Dendritic spatial flicker of local membrane potential due to channel noise and probabilistic firing of hippocampal neurons in culture.
Whole-cell recordings and imaging of dissociated hippocampal neurons stained with voltage sensitive dye provide a new microscopic picture of neuronal excitation. This is the first attempt to combine imaging of active channel clusters on the geometry of live neurons and a theoretical approach. During single somatic action potentials and the back-invasion into the neurites, local mean potentials are generated at sites of active channel clusters which are unevenly distributed in the neuronal membrane. Similar mean membrane potentials are observed in the neurites and at the soma. Identical action potentials produce different spatial patterns of mean membrane potentials from trial to trial. This spatial variability is explained by the stochastic behavior of the channels in the clusters. When hippocampal neurons are excited by synaptic inputs, their evoked responses are probabilistic and generate variable spatial patterns of mean membrane potential trial after trial. Our stochastic model reproduces this random behavior by assuming that the voltage fluctuations generated by channel noise are added to the synaptic potentials reaching the soma. We demonstrate that the probability of action potential initiation depends on the strength of the synaptic input, the diameter of the dendrites and the relative positions of the channel clusters, of the synapse and of the soma.
Savtchenko
L P
LP
Unité de Neurocybernétique Cellulaire, 280 Bd Sainte Marguerite, 13009 Marseille, France.
Gogan
P
P
Tyc-Dumont
S
S
D000200:Action Potentials / Q000502:physiology*; D000818:Animals; D000831:Animals, Newborn; D016477:Artifacts; D002450:Cell Communication / Q000502:physiology; D002478:Cells, Cultured / Q000166:cytology / Q000502:physiology; D003712:Dendrites / Q000502:physiology* / Q000648:ultrastructure; D004558:Electric Stimulation; D001330:Electronic Data Processing / Q000295:instrumentation / Q000379:methods; D005456:Fluorescent Dyes / Q000493:pharmacokinetics; D006624:Hippocampus / Q000166:cytology / Q000502:physiology*; D007091:Image Processing, Computer-Assisted / Q000295:instrumentation / Q000379:methods; D007473:Ion Channels / Q000502:physiology*; D018715:Microscopy, Video / Q000295:instrumentation / Q000379:methods; D008959:Models, Neurological; D015233:Models, Statistical; D018408:Patch-Clamp Techniques; D017966:Pyramidal Cells / Q000166:cytology / Q000502:physiology; D011726:Pyridinium Compounds / Q000493:pharmacokinetics; D051381:Rats; D017208:Rats, Wistar; D013269:Stochastic Processes; D013569:Synapses / Q000502:physiology*; D009435:Synaptic Transmission / Q000502:physiology*
D005456:Fluorescent Dyes; D007473:Ion Channels; D011726:Pyridinium Compounds; C048153:4-(6-(4-dibutylaminophenyl)-1,3,5-hexatrienyl)-1-(4'-sulfobutyl)pyridinium