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.

  • Article
  • Published:

Engaging in an auditory task suppresses responses in auditory cortex

Abstract

Although systems that are involved in attentional selection have been studied extensively, much less is known about nonselective systems. To study these preparatory mechanisms, we compared activity in auditory cortex that was elicited by sounds while rats performed an auditory task ('engaged') with activity that was elicited by identical stimuli while subjects were awake but not performing a task ('passive'). We found that engagement suppressed responses, an effect that was opposite in sign to that elicited by selective attention. In the auditory thalamus, however, engagement enhanced spontaneous firing rates but did not affect evoked responses. These results indicate that neural activity in auditory cortex cannot be viewed simply as a limited resource that is allocated in greater measure as the state of the animal passes from somnolent to passively listening to engaged and attentive. Instead, the engaged condition possesses a characteristic and distinct neural signature in which sound-evoked responses are paradoxically suppressed.

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: Cortical evoked responses are suppressed in the engaged condition, but spontaneous activity is unchanged.
Figure 2: Decision-relevant target is suppressed in engaged condition.
Figure 3: Evoked auditory responses are not suppressed during an auditory task relative to an olfactory task.
Figure 4: Changes in arousal and anesthesia have distinct neural signatures.
Figure 5: Suppression of evoked responses is not caused by self-triggering of stimulus.
Figure 6: Neural correlate of engagement differs in auditory thalamus.

Similar content being viewed by others

References

  1. Steriade, M., Timofeev, I. & Grenier, F. Natural waking and sleep states: a view from inside neocortical neurons. J. Neurophysiol. 85, 1969–1985 (2001).

    Article  CAS  PubMed  Google Scholar 

  2. Edeline, J.M., Dutrieux, G., Manunta, Y. & Hennevin, E. Diversity of receptive field changes in auditory cortex during natural sleep. Eur. J. Neurosci. 14, 1865–1880 (2001).

    Article  CAS  PubMed  Google Scholar 

  3. Talwar, S.K. & Gerstein, G.L. Reorganization in awake rat auditory cortex by local microstimulation and its effect on frequency-discrimination behavior. J. Neurophysiol. 86, 1555–1572 (2001).

    Article  CAS  PubMed  Google Scholar 

  4. Castro-Alamancos, M.A. Dynamics of sensory thalamocortical synaptic networks during information processing states. Prog. Neurobiol. 74, 213–247 (2004).

    Article  PubMed  Google Scholar 

  5. Moran, J. & Desimone, R. Selective attention gates visual processing in the extrastriate cortex. Science 229, 782–784 (1985).

    Article  CAS  PubMed  Google Scholar 

  6. Desimone, R. & Duncan, J. Neural mechanisms of selective visual attention. Annu. Rev. Neurosci. 18, 193–222 (1995).

    Article  CAS  PubMed  Google Scholar 

  7. Maunsell, J.H. & Cook, E.P. The role of attention in visual processing. Phil. Trans. R. Soc. Lond. B 357, 1063–1072 (2002).

    Article  Google Scholar 

  8. 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  PubMed  Google Scholar 

  9. Fritz, J.B., Elhilali, M., David, S.V. & Shamma, S.A. Does attention play a role in dynamic receptive field adaptation to changing acoustic salience in A1? Hear. Res. 229, 186–203 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  11. Raz, A. & Buhle, J. Typologies of attentional networks. Nat. Rev. Neurosci. 7, 367–379 (2006).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  13. Yang, Y., DeWeese, M.R., Otazu, G.H. & Zador, A.M. Millisecond-scale differences in neural activity in auditory cortex can drive decisions. Nat. Neurosci. 11, 1262–1263 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Kilgard, M.P. & Merzenich, M.M. Plasticity of temporal information processing in the primary auditory cortex. Nat. Neurosci. 1, 727–731 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  16. Hubel, D.H., Henson, C.O., Rupert, A. & Galambos, R. “Attention” units in the auditory cortex. Science 129, 1279–1280 (1959).

    Article  CAS  PubMed  Google Scholar 

  17. Picton, T.W., Hillyard, S.A., Galambos, R. & Schiff, M. Human auditory attention: a central or peripheral process? Science 173, 351–353 (1971).

    Article  CAS  PubMed  Google Scholar 

  18. Fritz, J.B., Elhilali, M. & Shamma, S.A. Adaptive changes in cortical receptive fields induced by attention to complex sounds. J. Neurophysiol. 98, 2337–2346 (2007).

    Article  PubMed  Google Scholar 

  19. Scott, B.H., Malone, B.J. & Semple, M.N. Effect of behavioral context on representation of a spatial cue in core auditory cortex of awake macaques. J. Neurosci. 27, 6489–6499 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Hocherman, S., Benson, D.A., Goldstein, M.H. Jr., Heffner, H.E. & Hienz, R.D. Evoked unit activity in auditory cortex of monkeys performing a selective attention task. Brain Res. 117, 51–68 (1976).

    Article  CAS  PubMed  Google Scholar 

  21. Spitzer, H., Desimone, R. & Moran, J. Increased attention enhances both behavioral and neuronal performance. Science 240, 338–340 (1988).

    Article  CAS  PubMed  Google Scholar 

  22. Tai, L.H. & Zador, A. Neural Mechanisms of Selective Auditory Attention in Rats. PhD Thesis. Stony Brook Univ. 〈http://dx.doi.org/10.1038/npre.2008.2355.1〉 (2008).

    Book  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  24. Castro-Alamancos, M.A. & Oldford, E. Cortical sensory suppression during arousal is due to the activity-dependent depression of thalamocortical synapses. J. Physiol. (Lond.) 541, 319–331 (2002).

    Article  CAS  Google Scholar 

  25. Müller-Preuss, P. & Ploog, D. Inhibition of auditory cortical neurons during phonation. Brain Res. 215, 61–76 (1981).

    Article  PubMed  Google Scholar 

  26. Eliades, S.J. & Wang, X. Neural substrates of vocalization feedback monitoring in primate auditory cortex. Nature 453, 1102–1106 (2008).

    Article  CAS  PubMed  Google Scholar 

  27. Martikainen, M.H., Kaneko, K. & Hari, R. Suppressed responses to self-triggered sounds in the human auditory cortex. Cereb. Cortex 15, 299–302 (2005).

    Article  PubMed  Google Scholar 

  28. Boly, M. et al. Baseline brain activity fluctuations predict somatosensory perception in humans. Proc. Natl. Acad. Sci. USA 104, 12187–12192 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Reinagel, P., Godwin, D., Sherman, S.M. & Koch, C. Encoding of visual information by LGN bursts. J. Neurophysiol. 81, 2558–2569 (1999).

    Article  CAS  PubMed  Google Scholar 

  30. Sherman, S.M. Thalamic relays and cortical functioning. Prog. Brain Res. 149, 107–126 (2005).

    Article  PubMed  Google Scholar 

  31. Swadlow, H.A. & Gusev, A.G. The impact of 'bursting' thalamic impulses at a neocortical synapse. Nat. Neurosci. 4, 402–408 (2001).

    Article  CAS  PubMed  Google Scholar 

  32. Massaux, A., Dutrieux, G., Cotillon-Williams, N., Manunta, Y. & Edeline, J.M. Auditory thalamus bursts in anesthetized and non-anesthetized states: contribution to functional properties. J. Neurophysiol. 91, 2117–2134 (2004).

    Article  CAS  PubMed  Google Scholar 

  33. Poulet, J.F. & Petersen, C.C. Internal brain state regulates membrane potential synchrony in barrel cortex of behaving mice. Nature 454, 881–885 (2008).

    Article  CAS  PubMed  Google Scholar 

  34. Deweese, M.R. & Zador, A.M. Shared and private variability in the auditory cortex. J. Neurophysiol. 92, 1840–1855 (2004).

    Article  PubMed  Google Scholar 

  35. Chung, S., Li, X. & Nelson, S. Short-term depression at thalamocortical synapses contributes to rapid adaptation of cortical sensory responses in vivo. Neuron 34, 437–446 (2002).

    Article  CAS  PubMed  Google Scholar 

  36. Abbott, L.F., Varela, J.A., Sen, K. & Nelson, S.B. Synaptic depression and cortical gain control. Science 275, 220–224 (1997).

    Article  CAS  PubMed  Google Scholar 

  37. Crochet, S. & Petersen, C.C. Correlating whisker behavior with membrane potential in barrel cortex of awake mice. Nat. Neurosci. 9, 608–610 (2006).

    Article  CAS  PubMed  Google Scholar 

  38. Ferezou, I., Bolea, S. & Petersen, C.C. Visualizing the cortical representation of whisker touch: voltage-sensitive dye imaging in freely moving mice. Neuron 50, 617–629 (2006).

    Article  CAS  PubMed  Google Scholar 

  39. Fanselow, E.E. & Nicolelis, M.A. Behavioral modulation of tactile responses in the rat somatosensory system. J. Neurosci. 19, 7603–7616 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Castro-Alamancos, M.A. Role of thalamocortical sensory suppression during arousal: focusing sensory inputs in neocortex. J. Neurosci. 22, 9651–9655 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Castro-Alamancos, M.A. Absence of rapid sensory adaptation in neocortex during information processing states. Neuron 41, 455–464 (2004).

    Article  CAS  PubMed  Google Scholar 

  42. Hirata, A. & Castro-Alamancos, M.A. Relief of synaptic depression produces long-term enhancement in thalamocortical networks. J. Neurophysiol. 95, 2479–2491 (2006).

    Article  PubMed  Google Scholar 

  43. Kawai, H., Lazar, R. & Metherate, R. Nicotinic control of axon excitability regulates thalamocortical transmission. Nat. Neurosci. 10, 1168–1175 (2007).

    Article  CAS  PubMed  Google Scholar 

  44. Reynolds, J.H., Chelazzi, L. & Desimone, R. Competitive mechanisms subserve attention in macaque areas V2 and V4. J. Neurosci. 19, 1736–1753 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Cook, E.P. & Maunsell, J.H. Dynamics of neuronal responses in macaque MT and VIP during motion detection. Nat. Neurosci. 5, 985–994 (2002).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  47. Hromádka, T. Representation of Sounds in Auditory Cortex of Awake Rats. PhD Thesis.Cold Spring Harbor Laboratory 〈http://dx.doi.org/10.1038/npre.2008.2464.1〉 (2008).

    Book  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  49. Schmitzer-Torbert, N., Jackson, J., Henze, D., Harris, K. & Redish, A.D. Quantitative measures of cluster quality for use in extracellular recordings. Neuroscience 131, 1–11 (2005).

    Article  CAS  PubMed  Google Scholar 

  50. Feierstein, C.E., Quirk, M.C., Uchida, N., Sosulski, D.L. & Mainen, Z.F. Representation of spatial goals in rat orbitofrontal cortex. Neuron 51, 495–507 (2006).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the US National Institutes of Health, the Swartz Foundation, the Marie Robertson Fund, the Louis Morin Charitable Trust and the Coleman Fung Foundation.

Author information

Authors and Affiliations

Authors

Contributions

G.H.O. and A.M.Z. designed the overall experiments and wrote the manuscript. G.H.O. designed and performed the experiments in Figures 1, 2, 4 and 6. L.-H.T. designed and performed the experiments in Figure 3 (intermodal attention). Y.Y. designed and performed the experiments in Figure 4 (head-fixed behavior).

Corresponding author

Correspondence to Anthony M Zador.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–8, Supplementary Table 1, Supplementary Methods, Supplementary Analysis, Supplementary Data and Supplementary Model (PDF 546 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Otazu, G., Tai, LH., Yang, Y. et al. Engaging in an auditory task suppresses responses in auditory cortex. Nat Neurosci 12, 646–654 (2009). https://doi.org/10.1038/nn.2306

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2306

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