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:

Change detection by thalamic reticular neurons

Abstract

The thalamic reticular nucleus (TRN) is thought to function in the attentional searchlight. We analyzed the detection of deviant acoustic stimuli by TRN neurons and the consequences of deviance detection on the TRN target, the medial geniculate body (MGB) of the rat. TRN neurons responded more strongly to pure-tone stimuli presented as deviant stimuli (low appearance probability) than those presented as standard stimuli (high probability) (deviance-detection index = 0.321). MGB neurons also showed deviance detection in this procedure, albeit to a smaller extent (deviance-detection index = 0.154). TRN neuron deviance detection either enhanced (14 neurons) or suppressed (27 neurons) MGB neuronal responses to a probe stimulus. Both effects were neutralized by inactivation of the auditory TRN. Deviance modulation effects were cross-modal. Deviance detection probably causes TRN neurons to transiently deactivate surrounding TRN neurons in response to a fresh stimulus, altering auditory thalamus responses and inducing attention shift.

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: Responses of a TRN neuron to pure-tone stimuli of two frequencies presented in an oddball procedure.
Figure 2: Differential responses of TRN neurons to pure-tone stimuli of two frequencies presented in an oddball procedure.
Figure 3: Differential responses of MGB neurons to pure-tone stimuli presented in an oddball procedure.
Figure 4: Deviance preferences of TRN and MGB neurons.
Figure 5: Effect of the deviant-stimulus procedure on MGB neuronal responses to a probe stimulus.
Figure 6: Effect of TRN inactivation on modulation of MGB neuronal responses by deviant procedures.
Figure 7: Effect of a preceding light stimulus on MGB neuronal responses to sound stimuli.

Similar content being viewed by others

References

  1. Jones, E.G. Some aspects of the organization of the thalamic reticular complex. J. Comp. Neurol. 162, 285–308 (1975).

    Article  CAS  Google Scholar 

  2. Steriade, M., Jones, E.G. & McCormick, D.A. Thalamus: Organization and Function (Elsevier Science, Oxford, 1997).

  3. Yen, C.T., Conley, M., Hendry, S.H. & Jones, E.G. The morphology of physiologically identified GABAergic neurons in the somatic sensory part of the thalamic reticular nucleus in the cat. J. Neurosci. 5, 2254–2268 (1985).

    Article  CAS  Google Scholar 

  4. Houser, C.R., Vaughn, J.E., Barber, R.P. & Roberts, E. GABA neurons are the major cell type of the nucleus reticularis thalami. Brain Res. 200, 341–354 (1980).

    Article  CAS  Google Scholar 

  5. Deschênes, M., Madariaga-Domich, A. & Steriade, M. Dendrodendritic synapses in the cat reticularis thalami nucleus: a structural basis for thalamic spindle synchronization. Brain Res. 334, 165–168 (1985).

    Article  Google Scholar 

  6. Steriade, M. & Deschênes, M. The thalamus as a neuronal oscillator. Brain Res. 320, 1–63 (1984).

    Article  CAS  Google Scholar 

  7. Bal, T. & McCormick, D.A. Mechanisms of oscillatory activity in guinea-pig nucleus reticularis thalami in vitro: a mammalian pacemaker. J. Physiol. (Lond.) 468, 669–691 (1993).

    Article  CAS  Google Scholar 

  8. McCormick, D.A. & Prince, D.A. Acetylcholine induces burst firing in thalamic reticular neurones by activating a potassium conductance. Nature 319, 402–405 (1986).

    Article  CAS  Google Scholar 

  9. Crick, F. Function of the thalamic reticular complex: the searchlight hypothesis. Proc. Natl. Acad. Sci. USA 81, 4586–4590 (1984).

    Article  CAS  Google Scholar 

  10. Llinás, R. & Paré, D. in Thalamus (eds. Steriade M., Jones E.G. & McCormick D.A.) 501–516 (Plenum, New York, 1997).

    Google Scholar 

  11. Shosaku, A. & Sumitomo, I. Auditory neurons in the rat thalamic reticular nucleus. Exp. Brain Res. 49, 432–442 (1983).

    Article  CAS  Google Scholar 

  12. Simm, G.M., de Ribaupierre, F., de Ribaupierre, Y. & Rouiller, E.M. Discharge properties of single units in auditory part of reticular nucleus of thalamus in cat. J. Neurophysiol. 63, 1010–1021 (1990).

    Article  CAS  Google Scholar 

  13. Malone, B.J. & Semple, M.N. Effects of auditory stimulus context on the representation of frequency in the gerbil inferior colliculus. J. Neurophysiol. 86, 1113–1130 (2001).

    Article  CAS  Google Scholar 

  14. Pérez-González, D., Malmierca, M.S. & Covey, E. Novelty detector neurons in the mammalian auditory midbrain. Eur. J. Neurosci. 22, 2879–2885 (2005).

    Article  Google Scholar 

  15. Yu, X.-J., Xu, X.-X., Chen, X., He, S.-G. & He, J. Slow recovery from excitation of thalamic reticular nucleus neurons. J. Neurophysiol. 101, 980–987 (2009).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  17. Zhang, Z. et al. Corticofugal projection inhibits the auditory thalamus through the thalamic reticular nucleus. J. Neurophysiol. 99, 2938–2945 (2008).

    Article  Google Scholar 

  18. He, J., Yu, Y.Q., Xiong, Y., Hashikawa, T. & Chan, Y.S. Modulatory effect of cortical activation on the lemniscal auditory thalamus of the Guinea pig. J. Neurophysiol. 88, 1040–1050 (2002).

    Article  Google Scholar 

  19. Landisman, C.E. et al. Electrical synapses in the thalamic reticular nucleus. J. Neurosci. 22, 1002–1009 (2002).

    Article  CAS  Google Scholar 

  20. Long, M.A., Landisman, C.E. & Connors, B.W. Small clusters of electrically coupled neurons generate synchronous rhythms in the thalamic reticular nucleus. J. Neurosci. 24, 341–349 (2004).

    Article  CAS  Google Scholar 

  21. Warren, R.A., Agmon, A. & Jones, E.G. Oscillatory synaptic interactions between ventroposterior and reticular neurons in mouse thalamus in vitro. J. Neurophysiol. 72, 1993–2003 (1994).

    Article  CAS  Google Scholar 

  22. Zikopoulos, B. & Barbas, H. Prefrontal projections to the thalamic reticular nucleus form a unique circuit for attentional mechanisms. J. Neurosci. 26, 7348–7361 (2006).

    Article  CAS  Google Scholar 

  23. Knight, R. Contribution of human hippocampal region to novelty detection. Nature 383, 256–259 (1996).

    Article  CAS  Google Scholar 

  24. Tiitinen, H., May, P., Reinikainen, K. & Náátánen, R. Attentive novelty detection in humans is governed by pre-attentive sensory memory. Nature 372, 90–92 (1994).

    Article  CAS  Google Scholar 

  25. Carpenter, G.A. & Grossberg, S. Normal and amnesic learning, recognition and memory by a neural model of cortico-hippocampal interactions. Trends Neurosci. 16, 131–137 (1993).

    Article  CAS  Google Scholar 

  26. Mühlau, M. et al. Structural brain changes in tinnitus. Cereb. Cortex 16, 1283–1288 (2006).

    Article  Google Scholar 

  27. Llinás, R.R. & Paré, D. Of dreaming and wakefulness. Neuroscience 44, 521–535 (1991).

    Article  Google Scholar 

  28. Crabtree, J.W. & Isaac, J.T. New intrathalamic pathways allowing modality-related and cross-modality switching in the dorsal thalamus. J. Neurosci. 22, 8754–8761 (2002).

    Article  CAS  Google Scholar 

  29. Jahnsen, H. & Llinás, R. Electrophysiological properties of guinea-pig thalamic neurones: an in vitro study. J. Physiol. (Lond.) 349, 205–226 (1984).

    Article  CAS  Google Scholar 

  30. Jahnsen, H. & Llinás, R. Ionic basis for the electro-responsiveness and oscillatory properties of guinea-pig thalamic neurones in vitro. J. Physiol. (Lond.) 349, 227–247 (1984).

    Article  CAS  Google Scholar 

  31. Sherman, S.M. A wake-up call from the thalamus. Nat. Neurosci. 4, 344–346 (2001).

    Article  CAS  Google Scholar 

  32. Guillery, R.W. & Sherman, S.M. Thalamic relay functions and their role in corticocortical communication: generalizations from the visual system. Neuron 33, 163–175 (2002).

    Article  CAS  Google Scholar 

  33. He, J. On and off pathways segregated at the auditory thalamus of the guinea pig. J. Neurosci. 21, 8672–8679 (2001).

    Article  CAS  Google Scholar 

  34. Guo, Y.P. et al. Corticothalamic synchronization leads to c-fos expression in the auditory thalamus. Proc. Natl. Acad. Sci. USA 104, 11802–11807 (2007).

    Article  CAS  Google Scholar 

  35. Xiong, Y., Yu, Y.Q., Chan, Y.S. & He, J. Effects of cortical stimulation on auditory-responsive thalamic neurones in anaesthetized guinea pigs. J. Physiol. (Lond.) 560, 207–217 (2004).

    Article  CAS  Google Scholar 

  36. Paxinos, G. & Watson, C. The Rat Brain in Stereotaxic Coordinates (Elsevier Academic Press, Amsterdam, 2005).

    Google Scholar 

Download references

Acknowledgements

The authors thank A. Palmer and M. Wallace for their critical readings and comments. This work was supported by the Natural Science Foundation of China (Overseas Cooperation Fund) and the Hong Kong Grants Council (PolyU 5412/06M).

Author information

Authors and Affiliations

Authors

Contributions

X.-J.Y., S.H. and J.H. designed the experiments. X.-J.Y. and X.-X.X. performed the experiments. X.-J.Y. and J.H. analyzed the results and wrote the manuscript.

Corresponding authors

Correspondence to Shigang He or Jufang He.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–5 (PDF 1645 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Yu, XJ., Xu, XX., He, S. et al. Change detection by thalamic reticular neurons. Nat Neurosci 12, 1165–1170 (2009). https://doi.org/10.1038/nn.2373

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2373

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