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The Journal of Neuroscience, July 2, 2003, 23(13):5553-5560

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Action Potential Propagation in Dendrites of Rat Mitral Cells In Vivo

F. Debarbieux, E. Audinat, and S. Charpak

Laboratoire de Neurophysiologie, Institut National de la Santé et la Recherche Médicale, EPI 0002, Centre National de la Recherche Scientifique, FRE 2500, Ecole Supérieure de Physique et Chimie Industrielles de la Ville de Paris, 75231 Paris, France

Odors evoke - frequency field potential oscillations in the olfactory systems of awake and anesthetized vertebrates. In the rat olfactory bulb, these oscillations reflect the synchronous discharges of mitral cells that result from both their intrinsic membrane properties and their dendrodendritic interactions with local inhibitory interneurons. Activation of dendrodendritic synapses is purportedly involved in odor memory and odor contrast enhancement. Here we investigate in vivo to what extent action potentials propagate to remote dendrodendritic sites in the entire dendritic tree and if this propagation is changed during discharges at 40 Hz. By combining intracellular recording and two-photon microscopy imaging of intracellular calcium ([Ca²⁺]_i), we show that in remote branches of the apical tuft and basal dendrites, transient Ca²⁺ changes are triggered by single sodium action potentials. Neither the amplitude of these Ca²⁺ transients nor that of action potentials obtained from intradendritic recordings showed a significant attenuation as a function of the distance from the soma. Calcium channel density seemed homogeneous; however, propagating action potentials occasionally failed to trigger a Ca²⁺ transient at a site closer to the soma whereas it did farther. This suggests that measurements of calcium transients underestimate the occurrence of sodium action potentials. During 40 Hz bursts of action potentials, [Ca²⁺]_i increases with the number of action potentials in all dendritic compartments. These results suggest that the presence of release sites in dendrites is accompanied by an "axonal-like behavior" of the entire dendritic tree of mitral cells, including their most distal dendritic branches.

Key words: olfactory bulb; two-photon microscopy; oscillation; calcium signaling; rat; intracellular recording

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Received Jan. 29, 2003; revised Apr. 7, 2003; accepted Apr. 15, 2003.

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