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.
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References
Sherman, S. M. & Guillery, R. W. Functional organization of thalamocortical relays. J. Neurophysiol. 76, 1367–1395 (1996).
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).
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).
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).
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).
Ralston, H. J. Evidence for presynaptic dendrites and a proposal for their mechanism of action. Nature 230, 585–587 (1971).
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).
Guillery, R. W. Astudy of Golgi preparations from the dorsal lateral geniculate nucleus of the adult cat. J. Comp. Neurol. 128, 21–50 (1966).
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).
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).
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).
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).
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).
McCormick, D. A. & von Krosigk, M. Corticothalamic activation modulates thalamic firing through glutamate “metabotropic” receptors. Proc. Natl Acad. Sci. USA 89, 2774–2778 (1992).
Pape, H.-C. & McCormick, D. A. Electrophysiological and pharmacological properties of interneurons in the cat dorsal lateral geniculate nucleus. Neuroscience 68, 1105–1125 (1995).
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).
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).
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).
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).
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).
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).
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This work was supported by National Eye Institute (NIH).
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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
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DOI: https://doi.org/10.1038/28855
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