Suppression of Adult Neurogenesis Impairs Olfactory Learning and Memory in an Adult Insect

• Published in: The Journal of neuroscience 2003-10, Vol.23 (28), p.9289-9296
• Main Authors: Scotto-Lomassese, Sophie, Strambi, Colette, Strambi, Alain, Aouane, Aicha, Augier, Roger, Rougon, Genevieve, Cayre, Myriam
• Format: Article
• Language: English
• Subjects: Animals; Behavior, Animal - physiology; Behavior, Animal - radiation effects; Behavioral/Systems/Cognitive; Conditioning, Operant - physiology; Cues; Dose-Response Relationship, Radiation; Gamma Rays; Ganglia, Invertebrate - cytology; Ganglia, Invertebrate - physiology; Ganglia, Invertebrate - radiation effects; Gryllidae - physiology; Learning - physiology; Learning - radiation effects; Memory - physiology; Memory - radiation effects; Motor Activity - radiation effects; Mushroom Bodies - cytology; Mushroom Bodies - radiation effects; Neurons - physiology; Neurons - radiation effects; Photic Stimulation; Retention (Psychology) - radiation effects; Smell - physiology; Smell - radiation effects; Stimulation, Chemical
• ISSN: 0270-6474; 1529-2401
• DOI: 10.1523/jneurosci.23-28-09289.2003

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 gamma 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.