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Open Access Highly Accessed Research article

Dynamics of glutamatergic signaling in the mushroom body of young adult Drosophila

Irina Sinakevitch125*, Yves Grau3, Nicholas J Strausfeld4 and Serge Birman12*

Author Affiliations

1 Laboratoire de Neurobiologie, CNRS UMR 7637, ESPCI ParisTech, 10 rue Vauquelin, 75231 Paris cedex 5, France

2 Institut de Biologie du Développement de Marseille-Luminy, CNRS UMR 6216, Université de la Méditerranée, Campus de Luminy case 907, 13288 Marseille cedex 9, France

3 Institut de Génomique Fonctionnelle, CNRS UMR 5203, INSERM U661, Université de Montpellier I et II, 141 rue de la Cardonille, 34094 Montpellier cedex 5, France

4 Center for Insect Science and Department of Neuroscience, University of Arizona, Tucson, Arizona 85721, USA

5 Current address: Arizona State University, School of Life Sciences, Tempe, AZ 85287-4501, USA

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Neural Development 2010, 5:10  doi:10.1186/1749-8104-5-10

Published: 6 April 2010

Abstract

Background

The mushroom bodies (MBs) are paired brain centers located in the insect protocerebrum involved in olfactory learning and memory and other associative functions. Processes from the Kenyon cells (KCs), their intrinsic neurons, form the bulk of the MB's calyx, pedunculus and lobes. In young adult Drosophila, the last-born KCs extend their processes in the α/β lobes as a thin core (α/β cores) that is embedded in the surrounding matrix of other mature KC processes. A high level of L-glutamate (Glu) immunoreactivity is present in the α/β cores (α/βc) of recently eclosed adult flies. In a Drosophila model of fragile X syndrome, the main cause of inherited mental retardation, treatment with metabotropic Glu receptor (mGluR) antagonists can rescue memory deficits and MB structural defects.

Results

To address the role of Glu signaling in the development and maturation of the MB, we have compared the time course of Glu immunoreactivity with the expression of various glutamatergic markers at various times, that is, 1 hour, 1 day and 10 days after adult eclosion. We observed that last-born α/βc KCs in young adult as well as developing KCs in late larva and at various pupal stages transiently express high level of Glu immunoreactivity in Drosophila. One day after eclosion, the Glu level was already markedly reduced in the α/βc neurons. Glial cell processes expressing glutamine synthetase and the Glu transporter dEAAT1 were found to surround the Glu-expressing KCs in very young adults, subsequently enwrapping the α/β lobes to become distributed equally over the entire MB neuropil. The vesicular Glu transporter DVGluT was detected by immunostaining in processes that project within the MB lobes and pedunculus, but this transporter is apparently never expressed by the KCs themselves. The NMDA receptor subunit dNR1 is widely expressed in the MB neuropil just after eclosion, but was not detected in the α/βc neurons. In contrast, we provide evidence that DmGluRA, the only Drosophila mGluR, is specifically expressed in Glu-accumulating cells of the MB α/βc immediately and for a short time after eclosion.

Conclusions

The distribution and dynamics of glutamatergic markers indicate that newborn KCs transiently accumulate Glu at a high level in late pupal and young eclosed Drosophila, and may locally release this amino acid by a mechanism that would not involve DVGluT. At this stage, Glu can bind to intrinsic mGluRs abundant in the α/βc KCs, and to NMDA receptors in the rest of the MB neuropil, before being captured and metabolized in surrounding glial cells. This suggests that Glu acts as an autocrine or paracrine agent that contributes to the structural and functional maturation of the MB during the first hours of Drosophila adult life.