Membrane lipids tune synaptic transmission by direct modulation of presynaptic potassium channels.
Voltage-gated potassium (Kv) channels are involved in action potential (AP) repolarization in excitable cells. Exogenous application of membrane-derived lipids, such as arachidonic acid (AA), regulates the gating of Kv channels. Whether membrane-derived lipids released under physiological conditions have an impact on neuronal coding through this mechanism is unknown. We show that AA released in an activity-dependent manner from postsynaptic hippocampal CA3 pyramidal cells acts as retrograde messenger, inducing a robust facilitation of mossy fiber (Mf) synaptic transmission over several minutes. AA acts by broadening presynaptic APs through the direct modulation of Kv channels. This form of short-term plasticity can be triggered when postsynaptic cell fires with physiologically relevant patterns and sets the threshold for the induction of the presynaptic form of long-term potentiation (LTP) at hippocampal Mf synapses. Hence, direct modulation of presynaptic Kv channels by activity-dependent release of lipids serves as a physiological mechanism for tuning synaptic transmission.
University of Bordeaux, Interdisciplinary Institute for Neuroscience, CNRS UMR 5297, 33000 Bordeaux, France.
Mario
M
Carta
University of Bordeaux, Interdisciplinary Institute for Neuroscience, CNRS UMR 5297, 33000 Bordeaux, France.
Frederic
F
Lanore
University of Bordeaux, Interdisciplinary Institute for Neuroscience, CNRS UMR 5297, 33000 Bordeaux, France.
Nelson
N
Rebola
University of Bordeaux, Interdisciplinary Institute for Neuroscience, CNRS UMR 5297, 33000 Bordeaux, France.
Zsolt
Z
Szabo
University of Bordeaux, Interdisciplinary Institute for Neuroscience, CNRS UMR 5297, 33000 Bordeaux, France.
Silvia Viana
SV
Da Silva
University of Bordeaux, Interdisciplinary Institute for Neuroscience, CNRS UMR 5297, 33000 Bordeaux, France.
Joana
J
Lourenço
Institut Jacques Monod, UMR 7592, CNRS and INSERM ERL U950, University Paris Diderot, Sorbonne Paris Cité, 75013 Paris, France.
Agathe
A
Verraes
EMBL Heidelberg, Meyerhofstraße 1, 69117 Heidelberg, Germany.
André
A
Nadler
EMBL Heidelberg, Meyerhofstraße 1, 69117 Heidelberg, Germany.
Carsten
C
Schultz
University of Bordeaux, Interdisciplinary Institute for Neuroscience, CNRS UMR 5297, 33000 Bordeaux, France.
Christophe
C
Blanchet
University of Bordeaux, Interdisciplinary Institute for Neuroscience, CNRS UMR 5297, 33000 Bordeaux, France. Electronic address: christophe.mulle@u-bordeaux.fr.
Christophe
C
Mulle
D000818:Animals; D004558:Electric Stimulation / Q000379:methods; D019706:Excitatory Postsynaptic Potentials / Q000502:physiology; D006624:Hippocampus / Q000378:metabolism*; D017774:Long-Term Potentiation / Q000502:physiology; D008563:Membrane Lipids / Q000378:metabolism*; D051379:Mice; D008810:Mice, Inbred C57BL; D019599:Mossy Fibers, Hippocampal / Q000378:metabolism; D009474:Neurons / Q000378:metabolism; D015221:Potassium Channels / Q000378:metabolism*; D017966:Pyramidal Cells / Q000378:metabolism; D013569:Synapses / Q000378:metabolism*; D009435:Synaptic Transmission / Q000502:physiology*
D008563:Membrane Lipids; D015221:Potassium Channels