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.

  • Letter
  • Published:

Glutamate locally activates dendritic outputs of thalamic interneurons

Abstract

The relay of information through thalamus to cortex is dynamically gated, as illustrated by the retinogeniculocortical pathway1. Important to this is the inhibitory interneuron in the lateral geniculate nucleus (LGN). For the typical neuron, synaptic information arrives through postsynaptic dendrites and is transmitted by axon terminals. However, the typical thalamic interneuron, in addition to conventional axonal outputs, has distal dendrites that serve both pre- and postsynaptic roles2,3,4,5,6. These dendritic terminals participate in curious and enigmatic triadic arrangements, in which each contacts a relay cell dendrite and is contacted by a glutamatergic retinal terminal that innervates the same relay cell dendrite. Here we show that agonists of the metabotropic glutamate receptor (mGluR) activate dendritic terminals of interneurons in the absence of action potentials, thereby inhibiting the postsynaptic relay neuron. Somatic recordings from LGN interneurons reveal that there is no response to mGluR agonists, suggesting that their dendritic terminals are electrically isolated from their somata and axons, consistent with anatomical modelling of these cells7. Our results offer insight into the functioning of triadic circuitry and indicate that thalamic interneurons can perform independent computations expressed through axonal as opposed to dendritic outputs.

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: Activation of mGluRs increases inhibition in cat LGN relay neurons.
Figure 2: Voltage and current clamp recordings from cat LGN neuron.
Figure 3: Inhibitory innervation of thalamic relay neurons and voltage clamp recording from rat LGN relay neuron.

Similar content being viewed by others

References

  1. Sherman, S. M. & Guillery, R. W. Functional organization of thalamocortical relays. J. Neurophysiol. 76, 1367–1395 (1996).

    Article  CAS  Google Scholar 

  2. Famiglietti, E. V. J & Peters, A. The synaptic glomerulus and the intrinsic neuron in the dorsal lateral geniculate nucleus of the cat. J. Comp. Neurol. 144, 285–334 (1972).

    Article  Google Scholar 

  3. Guillery, R. W. The organization of synaptic interconnections in the laminae of the dorsal lateral geniculate nucleus of the cat. Zeitschr. Zellforsch. Mikroskop. Anat. 96, 1–38 (1969).

    Article  CAS  Google Scholar 

  4. Hamos, J. E., Van Horn, S. C., Raczkowski, D., Uhlrich, D. J. & Sherman, S. M. Synaptic connectivity of a local circuit neurone in lateral geniculate nucleus of the cat. Nature 317, 618–621 (1985).

    Article  ADS  CAS  Google Scholar 

  5. Montero, V. M. Localization of gamma-aminobutyric acid (GABA) in type 3 cells and demonstration of their source to F2 terminals in the cat lateral geniculate nucleus: a Golgi–electron-microscopic GABA–immunocytochemical study. J. Comp. Neurol. 254, 228–245 (1986).

    Article  CAS  Google Scholar 

  6. Ralston, H. J. Evidence for presynaptic dendrites and a proposal for their mechanism of action. Nature 230, 585–587 (1971).

    Article  ADS  Google Scholar 

  7. Bloomfield, S. A. & Sherman, S. M. Dendritic current flow in relay cells and interneurons of the cat's lateral geniculate nucleus. Proc. Natl Acad. Sci. USA 86, 3911–3914 (1989).

    Article  ADS  CAS  Google Scholar 

  8. Guillery, R. W. Astudy of Golgi preparations from the dorsal lateral geniculate nucleus of the adult cat. J. Comp. Neurol. 128, 21–50 (1966).

    Article  CAS  Google Scholar 

  9. Friedlander, M. J., Lin, C.-S., Stanford, L. R. & Sherman, S. M. Morphology of functionally identified neurons in lateral geniculate nucleus of the cat. J. Neurophysiol. 46, 80–129 (1981).

    Article  CAS  Google Scholar 

  10. LeVay, S. & Ferster, D. Relay cell classes in the lateral geniculate nucleus of the cat and the effects of visual deprivation. J. Comp. Neurol. 172, 563–584 (1977).

    Article  CAS  Google Scholar 

  11. Wilson, J. R., Friedlander, M. J. & Sherman, S. M. Fine structural morphology of identified X- and Y-cells in the cat's lateral geniculate nucleus. Proc. R. Soc. B 22, 411–436 (1984).

    ADS  Google Scholar 

  12. Godwin, D. W. et al. Ultrastructural localization suggests that retinal and cortical inputs access different metabotropic glutamate receptors in the lateral geniculate nucleus. J. Neurosci. 16, 8181–8192 (1996).

    Article  CAS  Google Scholar 

  13. Charpak, S., Gähwiler, B. H., Do, K.-Q. & Knöpfel, T. Potassium conductances in hippocampal neurons blocked by excitatory amino-acid transmitters. Nature 347, 765–767 (1990).

    Article  ADS  CAS  Google Scholar 

  14. McCormick, D. A. & von Krosigk, M. Corticothalamic activation modulates thalamic firing through glutamate “metabotropic” receptors. Proc. Natl Acad. Sci. USA 89, 2774–2778 (1992).

    Article  ADS  CAS  Google Scholar 

  15. Pape, H.-C. & McCormick, D. A. Electrophysiological and pharmacological properties of interneurons in the cat dorsal lateral geniculate nucleus. Neuroscience 68, 1105–1125 (1995).

    Article  CAS  Google Scholar 

  16. Lee, K. H. & McCormick, D. A. Modulation of spindle oscillations by acetylcholine, cholecystokinin and 1 S,3 R -ACPD in the ferret lateral geniculate and perigeniculate nuclei in vitro. Neuroscience 77, 335–350 (1997).

    Article  CAS  Google Scholar 

  17. Sherman, S. M. & Cox, C. L. Excitatory and inhibitory actions of metabotropic glutamate receptor activation in rat thalamic reticular neurons. Soc. Neurosci. Abstr. 23, 73.10 (1997).

    Google Scholar 

  18. Arcelli, P., Frassoni, C., Regondi, M. C., De Biasi, S. & Spreafico, R. GABAergic neurons in mammalian thalamus: A marker of thalamic complexity? Brain Res. Bull. 42, 27–37 (1997).

    Article  CAS  Google Scholar 

  19. Ottersen, O. P. & Storm-Mathisen, J. GABA-containing neurons in the thalamus and protectum of the rodent. An immunocytochemical study. Anat. Embryol. 170, 197–207 (1984).

    Article  CAS  Google Scholar 

  20. Edwards, F. A., Konnerth, A., Sakmann, B. & Takahashi, T. Athin slice preparation for patch clamp recordings from neurons of the mammalian central nervous system. Pflugers Arch. 414, 600–612 (1989).

    Article  CAS  Google Scholar 

  21. Stuart, G. J., Dodt, H. U. & Sakmann, B. Patch-clamp recordings from the soma and dendrites of neurons in brain slices using infrared video microscopy. Eur. J. Physiol. 423, 511–518 (1993).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by National Eye Institute (NIH).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to S. Murray Sherman.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cox, C., Zhou, Q. & Sherman, S. Glutamate locally activates dendritic outputs of thalamic interneurons. Nature 394, 478–482 (1998). https://doi.org/10.1038/28855

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/28855

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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