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:

Differential synaptic processing separates stationary from transient inputs to the auditory cortex

Abstract

Sound features are blended together en route to the central nervous system before being discriminated for further processing by the cortical synaptic network. The mechanisms underlying this synaptic processing, however, are largely unexplored. Intracortical processing of the auditory signal was investigated by simultaneously recording from pairs of connected principal neurons in layer II/III in slices from A1 auditory cortex. Physiological patterns of stimulation in the presynaptic cell revealed two populations of postsynaptic events that differed in mean amplitude, failure rate, kinetics and short-term plasticity. In contrast, transmission between layer II/III pyramidal neurons in barrel cortex were uniformly of large amplitude and high success (release) probability (Pr). These unique features of auditory cortical transmission may provide two distinct mechanisms for discerning and separating transient from stationary features of the auditory signal at an early stage of cortical processing.

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: Two layer II/III cortico–cortical excitatory connection phenotypes.
Figure 2: Differing properties of HPCs and LPCs.
Figure 3: Short-term plasticity at LFCs and HFC connections.
Figure 4: Time course of recovery from short-term depression at HPCs.
Figure 5: Differential dependence of short-term plasticity on [Ca2+]o in HPCs.
Figure 6: Differential dependence of short term plasticity on [Ca2+]o in LPCs.
Figure 7: Equivalent connections were not observed in barrel cortex.
Figure 8: Synchronous spontaneous synaptic input onto connected layer II/III cells.

Similar content being viewed by others

References

  1. Rouiller, E., de Ribaupierre, Y., Toros-Morel, A. & de Ribaupierre, F. Neural coding of repetitive clicks in the medial geniculate body of the cat. Hear. Res. 5, 81–100 (1981).

    Article  CAS  PubMed  Google Scholar 

  2. Phillips, D. P. & Kelly, J. B. Coding of tone-pulse amplitude by single neurons in auditory cortex of albino rat. Hear. Res. 37, 269–280 (1989).

    Article  CAS  PubMed  Google Scholar 

  3. Clarey, J. C., Barone, P. & Imig, T. J. in The Mammalian Auditory Pathway: Neurophysiology (eds. Popper, A. N. & Fay, R. R.) 232–334 (Springer, New York, 1992).

    Book  Google Scholar 

  4. Winer, J. A. The pyramidal neurons in layer III of cat primary auditory cortex (AI). J. Comp. Neurol. 229, 476–496 (1984).

    Article  CAS  PubMed  Google Scholar 

  5. Winer, J. A. Structure of layer II in cat primary auditory cortex (AI). J. Comp. Neurol. 238, 10–37 (1985).

    Article  CAS  PubMed  Google Scholar 

  6. Metherate, R. & Aramakis, V. B. Intrinsic electrophysiology of neurons in thalamorecipient layers of developing rat auditory cortex. Dev. Brain Res. 115, 131–44 (1999).

    Article  CAS  Google Scholar 

  7. Clarke, S., de Ribaupierre, F., Rouiller, E. M. & de Ribaupierre, Y. Several neuronal and axonal types form long intrinsic connections in the cat primary auditory cortical field (AI). Anat. Embryol. (Berl.) 188, 117–138 (1993).

    Article  CAS  Google Scholar 

  8. Shen, J. X., Xu, Z. M. & Yao, Y. D. Evidence for columnar organization in the auditory cortex of the mouse. Hear. Res. 137, 174–177 (1999).

    Article  CAS  PubMed  Google Scholar 

  9. Blaschke, M. et al. A single amino-acid determines the subunit-specific spider toxin block of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionate kainate receptor channels. Proc. Natl. Acad. Sci. USA 90, 6528–6528 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Brackley, P. T., Bell, D. R., Choi, D. K., Nakanishi, K. & Usherwood, P. N. Selective antagonism of native and cloned kainate and NMDA receptors by polyamine-containing toxins. J. Pharmacol. Exp. Ther. 266, 1573–1580 (1993).

    CAS  PubMed  Google Scholar 

  11. Herlitze, S. et al. Argiotoxin detects molecular differences in AMPA receptor channels. Neuron 10, 1131–1140 (1993).

    Article  CAS  PubMed  Google Scholar 

  12. Washburn, M. S. & Dingledine, R. Block of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors by polyamines and polyamine toxins. J. Pharmacol. Exp. Ther. 278, 669–678 (1996).

    CAS  PubMed  Google Scholar 

  13. Toth, K., & McBain, C. J. Afferent specific innervation of two distinct AMPA receptor subtypes on single hippocampal interneurons. Nat. Neurosci. 1, 572–578 (1998).

    Article  CAS  PubMed  Google Scholar 

  14. Dingledine, R., Borges, K., Bowie, D. & Traynelis, S. The glutamate receptor ion channels. Pharmacol. Rev. 51, 7–61 (1999).

    CAS  PubMed  Google Scholar 

  15. Markram, H., Lubke, J., Frotscher, M., Roth, A. & Sakmann, B. Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. J. Physiol. (Lond.) 500, 409–440 (1997).

    Article  CAS  Google Scholar 

  16. Faber, D. & Korn, H. Applicability of the coefficient of variation method for analyzing synaptic plasticity. Biophys. J. 60, 1288–1291 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. DeCharms, R. C., Blake, D. T. & Merzenich, M. M. Optimizing sound features for cortical neurons. Science 280, 1439–1443 (1998).

    Article  CAS  PubMed  Google Scholar 

  18. DeCharms, R. C. & Zador, A. Neural representation and the cortical code. Annu. Rev. Neurosci. 23, 613–647 (2000).

    Article  CAS  PubMed  Google Scholar 

  19. 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 

  20. Zucker, R. S. Short-term synaptic plasticity. Annu. Rev. Neurosci. 12, 13–31 (1989).

    Article  CAS  PubMed  Google Scholar 

  21. Zucker, R. S. Calcium- and activity-dependent synaptic plasticity. Curr. Opin. Neurobiol. 9, 305–313 (1999).

    Article  CAS  PubMed  Google Scholar 

  22. Debanne, D., Guerineau, N. C., Gahwiler, B. H. & Thompson, S. M. Paired pulse facilitation and depression at unitary synapses in rat hippocampus: quantal fluctuation affects subsequent release. J. Physiol. (Lond.) 491, 163–176 (1996).

    Article  CAS  Google Scholar 

  23. Feldman, D. E. Timing-based LTP and LTD at vertical inputs to Layer II/III pyramidal cells in rat barrel cortex. Neuron 27, 45–56 (2000).

    Article  CAS  PubMed  Google Scholar 

  24. Schreiner, C. E., Read, H. L. & Sutter, M. L. Modular organization of frequency integration in primary auditory cortex. Annu. Rev. Neurosci. 23, 501–529 (2000).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  26. Giraud, A. et al. Representation of the temporal envelope sounds in the human brain. J. Neurophysiol. 22, 1588–1598 (2000).

    Article  Google Scholar 

  27. Kaas, J. & Hackett, T. 'What' and 'where' processing in the auditory cortex. Nat. Neurosci. 2, 1045–1047 (1999).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank D. Feldman for his assistance in preparing Barrel cortex slices and C. Trouth for cell reconstruction and camera lucida drawings of neurons. This work was supported by an Intramural Research award to C.McB.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chris J. McBain.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Atzori, M., Lei, S., Evans, D. et al. Differential synaptic processing separates stationary from transient inputs to the auditory cortex. Nat Neurosci 4, 1230–1237 (2001). https://doi.org/10.1038/nn760

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn760

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