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The evolution of brain activation during temporal processing

Nature Neuroscience volume 4, pages 317–323 (2001)Cite this article

Abstract

Timing is crucial to many aspects of human performance. To better understand its neural underpinnings, we used event-related fMRI to examine the time course of activation associated with different components of a time perception task. We distinguished systems associated with encoding time intervals from those related to comparing intervals and implementing a response. Activation in the basal ganglia occurred early, and was uniquely associated with encoding time intervals, whereas cerebellar activation unfolded late, suggesting an involvement in processes other than explicit timing. Early cortical activation associated with encoding of time intervals was observed in the right inferior parietal cortex and bilateral premotor cortex, implicating these systems in attention and temporary maintenance of intervals. Late activation in the right dorsolateral prefrontal cortex emerged during comparison of time intervals. Our results illustrate a dynamic network of cortical-subcortical activation associated with different components of temporal information processing.

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Figure 1: Trial events in the time perception (a), pitch perception (b), and control (c) conditions.
Figure 2: Temporal relationship among the trial events, acquisition of images and hypothetical hemodynamic response functions to different task components.
Figure 3: Mean (± standard error of mean) reaction time and percent correct for the time perception (a, b) and the pitch perception (c, d) conditions.
Figure 4: Activation foci in the basal ganglia (a), cerebellum (b), and pre-supplementary motor area/anterior cingulate (c) resulting from subtraction of the control (C) condition from the time (T) and the pitch (P) perception conditions at 2.5, 5.0, 7.5 and 10.0 s after trial onset.
Figure 5: Activation foci in the lateral surface of the left and right hemispheres denote greater activation for the time (T) and the pitch (P) perception conditions relative to the control (C) condition at 2.5, 5.0, 7.5 and 10.0 s after trial onset.
Figure 6: Activation foci in the basal ganglia, insula/frontal operculum and dorsal lateral prefrontal cortex resulting from greater activation for the time (T) relative to the pitch (P) perception conditions at 2.5, 5.0, 7.5 and 10.0 s after trial onset.

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References

  1. Wearden, J. H. “Beyond the fields we know. . .”: Exploring and developing scalar timing theory. Behavioural Processes 45, 3–21 (1999).

    Article  CAS  Google Scholar 

  2. Gibbon, J., Church, R. M. & Meck, W. H. Scalar timing in memory. Ann. NY Acad. Sci. 423, 52–77 (1984).

    Article  CAS  Google Scholar 

  3. Matell, M. S. & Meck, W. H. Neuropsychological mechanisms of interval timing behavior. Bioessays 22, 94–103 (2000).

    Article  CAS  Google Scholar 

  4. Brown, S. W. Time perception and attention: the effects of prospective versus retrospective paradigms and task demands on perceived duration. Percept. Psychophys. 38, 115–124 (1985).

    Article  CAS  Google Scholar 

  5. Zakay, D. & Block, R. A. in Time, Internal Clocks, and Movement (eds. Pastor, M. A. & Artieda, J.) 143–164 (Elsevier Science BV, Amsterdam, 1996).

    Book  Google Scholar 

  6. Baddeley, A. Working Memory (Clarendon/Oxford Univ. Press, Oxford, 1986).

    Google Scholar 

  7. 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  Google Scholar 

  8. Narabayashi, H. & Nakamura, R. in Clinical Neurophysiology of Parkinsonism. (eds. Delwaide, P. J. & Agnoli, A.) 45–57 (Elsevier, New York, 1985).

    Google Scholar 

  9. Manto, M. Pathophysiology of cerebellar dysmetria: the imbalance between the agonist and the antagonist electromyographic activities. Eur. Neurol. 36, 333–337 (1996).

    Article  CAS  Google Scholar 

  10. Artieda, J., Pastor, M. A., Lacruz, F. & Obeso, J. A. Temporal discrimination is abnormal in Parkinson's disease. Brain 115, 199–210 (1992).

    Article  Google Scholar 

  11. Harrington, D. L., Haaland, K. Y. & Hermanowicz, N. Temporal processing in the basal ganglia. Neuropsycholologia 12, 3–12 (1998).

    Article  CAS  Google Scholar 

  12. Maricq, A. V. & Church, R. M. The differential effects of haloperidol and methamphetamine on time estimation in the rat. Psychopharmacology 79, 10–15 (1983).

    Article  CAS  Google Scholar 

  13. Meck, W. H. Affinity for the dopamine D2 receptor predicts neuroleptic potency in decreasing the speed of an internal clock. Pharmacol. Biochem. Behav. 25, 1185–1189 (1986).

    Article  CAS  Google Scholar 

  14. Casini, L. & Ivry, R. Effects of divided attention on temporal processing in patients with lesions of the cerebellum or frontal lobe. Neuropsychologia 13, 10–21 (1999).

    Article  CAS  Google Scholar 

  15. Ivry, R. B., Keele, S. W. & Diener, H. C. Dissociation of the lateral and medial cerebellum in movement timing and movement execution. Exp. Brain Res. 73, 167–180 (1988).

    Article  CAS  Google Scholar 

  16. Ivry, R. B. & Keele, S. W. Timing functions of the cerebellum. J. Cogn. Neurosci. 1, 136–152 (1989).

    Article  CAS  Google Scholar 

  17. Malapani, C., Dubois, B., Rancurel, G. & Gibbon, J. Cerebellar dysfunctions of temporal processing in the seconds range in humans. Neuroreport 9, 3907–3912 (1998).

    Article  CAS  Google Scholar 

  18. Mangels, J. A., Ivry, R. & Shimizu, N. Dissociable contributions of the prefrontal and neocerebellar cortex to time perception. Cogn. Brain Res. 7, 15–39 (1998).

    Article  CAS  Google Scholar 

  19. Goldman-Rakic, P. S. Regional and cellular fractionation of working memory. Proc. Natl. Acad. Sci. USA 93, 13473–13480 (1996).

    Article  CAS  Google Scholar 

  20. Smith, E. & Jonides, J. Storage and executive processes in the frontal lobes. Science 283, 1657–1661 (1999).

    Article  CAS  Google Scholar 

  21. Harrington, D. L., Haaland, K. Y. & Knight, R. T. Cortical networks underlying mechanisms of time perception. J. Neurosci. 18, 1085–1095 (1998).

    Article  CAS  Google Scholar 

  22. Meck, W. H., Church, R. M., Wenk, G. L. & Olton, D. S. Nucleus basalis magnocellularis and medial septal area lesions differentially impair temporal memory. J. Neurosci. 7, 3505–3511 (1987).

    Article  CAS  Google Scholar 

  23. Halsband, U., Ito, N., Tanji, J. & Freund, H. J. The role of premotor cortex and the supplementary motor area in the temporal control of movement in man. Brain 116, 243–266 (1993).

    Article  Google Scholar 

  24. Larsson, J., Gulyas, B. & Roland, P. E. Cortical representation of self-paced finger movement. Neuroreport 7, 463–468 (1996).

    Article  CAS  Google Scholar 

  25. Lejeune, H. et al. The basic pattern of activation in motor and sensory temporal tasks: positron emission tomography data. Neurosci. Lett. 235, 21–24 (1997).

    Article  CAS  Google Scholar 

  26. Penhune, V. B., Zatorre, R. J. & Evans, A. Cerebellar contributions to motor timing: a PET study of auditory and visual rhythm reproduction. J. Cogn. Neurosci. 10, 752–765 (1998).

    Article  CAS  Google Scholar 

  27. Rao, S. M. et al. Distributed neural systems underlying the timing of movements. J. Neurosci. 17, 5528–5535 (1997).

    Article  CAS  Google Scholar 

  28. Jueptner, I. H. et al. Localization of a cerebellar timing process using PET. Neurology 45, 1540–1545 (1995).

    Article  CAS  Google Scholar 

  29. Maquet, P. et al. Brain activation induced by estimation of duration: a PET study. Neuroimage 3, 119–126 (1996).

    Article  CAS  Google Scholar 

  30. O'Boyle, D. J., Freeman, J. S. & Cody, F. W. J. The accuracy and precision of timing of self-paced, repetitive movements in subjects with Parkinson's disease. Brain 119, 51–70 (1996).

    Article  Google Scholar 

  31. Pastor, M. A., Artieda, J., Jahanshahi, M. & Obeso, J. A. Performance of repetitive wrist movements in Parkinson's disease. Brain 115, 875–891 (1992).

    Article  Google Scholar 

  32. Malapani, C. et al. Coupled temporal memories in Parkinson's disease: a dopamine-related dysfunction. J. Cogn. Neurosci. 10, 316–331 (1998).

    Article  CAS  Google Scholar 

  33. Ivry, R. The representation of temporal information in perception and motor control. Curr. Opin. Neurobiol. 6, 851–857 (1996).

    Article  CAS  Google Scholar 

  34. Casini, L. & Macar, F. Effects of attention manipulation on judgments of duration and of intensity in the visual modality. Mem. Cognit. 25, 812–818 (1997).

    Article  CAS  Google Scholar 

  35. Gao, J. H. et al. Cerebellum implicated in sensory acquisition and discrimination rather than motor control. Science 272, 545–547 (1996).

    Article  CAS  Google Scholar 

  36. Desmond, J. E., Gabrieli, J. D. E., Wagner, A. D., Ginier, B. L. & Glover, G. H. Lobular patterns of cerebellar activation in verbal working-memory and finger-tapping tasks as revealed by functional MRI. J. Neurosci. 17, 9675–9685 (1997).

    Article  CAS  Google Scholar 

  37. Schmahmann, J. D. The Cerebellum and Cognition (Academic, New York, 1997).

    Google Scholar 

  38. Bower, J. M. Is the cerebellum sensory for motor's sake, or motor for sensory's sake: the view from the whiskers of a rat? Prog. Brain Res. 114, 463–496 (1997).

    Article  CAS  Google Scholar 

  39. Brodal, P. The ponto-cerebellar projection in the rhesus monkey: an experimental study with retrograde axonal transport of horseradish peroxidase. Neuroscience 4, 193–208 (1979).

    Article  CAS  Google Scholar 

  40. Alexander, G. E., DeLong, M. R. & Strick, P. L. in Annual Review of Neuroscience (ed. Cowan, W. M.) 357–381 (Society for Neuroscience, Washington, DC, 1986).

    Google Scholar 

  41. Brunia, C. & Damen, E. Distribution of slow brain potentials related to motor preparation and stimulus anticipation in a time estimation task. Electroencephalogr. Clin. Neurophysiol. 69, 234–243 (1988).

    Article  CAS  Google Scholar 

  42. Mohl, W. & Pfurtscheller, G. The role of the right parietal region in a movement time estimation task. Neuroreport 2, 309–312 (1991).

    Article  CAS  Google Scholar 

  43. Posner, M. I., Walker, J. A., Friedrich, F. J. & Rafal, R. D. Effects of parietal injury on covert orienting of attention. J. Neurosci. 4, 1863–1874 (1984).

    Article  CAS  Google Scholar 

  44. Cavada, C. & Goldman-Rakic, P. S. Topographic segregation of corticostriatal projections from posterior parietal subdivisions in the macaque monkey. Neuroscience 42, 683–696 (1991).

    Article  CAS  Google Scholar 

  45. Cohen, J. et al. Temporal dynamics of brain activation during a working memory task. Nature 386, 604–607 (1997).

    Article  CAS  Google Scholar 

  46. Awh, E., Smith, E. E. & Jonides, J. Human rehearsal processes and the frontal lobes: PET evidence. Ann. NY Acad. Sci. 769, 97–117 (1995).

    Article  CAS  Google Scholar 

  47. Prabhakaran, V., Narayanan, K., Zhao, Z. & Gabrieli, J. D. E. Integration of diverse information in working memory within the frontal lobe. Nat. Neurosci. 3, 85–90 (2000).

    Article  CAS  Google Scholar 

  48. Cox, R. W. AFNI: Software for analysis and visualization of functional magnetic resonance neuroimages. Comput. Biomed. Res. 29, 162–173 (1996).

    Article  CAS  Google Scholar 

  49. Talairach, J. & Tournoux, P. Co-Planar Stereotaxic Atlas of the Human Brain (Thieme, New York, 1988).

    Google Scholar 

  50. Forman, S. D. et al. Improved assessment of significant activation in functional magnetic resonance imaging (fMRI): use of a cluster-size threshold. Magn. Reson. Med. 33, 636–647 (1995)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This study was funded in part by grants from the Department of Veterans Affairs and National Foundation for Functional Brain Imaging (D.L.H.), the National Institutes of Health (P01 MH51358, R01 MH57836, M01 RR00058) and W.M. Keck Foundation (S.M.R.). We thank R. Cox, E. DeYoe, S. Durgerian, R. Lee, G. Mallory, L. Mead, J. Neitz and B. Ward for their assistance.

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Author notes

  1. Stephen M. Rao and Deborah L. Harrington: These authors contributed equally to this work

Authors and Affiliations

  1. Department of Neurology, Medical College of Wisconsin, Milwaukee, 53226, Wisconsin, USA

    Stephen M. Rao, Andrew R. Mayer & Deborah L. Harrington

  2. Department of Veterans Affairs, Albuquerque, 87108, New Mexico, USA

    Deborah L. Harrington

  3. Department of Neurology, University of New Mexico, Albuquerque, 87113, New Mexico, USA

    Deborah L. Harrington

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  1. Stephen M. Rao
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Correspondence to Deborah L. Harrington.

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Rao, S., Mayer, A. & Harrington, D. The evolution of brain activation during temporal processing. Nat Neurosci 4, 317–323 (2001). https://doi.org/10.1038/85191

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