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The auditory cortex mediates the perceptual effects of acoustic temporal expectation

Abstract

When events occur at predictable instants, anticipation improves performance. Knowledge of event timing modulates motor circuits and thereby improves response speed. By contrast, the neuronal mechanisms that underlie changes in sensory perception resulting from expectation are not well understood. We developed a behavioral procedure for rats in which we manipulated expectations about sound timing. Valid expectations improved both the speed and the accuracy of the subjects' performance, indicating not only improved motor preparedness but also enhanced perception. Single-neuron recordings in primary auditory cortex showed enhanced representation of sounds during periods of heightened expectation. Furthermore, we found that activity in auditory cortex was causally linked to the performance of the task and that changes in the neuronal representation of sounds predicted performance on a trial-by-trial basis. Our results indicate that changes in neuronal representation as early as primary sensory cortex mediate the perceptual advantage conferred by temporal expectation.

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Figure 1: Task and manipulation of temporal expectation.
Figure 2: Valid temporal expectation improved performance.
Figure 3: Inactivation of auditory cortex decreased performance.
Figure 4: Temporal expectation modulated neuronal activity in the auditory cortex.
Figure 5: Modulation of neuronal activity was specific to driven activity.
Figure 6: Neuronal response increased as the expected moment of the target approached.
Figure 7: Neuronal activity in auditory cortex was correlated with behavioral performance.

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References

  1. Nobre, A., Correa, A. & Coull, J. The hazards of time. Curr. Opin. Neurobiol. 17, 465–470 (2007).

    Article  CAS  Google Scholar 

  2. Winkler, I., Denham, S.L. & Nelken, I. Modeling the auditory scene: predictive regularity representations and perceptual objects. Trends Cogn. Sci. 13, 532–540 (2009).

    Article  Google Scholar 

  3. Ulanovsky, N., Las, L. & Nelken, I. Processing of low-probability sounds by cortical neurons. Nat. Neurosci. 6, 391–398 (2003).

    Article  CAS  Google Scholar 

  4. Fritz, J., Shamma, S., Elhilali, M. & Klein, D. Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex. Nat. Neurosci. 6, 1216–1223 (2003).

    Article  CAS  Google Scholar 

  5. Lange, K., Rosler, F. & Roder, B. Early processing stages are modulated when auditory stimuli are presented at an attended moment in time: an event-related potential study. Psychophysiology 40, 806–817 (2003).

    Article  Google Scholar 

  6. Nobre, A.C. Orienting attention to instants in time. Neuropsychologia 39, 1317–1328 (2001).

    Article  CAS  Google Scholar 

  7. Ohl, F.W., Wetzel, W., Wagner, T., Rech, A. & Scheich, H. Bilateral ablation of auditory cortex in mongolian gerbil affects discrimination of frequency modulated tones but not of pure tones. Learn. Mem. 6, 347–362 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Syka, J., Rybalko, N., Mazelová, J. & Druga, R. Gap detection threshold in the rat before and after auditory cortex ablation. Hear. Res. 172, 151–159 (2002).

    Article  CAS  Google Scholar 

  9. Newsome, W.T. & Paré, E. A selective impairment of motion perception following lesions of the middle temporal visual area (MT). J. Neurosci. 8, 2201–2211 (1988).

    Article  CAS  Google Scholar 

  10. Talwar, S.K., Musial, P.G. & Gerstein, G.L. Role of mammalian auditory cortex in the perception of elementary sound properties. J. Neurophysiol. 85, 2350–2358 (2001).

    Article  CAS  Google Scholar 

  11. Tai, L. & Zador, A. Neural mechanisms of selective auditory attention in rats (Dissertation). Nature Precedings <http://dx.doi.org/10.1038/npre.2008.2355.1> (2008).

  12. Otazu, G.H., Tai, L., Yang, Y. & Zador, A.M. Engaging in an auditory task suppresses responses in auditory cortex. Nat. Neurosci. 12, 646–654 (2009).

    Article  CAS  Google Scholar 

  13. Bar-Yosef, O., Rotman, Y. & Nelken, I. Responses of neurons in cat primary auditory cortex to bird chirps: effects of temporal and spectral context. J. Neurosci. 22, 8619–8632 (2002).

    Article  CAS  Google Scholar 

  14. Asari, H. & Zador, A.M. Long-lasting context dependence constrains neural encoding models in rodent auditory cortex. J. Neurophysiol. 102, 2638–2656 (2009).

    Article  Google Scholar 

  15. Hromádka, T., DeWeese, M.R. & Zador, A.M. Sparse representation of sounds in the unanesthetized auditory cortex. PLoS Biol. 6, e16 (2008).

    Article  Google Scholar 

  16. Wang, X., Lu, T., Snider, R.K. & Liang, L. Sustained firing in auditory cortex evoked by preferred stimuli. Nature 435, 341–346 (2005).

    Article  CAS  Google Scholar 

  17. Brosch, M. & Schreiner, C.E. Time course of forward masking tuning curves in cat primary auditory cortex. J. Neurophysiol. 77, 923–943 (1997).

    Article  CAS  Google Scholar 

  18. Wehr, M. & Zador, A.M. Synaptic mechanisms of forward suppression in rat auditory cortex. Neuron 47, 437–445 (2005).

    Article  CAS  Google Scholar 

  19. Shannon, C.E. A mathematical theory of communication. Bell Syst. Tech. J. 27, 379–423, 623–656 (1948).

    Article  Google Scholar 

  20. Haykin, S. Adaptive Filter Theory 4th edn. (Prentice Hall, 2001).

  21. Rieke, F., Warland, D., de Ruyter Van Steveninck, R. & Bialek, W. Spikes: Exploring the Neural Code (MIT Press, 1996).

  22. Smirnakis, S.M., Berry, M.J., Warland, D.K., Bialek, W. & Meister, M. Adaptation of retinal processing to image contrast and spatial scale. Nature 386, 69–73 (1997).

    Article  CAS  Google Scholar 

  23. Niemi, P. & Näätänen, R. Foreperiod and simple reaction time. Psychol. Bull. 89, 133–162 (1981).

    Article  Google Scholar 

  24. Correa, Á., Lupiáñez, J. & Tudela, P. Attentional preparation based on temporal expectancy modulates processing at the perceptual level. Psychon. Bull. Rev. 12, 328–334 (2005).

    Article  Google Scholar 

  25. Kilgard, M.P. & Merzenich, M.M. Cortical map reorganization enabled by nucleus basalis activity. Science 279, 1714–1718 (1998).

    Article  CAS  Google Scholar 

  26. Tremblay, L. & Schultz, W. Relative reward preference in primate orbitofrontal cortex. Nature 398, 704–708 (1999).

    Article  CAS  Google Scholar 

  27. Rao, S.M., Mayer, A.R. & Harrington, D.L. The evolution of brain activation during temporal processing. Nat. Neurosci. 4, 317–323 (2001).

    Article  CAS  Google Scholar 

  28. Ghose, G.M. & Maunsell, J.H.R. Attentional modulation in visual cortex depends on task timing. Nature 419, 616–620 (2002).

    Article  CAS  Google Scholar 

  29. Anderson, B. & Sheinberg, D.L. Effects of temporal context and temporal expectancy on neural activity in inferior temporal cortex. Neuropsychologia 46, 947–957 (2008).

    Article  Google Scholar 

  30. Shuler, M.G. & Bear, M.F. Reward timing in the primary visual cortex. Science 311, 1606–1609 (2006).

    Article  CAS  Google Scholar 

  31. Treue, S. & Trujillo, J.C.M. Feature-based attention influences motion processing gain in macaque visual cortex. Nature 399, 575–579 (1999).

    Article  CAS  Google Scholar 

  32. McAdams, C.J. & Maunsell, J.H. Effects of attention on orientation-tuning functions of single neurons in macaque cortical area v4. J. Neurosci. 19, 431–441 (1999).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  34. Britten, K.H., Newsome, W.T., Shadlen, M.N., Celebrini, S. & Movshon, J.A. A relationship between behavioral choice and the visual responses of neurons in macaque MT. Vis. Neurosci. 13, 87–100 (1996).

    Article  CAS  Google Scholar 

  35. Correa, Á., Lupiáñez, J., Madrid, E. & Tudela, P. Temporal attention enhances early visual processing: a review and new evidence from event-related potentials. Brain Res. 1076, 116–128 (2006).

    Article  CAS  Google Scholar 

  36. Uchida, N. & Mainen, Z.F. Speed and accuracy of olfactory discrimination in the rat. Nat. Neurosci. 6, 1224–1229 (2003).

    Article  CAS  Google Scholar 

  37. Paxinos, G. & Watson, C. The Rat Brain in Stereotaxic Coordinates 5th edn. (Academic, 2005).

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Acknowledgements

We thank G.H. Otazu, A.E. Baker, J.M. Abolafia and B.J. Burbach for assistance with preliminary studies. This research was supported by a postdoctoral fellowship from the Swartz Foundation and by grants from the Swartz Foundation, the US National Institutes of Health and the Marie Robertson Fund.

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Authors

Contributions

S.J. and A.M.Z. designed the project and wrote the manuscript. S.J. collected the data and performed the analyses.

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Correspondence to Anthony M Zador.

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The authors declare no competing financial interests.

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Supplementary Figures 1–14 and Supplementary Equations 1–3 (PDF 508 kb)

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Jaramillo, S., Zador, A. The auditory cortex mediates the perceptual effects of acoustic temporal expectation. Nat Neurosci 14, 246–251 (2011). https://doi.org/10.1038/nn.2688

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