Large, Stable Spikes Exhibit Differential Broadening in Excitatory and Inhibitory Neocortical Boutons
Andreas Ritzau-Jost,
Timur Tsintsadze,
Martin Krueger,
Jonas Ader,
Ingo Bechmann,
Jens Eilers,
Boris Barbour,
Stephen M. Smith,
Stefan Hallermann
Affiliations
Andreas Ritzau-Jost
Carl-Ludwig-Institute for Physiology, Faculty of Medicine, Leipzig University, 04103 Leipzig, Germany
Timur Tsintsadze
Division of Pulmonary and Critical Care Medicine, Department of Medicine, Oregon Health and Science University, Portland, OR 97239, USA; Section of Pulmonary and Critical Care Medicine, VA Portland Health Care System, Portland, OR 97239, USA
Martin Krueger
Institute of Anatomy, Faculty of Medicine, Leipzig University, 04103 Leipzig, Germany
Jonas Ader
Carl-Ludwig-Institute for Physiology, Faculty of Medicine, Leipzig University, 04103 Leipzig, Germany
Ingo Bechmann
Institute of Anatomy, Faculty of Medicine, Leipzig University, 04103 Leipzig, Germany
Jens Eilers
Carl-Ludwig-Institute for Physiology, Faculty of Medicine, Leipzig University, 04103 Leipzig, Germany
Boris Barbour
Institut de Biologie de l’Ecole Normale Supérieure (IBENS), Ecole Normale Supérieure, CNRS, INSERM, PSL Université Paris, 75005 Paris, France
Stephen M. Smith
Division of Pulmonary and Critical Care Medicine, Department of Medicine, Oregon Health and Science University, Portland, OR 97239, USA; Section of Pulmonary and Critical Care Medicine, VA Portland Health Care System, Portland, OR 97239, USA; Corresponding author
Stefan Hallermann
Carl-Ludwig-Institute for Physiology, Faculty of Medicine, Leipzig University, 04103 Leipzig, Germany; Corresponding author
Summary: 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.
