Analog modulation of spike-evoked transmission in CA3 circuits is determined by axonal Kv1.1 channels in a time-dependent manner.
Synaptic transmission usually depends on action potentials (APs) in an all-or-none (digital) fashion. Recent studies indicate, however, that subthreshold presynaptic depolarization may facilitate spike-evoked transmission, thus creating an analog modulation of spike-evoked synaptic transmission, also called analog-digital (AD) synaptic facilitation. Yet, the underlying mechanisms behind this facilitation remain unclear. We show here that AD facilitation at rat CA3-CA3 synapses is time-dependent and requires long presynaptic depolarization (5-10 s) for its induction. This depolarization-induced AD facilitation (d-ADF) is blocked by the specific Kv1.1 channel blocker dendrotoxin-K. Using fast voltage-imaging of the axon, we show that somatic depolarization used for induction of d-ADF broadened the AP in the axon through inactivation of Kv1.1 channels. Somatic depolarization enhanced spike-evoked calcium signals in presynaptic terminals, but not basal calcium. In conclusion, axonal Kv1.1 channels determine glutamate release in CA3 neurons in a time-dependent manner through the control of the presynaptic spike waveform.
INSERM, UMR_S 1072, Marseille, France; Aix-Marseille Université, UNIS, Marseille, France.
Andrzej
A
Bialowas
Sylvain
S
Rama
Mickaël
M
Zbili
Vincenzo
V
Marra
Laure
L
Fronzaroli-Molinieres
Norbert
N
Ankri
Edmond
E
Carlier
Dominique
D
Debanne
D000200:Action Potentials / Q000187:drug effects / Q000502:physiology*; D000818:Animals; D056654:CA3 Region, Hippocampal / Q000187:drug effects / Q000502:physiology*; D002118:Calcium / Q000378:metabolism; D065096:Calcium Chelating Agents / Q000494:pharmacology; D004533:Egtazic Acid / Q000494:pharmacology; D018698:Glutamic Acid / Q000378:metabolism; D051662:Kv1.1 Potassium Channel / Q000037:antagonists & inhibitors / Q000378:metabolism*; D008959:Models, Neurological; D018408:Patch-Clamp Techniques; D010455:Peptides / Q000494:pharmacology; D026902:Potassium Channel Blockers / Q000494:pharmacology; D017966:Pyramidal Cells / Q000187:drug effects / Q000502:physiology; D017208:Rats, Wistar; D012964:Sodium / Q000378:metabolism; D013569:Synapses / Q000187:drug effects / Q000502:physiology; D009435:Synaptic Transmission / Q000187:drug effects / Q000502:physiology*; D013995:Time; D046509:Tissue Culture Techniques
D065096:Calcium Chelating Agents; C489293:Kcna1 protein, rat; D010455:Peptides; D026902:Potassium Channel Blockers; C081506:dendrotoxin K; D051662:Kv1.1 Potassium Channel; D018698:Glutamic Acid; D004533:Egtazic Acid; D012964:Sodium; D002118:Calcium
axon terminal; potassium channels; rat; synaptic plasticity