Large, Stable Spikes Exhibit Differential Broadening in Excitatory and Inhibitory Neocortical Boutons

• Published in: Cell reports (Cambridge) Vol. 34; no. 2; p. 108612
• Main Authors: Ritzau-Jost, Andreas, Tsintsadze, Timur, Krueger, Martin, Ader, Jonas, Bechmann, Ingo, Eilers, Jens, Barbour, Boris, Smith, Stephen M., Hallermann, Stefan
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 12-01-2021; Cell Press; Elsevier
• Subjects: action potential; Electrophysiology - methods; en passant bouton; Humans; interneuron; layer 5 pyramidal neuron; long-term plasticity; neocortex; Neurons - physiology; presynapse; Presynaptic Terminals - physiology; short-term plasticity; Synapses - physiology; presynapse; en passant bouton; interneuron; long-term plasticity; neocortex; layer 5 pyramidal neuron; action potential; short-term plasticity
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2020.108612

Presynaptic action potential spikes control neurotransmitter release and thus interneuronal communication. However, the properties and the dynamics of presynaptic spikes in the neocortex remain enigmatic because boutons in the neocortex are small and direct patch-clamp recordings have not been performed. Here, we report direct recordings from boutons of neocortical pyramidal neurons and interneurons. Our data reveal rapid and large presynaptic action potentials in layer 5 neurons and fast-spiking interneurons reliably propagating into axon collaterals. For in-depth analyses, we establish boutons of mature cultured neurons as models for excitatory neocortical boutons, demonstrating that the presynaptic spike amplitude is unaffected by potassium channels, homeostatic long-term plasticity, and high-frequency firing. In contrast to the stable amplitude, presynaptic spikes profoundly broaden during high-frequency firing in layer 5 pyramidal neurons, but not in fast-spiking interneurons. Thus, our data demonstrate large presynaptic spikes and fundamental differences between excitatory and inhibitory boutons in the neocortex.
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•Establishment of patch-clamp recordings from boutons in the neocortex•High-resolution current clamp recordings reveal large and rapid action potentials•Action potentials reliably propagate into axon collaterals in the neocortex•Action potentials show differential plasticity in excitatory and inhibitory boutons
Small en passant boutons are the mammalian brain’s predominant synapse type. By establishing direct electrical bouton recordings, Ritzau-Jost et al. demonstrate large and reliably propagating action potentials. Action potentials in boutons of excitatory pyramidal neurons and inhibitory interneurons are unaffected during long-term plasticity but differentially broaden during short-term plasticity.