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The Journal of Neuroscience, September 30, 2009, 29(39):12302-12314; doi:10.1523/JNEUROSCI.3383-09.2009

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Development/Plasticity/Repair
Turnover of Newborn Olfactory Bulb Neurons Optimizes Olfaction

Aurélie Mouret,^1,2 Gabriel Lepousez,³ Julien Gras,^1,2 Marie-Madeleine Gabellec,^1,2 and Pierre-Marie Lledo^1,2

¹Institut Pasteur, Perception and Memory Unit, ²Centre National de la Recherche Scientifique, Unité de Recherche Associée 2182, F-75724 Paris, France, and ³Inserm Unité Mixte de Recherche 894, Centre de Psychiatrie et Neurosciences, Université Paris Descartes, F-75014 Paris, France

Correspondence should be addressed to Dr. Pierre-Marie Lledo, Institut Pasteur, Perception and Memory Unit, 25 rue du Dr. Roux, F-75724 Paris Cedex 15, France. Email: pierre-marie.lledo{at}pasteur.fr

Postdevelopmental neurogenesis occurs in the olfactory bulb (OB), to which new interneurons are continuously recruited. However, only a subset of the adult-generated interneurons survives, as many undergo programmed cell death. As part of homeostatic processes, the removal of new neurons is required alongside the addition of new ones, to ensure a stable neuron number. In addition to a critical role in tissue maintenance, it is still unclear whether this neuronal elimination affects the functioning of adult circuits. Using focal drug delivery restricted to the OB, we investigated the significance of programmed cell death in the adult OB circuits. Cell death was effectively blocked by the broad-spectrum caspase inhibitor benzyloxycarbonyl-Val-Ala-Asp(OMe)-fluoromethylketone (zVAD). The zVAD effect differed with newborn interneuron location, either in the superficial (periglomerular cells) or in the deep (granule cells) OB layers. Furthermore, whereas sensory experience potentiated the effect of zVAD on the survival of new granule cells, it had no additional effect on the survival of new periglomerular cells. Thus, distinct mechanisms control the survival/elimination decision of newborn interneuron subtypes. However, zVAD had no effect on the olfactory sensory neurons projecting to the bulb. Remarkably, psychophysical analyzes revealed that a normal rate of new neuron elimination was essential for optimal odorant exploration and discrimination. This study highlights the importance of cell elimination for adjusting olfactory performance. We conclude that adult-generated OB interneurons are continually turned over, rather than simply added, and the precise balance between new and mature interneurons, set through active selection/elimination processes, is essential for optimizing olfaction.

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Received July 14, 2009; accepted Aug. 5, 2009.

Correspondence should be addressed to Dr. Pierre-Marie Lledo, Institut Pasteur, Perception and Memory Unit, 25 rue du Dr. Roux, F-75724 Paris Cedex 15, France. Email: pierre-marie.lledo{at}pasteur.fr

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