Afferent-specific innervation of two distinct AMPA receptor subtypes on single hippocampal interneurons

Abstract

Using the polyamine toxin philanthotoxin, which selectively blocks calcium-permeable AMPA receptors, we show that synaptic transmission onto single hippocampal interneurons occurs by afferent-specific activation of philanthotoxin-sensitive and -insensitive AMPA receptors. Calcium-permeable AMPA receptors are found exclusively at synapses from mossy fibers. In contrast, synaptic responses evoked by stimulation of CA3 pyramidal neurons are mediated by calcium-impermeable AMPA receptors. Both pathways converge onto single interneurons and can be discriminated with Group II mGluR agonists. Thus, single interneurons target AMPA receptors of different subunit composition to specific postsynaptic sites, providing a mechanism to increase the synapse-specific computational properties of hippocampal interneurons.

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Figure 1: Rectification properties and PhTx sensitivity of EPSCs on stratum lucidum interneurons.
Figure 2: PhTx blocks EPSCs in a use-dependent manner.
Figure 3: Calcium-permeable AMPA receptors are targeted to mossy-fiber synapses.
Figure 4: Single stratum lucidum interneurons express both calcium-permeable and calcium-impermeable AMPA receptors.

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Acknowledgements

The authors thank Mark Mayer, Gianmaria Maccaferri, Derek Bowie and Robert Bähring for their help and advice throughout the course of these experiments, Raymond Dingledine for sharing data prior to publication, and Mark Fleck, Mark Mayer and Vittorio Gallo for comments on the manuscript.

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Correspondence to Chris J. McBain.

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Tóth, K., McBain, C. Afferent-specific innervation of two distinct AMPA receptor subtypes on single hippocampal interneurons. Nat Neurosci 1, 572–578 (1998). https://doi.org/10.1038/2807

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