Skip to main content
Log in

Dynamic Brain Responses Modulated by Precise Timing Prediction in an Opposing Process

  • Original Article
  • Published:
Neuroscience Bulletin Aims and scope Submit manuscript

Abstract

The brain function of prediction is fundamental for human beings to shape perceptions efficiently and successively. Through decades of effort, a valuable brain activation map has been obtained for prediction. However, much less is known about how the brain manages the prediction process over time using traditional neuropsychological paradigms. Here, we implemented an innovative paradigm for timing prediction to precisely study the temporal dynamics of neural oscillations. In the experiment recruiting 45 participants, expectation suppression was found for the overall electroencephalographic activity, consistent with previous hemodynamic studies. Notably, we found that N1 was positively associated with predictability while N2 showed a reversed relation to predictability. Furthermore, the matching prediction had a similar profile with no timing prediction, both showing an almost saturated N1 and an absence of N2. The results indicate that the N1 process showed a ‘sharpening’ effect for predictable inputs, while the N2 process showed a ‘dampening’ effect. Therefore, these two paradoxical neural effects of prediction, which have provoked wide confusion in accounting for expectation suppression, actually co-exist in the procedure of timing prediction but work in separate time windows. These findings strongly support a recently-proposed opposing process theory.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Egner T, Monti JM, Summerfield C. Expectation and surprise determine neural population responses in the ventral visual stream. J Neurosci 2010, 30: 16601–16608.

    CAS  PubMed  PubMed Central  Google Scholar 

  2. Clark A. Whatever next? Predictive brains, situated agents, and the future of cognitive science. Behav Brain Sci 2013, 36: 181–204.

    PubMed  Google Scholar 

  3. de Lange FP, Heilbron M, Kok P. How do expectations shape perception? Trends Cogn Sci 2018, 22: 764–779.

    PubMed  Google Scholar 

  4. Adams RA, Shipp S, Friston KJ. Predictions not commands: active inference in the motor system. Brain Struct Funct 2013, 218: 611–643.

    PubMed  Google Scholar 

  5. Cope TE, Sohoglu E, Sedley W, Patterson K, Jones PS, Wiggins J, et al. Evidence for causal top-down frontal contributions to predictive processes in speech perception. Nat Commun 2017, 8: 2154.

    PubMed  PubMed Central  Google Scholar 

  6. Pine A, Sadeh N, Ben-Yakov A, Dudai Y, Mendelsohn A. Knowledge acquisition is governed by striatal prediction errors. Nat Commun 2018, 9: 1673.

    PubMed  PubMed Central  Google Scholar 

  7. Summerfield C, de Lange FP. Expectation in perceptual decision making: neural and computational mechanisms. Nat Rev Neurosci 2014, 15: 745–756.

    CAS  PubMed  Google Scholar 

  8. Sun H, Ma X, Tang L, Han J, Zhao Y, Xu X, et al. Modulation of beta oscillations for implicit motor timing in primate sensorimotor cortex during movement preparation. Neurosci Bull 2019, 35: 826–840.

    PubMed  PubMed Central  Google Scholar 

  9. Rao RPN, Ballard DHJNN. Predictive coding in the visual cortex: a functional interpretation of some extra-classical receptive-field effects. Nat Neurosci 1999, 2: 79–87.

    CAS  PubMed  Google Scholar 

  10. Friston K. A theory of cortical responses. Philos Trans R Soc Lond B Biol Sci 2005, 360: 815–836.

    PubMed  PubMed Central  Google Scholar 

  11. Friston K. The free-energy principle: a unified brain theory? Nat Rev Neurosci 2010, 11: 127–138.

    CAS  PubMed  Google Scholar 

  12. Alink A, Schwiedrzik CM, Kohler A, Singer W, Muckli L. Stimulus predictability reduces responses in primary visual cortex. J Neurosci 2010, 30: 2960–2966.

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Barne LC, Claessens PME, Reyes MB, Caetano MS, Cravo AM. Low-frequency cortical oscillations are modulated by temporal prediction and temporal error coding. Neuroimage 2017, 146: 40–46.

    PubMed  Google Scholar 

  14. Blank H, Davis MH. Prediction errors but not sharpened signals simulate multivoxel fMRI patterns during speech perception. PLoS Biol 2016, 14: e1002577.

    PubMed  PubMed Central  Google Scholar 

  15. Ullsperger M, Fischer AG, Nigbur R, Endrass T. Neural mechanisms and temporal dynamics of performance monitoring. Trends Cogn Sci 2014, 18: 259–267.

    PubMed  Google Scholar 

  16. Richter D, Ekman M, Lange FPDJJoN. Suppressed sensory response to predictable object stimuli throughout the ventral visual stream. J Neurosci 2018, 38:7452–7461.

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Bueti D, Bahrami B, Walsh V, Rees G. Encoding of temporal probabilities in the human brain. J Neurosci 2010, 30: 4343–4352.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Doherty JR, Rao A, Mesulam MM, Nobre AC. Synergistic effect of combined temporal and spatial expectations on visual attention. J Neurosci 2005, 25: 8259–8266.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. Jaramillo S, Zador AM. The auditory cortex mediates the perceptual effects of acoustic temporal expectation. Nat Neurosci 2011, 14: 246–251.

    CAS  PubMed  Google Scholar 

  20. Kok P, Brouwer GJ, van Gerven MA, de Lange FP. Prior expectations bias sensory representations in visual cortex. J Neurosci 2013, 33: 16275–16284.

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Kouider S, Long B, Le Stanc L, Charron S, Fievet AC, Barbosa LS, et al. Neural dynamics of prediction and surprise in infants. Nat Commun 2015, 6: 8537.

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Kok P, Jehee JF, de Lange FP. Less is more: expectation sharpens representations in the primary visual cortex. Neuron 2012, 75: 265–270.

    CAS  PubMed  Google Scholar 

  23. Kok P, Rahnev D, Jehee JF, Lau HC, de Lange FP. Attention reverses the effect of prediction in silencing sensory signals. Cereb Cortex 2012, 22: 2197–2206.

    PubMed  Google Scholar 

  24. de Gardelle V, Waszczuk M, Egner T, Summerfield C. Concurrent repetition enhancement and suppression responses in extrastriate visual cortex. Cereb Cortex 2013, 23: 2235–2244.

    PubMed  Google Scholar 

  25. de Gardelle V, Stokes M, Johnen VM, Wyart V, Summerfield C. Overlapping multivoxel patterns for two levels of visual expectation. Front Hum Neurosci 2013, 7: 158.

    PubMed  PubMed Central  Google Scholar 

  26. Miller EK, Desimone R. Parallel neuronal mechanisms for short-term memory. Science 1994, 263: 520–522.

    CAS  PubMed  Google Scholar 

  27. Press C, Kok P, Yon D. The perceptual prediction paradox. Trends Cogn Sci 2020, 24: 13–24.

    PubMed  Google Scholar 

  28. Ekman M, Kok P, de Lange FP. Time-compressed preplay of anticipated events in human primary visual cortex. Nat Commun 2017, 8: 15276.

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Kok P, Mostert P, de Lange FP. Prior expectations induce prestimulus sensory templates. Proc Natl Acad Sci U S A 2017, 114: 10473–10478.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Summerfield C, Egner T, Greene M, Koechlin E, Mangels J, Hirsch J. Predictive codes for forthcoming perception in the frontal cortex. Science 2006, 314: 1311–1314.

    CAS  PubMed  Google Scholar 

  31. Bueti D, Lasaponara S, Cercignani M, Macaluso E. Learning about time: plastic changes and interindividual brain differences. Neuron 2012, 75: 725–737.

    CAS  PubMed  Google Scholar 

  32. Arnal LH, Doelling KB, Poeppel D. Delta-beta coupled oscillations underlie temporal prediction accuracy. Cereb Cortex 2015, 25: 3077–3085.

    PubMed  Google Scholar 

  33. Stefanics G, Hangya B, Hernadi I, Winkler I, Lakatos P, Ulbert I. Phase entrainment of human delta oscillations can mediate the effects of expectation on reaction speed. J Neurosci 2010, 30: 13578–13585.

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Summerfield C, Koechlin E. A neural representation of prior information during perceptual inference. Neuron 2008, 59: 336–347.

    CAS  PubMed  Google Scholar 

  35. Calderone DJ, Lakatos P, Butler PD, Castellanos FX. Entrainment of neural oscillations as a modifiable substrate of attention. Trends Cogn Sci 2014, 18: 300–309.

    PubMed  PubMed Central  Google Scholar 

  36. Lakatos P, Karmos G, Mehta AD, Ulbert I, Schroeder CE. Entrainment of neuronal oscillations as a mechanism of attentional selection. Science 2008, 320: 110–113.

    CAS  PubMed  Google Scholar 

  37. Melloni L, Schwiedrzik CM, Muller N, Rodriguez E, Singer W. Expectations change the signatures and timing of electrophysiological correlates of perceptual awareness. J Neurosci 2011, 31: 1386–1396.

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Delorme A, Makeig S. EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis. J Neurosci Methods 2004, 134: 9–21.

    PubMed  Google Scholar 

  39. Folstein JR, Van PCJP. Influence of cognitive control and mismatch on the N2 component of the ERP: a review. Psychophysiology 2008, 45: 152–170.

    PubMed  Google Scholar 

  40. Brunia CHM, Damen EJP. Distribution of slow brain potentials related to motor preparation and stimulus anticipation in a time estimation task. Electroencephalogr Clin Neurophysiol 1988, 69: 234–243.

    CAS  PubMed  Google Scholar 

  41. Luck SJ, Kappenman ES (Eds). The Oxford Handbook of Event-Related Potential Components. Oxford Library of Psychology 2008.

  42. Stahl J, Gibbons HJP. The application of jackknife-based onset detection of lateralized readiness potential in correlative approaches. Psychophysiology 2004, 41: 845–860.

    PubMed  Google Scholar 

  43. Miller J, Patterson AT, Ulrichb R. Jackknife-based method for measuring LRP onset latency differences. Psychophysiology 1998, 35: 99–115.

    CAS  PubMed  Google Scholar 

  44. Summerfield C, Egner T. Expectation (and attention) in visual cognition. Trends Cogn Sci 2009, 13: 403–409.

    PubMed  Google Scholar 

  45. Nobre AC, van Ede F. Anticipated moments: temporal structure in attention. Nat Rev Neurosci 2018, 19: 34–48.

    CAS  PubMed  Google Scholar 

  46. Buhusi CV, Meck WH. What makes us tick? Functional and neural mechanisms of interval timing. Nat Rev Neurosci 2005, 6: 755–765.

    CAS  PubMed  Google Scholar 

  47. Hillyard SA, Anllo-Vento L. Event-related brain potentials in the study of visual selective attention. Proc Natl Acad Sci U S A 1998, 95: 781–787.

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Stormer VS, McDonald JJ, Hillyard SA. Cross-modal cueing of attention alters appearance and early cortical processing of visual stimuli. Proc Natl Acad Sci U S A 2009, 106: 22456–22461.

    PubMed  PubMed Central  Google Scholar 

  49. Arnal LH, Giraud AL. Cortical oscillations and sensory predictions. Trends Cogn Sci 2012, 16: 390–398.

    PubMed  Google Scholar 

  50. Capilla A, Schoffelen JM, Paterson G, Thut G, Gross J. Dissociated alpha-band modulations in the dorsal and ventral visual pathways in visuospatial attention and perception. Cereb Cortex 2014, 24: 550–561.

    PubMed  Google Scholar 

  51. Klimesch W. alpha-band oscillations, attention, and controlled access to stored information. Trends Cogn Sci 2012, 16: 606–617.

    PubMed  PubMed Central  Google Scholar 

  52. Cravo AM, Rohenkohl G, Wyart V, Nobre AC. Endogenous modulation of low frequency oscillations by temporal expectations. J Neurophysiol 2011, 106: 2964–2972.

    PubMed  PubMed Central  Google Scholar 

  53. van Rijn H, Kononowicz TW, Meck WH, Ng KK, Penney TB. Contingent negative variation and its relation to time estimation: a theoretical evaluation. Front Integr Neurosci 2011, 5: 91.

    PubMed  PubMed Central  Google Scholar 

  54. Kononowicz TW, van Rijn H. Decoupling interval timing and climbing neural activity: a dissociation between CNV and N1P2 amplitudes. J Neurosci 2014, 34: 2931–2939.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Ni B, Wu R, Yu T, Zhu H, Li Y, Liu Z. Role of the hippocampus in distinct memory traces: timing of match and mismatch enhancement revealed by intracranial recording. Neurosci Bull 2017, 33: 664–674.

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Mangun GR, Hillyard SA. Modulations of sensory-evoked brain potentials indicate changes in perceptual processing during visual-spatial priming. J Exp Psychol Hum Percept Perform 1991, 17: 1057–1074.

    CAS  PubMed  Google Scholar 

  57. Summerfield C, Trittschuh EH, Monti JM, Mesulam MM, Egner T. Neural repetition suppression reflects fulfilled perceptual expectations. Nat Neurosci 2008, 11: 1004–1006.

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Chalk M, Marre O, Tkacik G. Toward a unified theory of efficient, predictive, and sparse coding. Proc Natl Acad Sci U S A 2018, 115: 186–191.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Key Research and Development Program of China (2017YFB1300302), the National Natural Science Foundation of China (81925020 and 61976152), and the Young Elite Scientist Sponsorship Program of the China Association for Science and Technology (2018QNRC001).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Dong Ming.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 399 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, M., Meng, J., Yu, H. et al. Dynamic Brain Responses Modulated by Precise Timing Prediction in an Opposing Process. Neurosci. Bull. 37, 70–80 (2021). https://doi.org/10.1007/s12264-020-00527-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12264-020-00527-1

Keywords

Navigation