Google Scholar 

  93. Wackermann, J. & Späti, J. Asymmetry of the discrimination function for temporal durations in human subjects. Acta Neurobiol. Exp. 66, 245–254 (2006).

    Google Scholar 

Download references

Acknowledgements

The author is grateful to J. Wackermann and K. Meissner for comments on earlier versions of the manuscript and wishes to thank the three anonymous reviewers whose criticism and suggestions helped to improve the final version of the paper. Over the years, the author's research has been supported by the Bundesministerium für Bildung und Forschung (Bonn/Berlin), the Else-Kröner-Fresenius Foundation (Bad Homburg), the Max Kade Foundation (New York), the National Institute on Drug Abuse (Bethesda) and the Kavli Institute for Brain and Mind (San Diego). The author has also been supported by the European project COST ISCH Action TD0904 “Time In MEntaL activitY: theoretical, behavioral, bioimaging and clinical perspectives” (TIMELY).

Author information

Authors and Affiliations

Authors

Ethics declarations

Competing interests

The author declares no competing financial interests.

Related links

Related links

FURTHER INFORMATION

Marc Wittmann's homepage

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wittmann, M. The inner sense of time: how the brain creates a representation of duration. Nat Rev Neurosci 14, 217–223 (2013). https://doi.org/10.1038/nrn3452

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrn3452

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing