PKA dynamics in a Drosophila learning center: coincidence detection by rutabaga adenylyl cyclase and spatial regulation by dunce phosphodiesterase.
The dynamics of PKA activity in the olfactory learning and memory center, the mushroom bodies (MBs), are still poorly understood. We addressed this issue in vivo using a PKA FRET probe. Application of dopamine, the main neuromodulator involved in aversive learning, resulted in PKA activation specifically in the vertical lobe, whereas octopamine, involved in appetitive learning, stimulated PKA in all MB lobes. Strikingly, MB lobes were homogeneously activated by dopamine in the learning mutant dunce, showing that Dunce phosphodiesterase plays a major role in the spatial regulation of cAMP dynamics. Furthermore, costimulation with acetylcholine and either dopamine or octopamine led to a synergistic activation of PKA in the MBs that depends on Rutabaga adenylyl cyclase. Our results suggest that Rutabaga acts as a coincidence detector and demonstrate the existence of subcellular domains of PKA activity that could underlie the functional specialization of MB lobes in aversive and appetitive learning.
Gervasi
Nicolas
N
Genes and Dynamics of Memory Systems, Neurobiology Unit, Ecole Supérieure de Physique et Chimie Industrielle, CNRS, 10 rue Vauquelin, 75005 Paris, France.
Tchénio
Paul
P
Preat
Thomas
T
D000109:Acetylcholine / Q000378:metabolism / Q000494:pharmacology; D000262:Adenylyl Cyclases / Q000235:genetics / Q000378:metabolism*; D000818:Animals; D030801:Animals, Genetically Modified; D001245:Association Learning / Q000187:drug effects / Q000502:physiology*; D001362:Avoidance Learning / Q000187:drug effects / Q000502:physiology; D001369:Axons / Q000187:drug effects / Q000378:metabolism; D017868:Cyclic AMP-Dependent Protein Kinases / Q000235:genetics / Q000378:metabolism*; D003712:Dendrites / Q000187:drug effects / Q000378:metabolism; D004298:Dopamine / Q000378:metabolism / Q000494:pharmacology; D029721:Drosophila Proteins / Q000235:genetics / Q000378:metabolism*; D004331:Drosophila melanogaster; D007091:Image Processing, Computer-Assisted; D008570:Memory, Short-Term / Q000187:drug effects / Q000502:physiology*; D036641:Microscopy, Fluorescence, Multiphoton; D009042:Motivation / Q000187:drug effects / Q000502:physiology; D024521:Mushroom Bodies / Q000187:drug effects / Q000378:metabolism*; D009655:Octopamine / Q000378:metabolism / Q000502:physiology; D009833:Olfactory Pathways / Q000187:drug effects / Q000378:metabolism; D015398:Signal Transduction / Q000502:physiology
D029721:Drosophila Proteins; C523245:dnc protein, Drosophila; D009655:Octopamine; D017868:Cyclic AMP-Dependent Protein Kinases; D000262:Adenylyl Cyclases; C479926:Rut protein, Drosophila; D000109:Acetylcholine; D004298:Dopamine