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The Journal of Neuroscience, November 15, 1999, 19(22):10125-10134

Reversible Downregulation of Protein Kinase A during Olfactory Learning Using Antisense Technique Impairs Long-Term Memory Formation in the Honeybee, Apis mellifera

André Fiala, Uli Müller, and Randolf Menzel

Institut für Neurobiologie der Freien Universität Berlin, 14195 Berlin, Germany

In this study, we examined the role of cAMP-dependent protein kinase (PKA) in associative olfactory learning of the honeybee, Apis mellifera. In the bee, specific interference with molecules to clarify their role in a certain behavior is difficult, because genetic approaches, such as mutants or transgenic animals, are not feasible at the moment. As a new approach in insects in vivo, we report the use of short antisense oligonucleotides. We show that phosphorothioate-modified oligodeoxynucleotides complementary to the mRNA of a catalytic subunit of PKA directly injected into the bee brain cause a reversible and specific downregulation of both the amount of the catalytic subunit and of PKA activity by 10-15%. The amounts of the regulatory subunit of PKA, as well as PKC, are not affected. The slight "knockdown" of PKA activity during the training procedure, a classical olfactory conditioning of the proboscis extension reflex, neither affects acquisition nor memory retention 3 or 6 hr after training. However, it causes an impairment of long-term memory retention 24 hr after training. Downregulation of PKA 3 hr after training has no detectable effect on memory formation. We conclude that PKA contributes to the induction of a long-term memory 24 hr after training when activated during learning. Second, we demonstrate that the antisense technique is feasible in honeybees in vivo and provides a new and powerful tool for the study of the molecular basis of learning and memory formation in insects.

Key words: antisense oligonucleotides; Apis mellifera; cAMP-dependent protein kinase; honeybee; insect; long-term memory; olfactory learning; PKA

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Copyright © 1999 Society for Neuroscience  0270-6474/99/192210125-10$05.00/0

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