A dendrodendritic reciprocal synapse provides a recurrent excitatory connection in the olfactory bulb

doi:10.1073/pnas.101126398

A dendrodendritic reciprocal synapse provides a recurrent excitatory connection in the olfactory bulb

^*Centre National de la Recherche Scientifique, UMR-5020, Université Claude Bernard, 69622, Villeurbanne Cedex, France; ^‡Centre National de la Recherche Scientifique, UPR-2197, 91198 Gif-sur-Yvette Cedex, France; and ^§Department of Anatomy, Institute for Basic Medical Sciences, University of Oslo, Blindern 0317 Oslo, Norway

Communicated by D. Carleton Gajdusek, Centre National de la Recherche Scientifique, Gif-sur-Yvette, France (received for review January 24, 2001)

Abstract

Neuronal synchronization in the olfactory bulb has been proposed to arise from a diffuse action of glutamate released from mitral cells (MC, olfactory bulb relay neurons). According to this hypothesis, glutamate spills over from dendrodendritic synapses formed between MC and granule cells (GC, olfactory bulb interneurons) to activate neighboring MC. The excitation of MC is balanced by a strong inhibition from GC. Here we show that MC excitation is caused by glutamate released from bulbar interneurons located in the GC layer. These reciprocal synapses depend on an unusual, 2-amino-5-phosphonovaleric acid-resistant, N-methyl-d-aspartate receptor. This type of feedback excitation onto relay neurons may strengthen the original sensory input signal and further extend the function of the dendritic microcircuit within the main olfactory bulb.

Footnotes

↵ † A.D. and A.C. contributed equally to this work.
↵ ¶ To whom reprint requests should be addressed. E-mail: Pierre-Marie.Lledo{at}iaf.cnrs-gif.fr.
Abbreviations:

APV,

2-amino-5-phosphonovaleric acid;

BMI,

bicuculline methiodide;

CPP,

3-[(±)-2-carboxypiperazin-4-yl]propyl-1-phosphonate;

dCK,

5,7-dichlorokynurenic acid;

EPL,

external plexiform layer;

EPSC,

excitatory postsynaptic current;

4-AP,

4-aminopyridine;

GABA,

γ-aminobutyric acid;

GC,

granule cells;

IA,

A-type potassium current;

IPSC,

inhibitory postsynaptic current;

MC,

mitral cells;

NBQX,

1,2,3,4-tetrahydro-6-nitro-2,3-dioxobenzo[f]quinoxaline-7-sulfonamide;

NMDA,

N-methyl-d-aspartate;

PTX,

picrotoxin;

TTX,

tetrodotoxin