An octopamine-mushroom body circuit modulates the formation of anesthesia-resistant memory in Drosophila.
BACKGROUND
Drosophila olfactory aversive conditioning produces two components of intermediate-term memory: anesthesia-sensitive memory (ASM) and anesthesia-resistant memory (ARM). Recently, the anterior paired lateral (APL) neuron innervating the whole mushroom body (MB) has been shown to modulate ASM via gap-junctional communication in olfactory conditioning. Octopamine (OA), an invertebrate analog of norepinephrine, is involved in appetitive conditioning, but its role in aversive memory remains uncertain.


RESULTS
Here, we show that chemical neurotransmission from the APL neuron, after conditioning but before testing, is necessary for aversive ARM formation. The APL neurons are tyramine, Tβh, and OA immunopositive. An adult-stage-specific RNAi knockdown of Tβh in the APL neurons or Octβ2R OA receptors in the MB α'β' Kenyon cells (KCs) impaired ARM. Importantly, an additive ARM deficit occurred when Tβh knockdown in the APL neurons was in the radish mutant flies or in the wild-type flies with inhibited serotonin synthesis.


CONCLUSIONS
OA released from the APL neurons acts on α'β' KCs via Octβ2R receptor to modulate Drosophila ARM formation. Additive effects suggest that two parallel ARM pathways, serotoninergic DPM-αβ KCs and octopaminergic APL-α'β' KCs, exist in the MB.
Brain Research Center, National Tsing Hua University, Hsinchu 30013, Taiwan; Department of Biochemistry and Graduate Institute of Biomedical Sciences, College of Medicine, Chang Gung University, Tao-Yuan 333, Taiwan.
Chia-Lin
CL
Wu
Meng-Fu Maxwell
MF
Shih
Pei-Tseng
PT
Lee
Ann-Shyn
AS
Chiang
D018759:Adrenergic Uptake Inhibitors / Q000494:pharmacology; D000316:Adrenergic alpha-Agonists / Q000494:pharmacology; D000758:Anesthesia; D000818:Animals; D030801:Animals, Genetically Modified; D003214:Conditioning, Classical / Q000502:physiology; D003213:Conditioning, Psychological / Q000502:physiology*; D017630:Connexins / Q000235:genetics; D004298:Dopamine / Q000378:metabolism; D029721:Drosophila Proteins / Q000096:biosynthesis / Q000235:genetics*; D004331:Drosophila melanogaster / Q000502:physiology*; D005968:Glutamate Decarboxylase / Q000235:genetics; D008568:Memory / Q000502:physiology*; D006899:Mixed Function Oxygenases / Q000235:genetics; D024521:Mushroom Bodies / Q000294:innervation; D009655:Octopamine / Q000096:biosynthesis / Q000378:metabolism*; D009812:Odorants; D034622:RNA Interference; D034741:RNA, Small Interfering; D043562:Receptors, G-Protein-Coupled / Q000235:genetics*; D009435:Synaptic Transmission; D014157:Transcription Factors / Q000096:biosynthesis; D014439:Tyramine / Q000378:metabolism; D014445:Tyrosine Decarboxylase; D005680:gamma-Aminobutyric Acid / Q000096:biosynthesis
D018759:Adrenergic Uptake Inhibitors; D000316:Adrenergic alpha-Agonists; D017630:Connexins; D029721:Drosophila Proteins; C557617:GAL4 protein, Drosophila; C503411:Octbeta2R protein, Drosophila; D034741:RNA, Small Interfering; D043562:Receptors, G-Protein-Coupled; D014157:Transcription Factors; C120023:inx7 protein, Drosophila; D009655:Octopamine; D005680:gamma-Aminobutyric Acid; D006899:Mixed Function Oxygenases; C023205:tyramine beta-hydroxylase; D005968:Glutamate Decarboxylase; C402565:glutamate decarboxylase 1; C500802:Tdc2 protein, Drosophila; D014445:Tyrosine Decarboxylase; D004298:Dopamine; D014439:Tyramine