Cl--dependent amplification of excitatory synaptic potentials at distal dendrites revealed by voltage imaging

Abstract

Processing of synaptic signals in somatodendritic compartments determines the neuronal computation. Although amplification of excitatory signals by local voltage-dependent cation channels has been extensively studied, its spatio-temporal dynamics in elaborate dendritic branches remains obscure because of technical limitation. Using fluorescent voltage imaging throughout dendritic arborizations in hippocampal pyramidal neurons, here we demonstrate a unique Cl--dependent remote computation mechanism equipped in distal branches. Local laser photolysis of caged-glutamate triggered excitatory postsynaptic potentials spreading along dendrites with gradual amplification toward the distal end whereas with attenuation toward the soma. Tour-de-force subcellular patch-clamp recordings from thin branches complemented with biophysical model simulation revealed that the asymmetric augmentation of excitation relies on the TTX-resistant Na+ channels and Cl--conductances accompanied with deeper dendritic resting potential. Taken together, the present study unveils cooperative voltage-dependent actions of cation and anion conductances for dendritic supralinear computation which can locally decode the spatio-temporal context of synaptic inputs.