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The Journal of Neuroscience, October 15, 2003, 23(28):9289-9296

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Behavioral/Systems/Cognitive
Suppression of Adult Neurogenesis Impairs Olfactory Learning and Memory in an Adult Insect

Sophie Scotto-Lomassese, Colette Strambi, Alain Strambi, Aïcha Aouane, Roger Augier, Geneviève Rougon, and Myriam Cayre

Laboratoire NMDA, Institut de Biologie du Développement de Marseille, Centre National de la Recherche Scientifique, Unité Mixte de Recherche 6156, Campus de Luminy, 13288 Marseille Cedex 9, France

Although adult neurogenesis has now been demonstrated in many different species, the functional role of newborn neurons still remains unclear. In the house cricket, a cluster of neuroblasts, located in the main associative center of the insect brain, keeps producing new interneurons throughout the animal's life. Here we address the functional significance of adult neurogenesis by specific suppression of neuroblast proliferation using irradiation of the insect's head and by examining the impact on the insect's learning ability. Forty gray irradiation performed on the first day of adult life massively suppressed neuroblasts and their progeny without inducing any noticeable side effect. We developed a new operant conditioning paradigm especially designed for crickets: the "escape paradigm." Using olfactory cues, visual cues, or both, crickets had to choose between two holes, one allowing them to escape and the other leading to a trap. Crickets lacking adult neurogenesis exhibited delayed learning when olfactory cues alone were used. Furthermore, retention 24 hr after conditioning was strongly impaired in irradiated crickets. By contrast, when visual cues instead of olfactory ones were provided, performance of irradiated insects was only slightly affected; when both olfactory and visual cues were present, their performance was not different from that of controls. From these results, it can be postulated that newborn neurons participate in the processing of olfactory information required for complex operant conditioning.

Key words: adult neurogenesis; mushroom body; neuroblasts; insect; house cricket; learning and memory; olfactory and visual conditioning; irradiation

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Received June 6, 2003; revised August 20, 2003; accepted August 21, 2003.

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