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Drosophila alpha/beta mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning.

ABSTRACT: Functional optical imaging showed that odor or electric shock stimuli presented to the fly causes transient calcium influx into the two major axon branches of alpha/beta mushroom body (MB) neurons. One pairing of odor and electric shock stimuli or multiple, massed pairings did not alter odor-evoked calcium influx. In contrast, animals that received multiple, spaced pairings exhibited a robust increase in calcium influx into the MB axons when tested at 9 or 24 hr after training, but not at 3 hr. This modification occurred only in the alpha branch of the neurons and was blocked by mutation of the amnesiac gene, inhibition of protein synthesis, or the expression of a protein blocker of the transcription factor Creb. Thus, behavioral long-term olfactory memory appears to be encoded as a branch-specific modification of calcium influx into the alpha/beta MB neurons that occurs after spaced training in a protein synthesis-, Creb-, and amnesiac-dependent way.

SUBMITTER: Yu D

PROVIDER: S-EPMC1779901 | biostudies-literature | 2006 Dec

REPOSITORIES: biostudies-literature

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Drosophila alpha/beta mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning.

Yu Dinghui D Akalal David-Benjamin G DB Davis Ronald L RL

Neuron 20061201 5

Functional optical imaging showed that odor or electric shock stimuli presented to the fly causes transient calcium influx into the two major axon branches of alpha/beta mushroom body (MB) neurons. One pairing of odor and electric shock stimuli or multiple, massed pairings did not alter odor-evoked calcium influx. In contrast, animals that received multiple, spaced pairings exhibited a robust increase in calcium influx into the MB axons when tested at 9 or 24 hr after training, but not at 3 hr. ...[more]

PMID: 17145505

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Project description:An animal's ability to learn and to form memories is essential for its survival. The fruit fly has proven to be a valuable model system for studies of learning and memory. One learned behavior in fruit flies is courtship conditioning. In Drosophila courtship conditioning, male flies learn not to court females during training with an unreceptive female. He retains a memory of this training and for several hours decreases courtship when subsequently paired with any female. Courtship conditioning is a unique learning paradigm; it uses a positive-valence stimulus, a female fly, to teach a male to decrease an innate behavior, courtship of the female. As such, courtship conditioning is not clearly categorized as either appetitive or aversive conditioning. The mushroom body (MB) region in the fruit fly brain is important for several types of memory; however, the precise subsets of intrinsic and extrinsic MB neurons necessary for courtship conditioning are unknown. Here, we disrupted synaptic signaling by driving a shibirets effector in precise subsets of MB neurons, defined by a collection of split-GAL4 drivers. Out of 75 lines tested, 32 showed defects in courtship conditioning memory. Surprisingly, we did not have any hits in the ? lobe Kenyon cells, a region previously implicated in courtship conditioning memory. We did find that several ? lobe extrinsic neurons were necessary for courtship conditioning memory. Overall, our memory hits in the dopaminergic neurons (DANs) and the mushroom body output neurons were more consistent with results from appetitive memory assays than aversive memory assays. For example, protocerebral anterior medial DANs were necessary for courtship memory, similar to appetitive memory, while protocerebral posterior lateral 1 (PPL1) DANs, important for aversive memory, were not needed. Overall, our results indicate that the MB circuits necessary for courtship conditioning memory coincide with circuits necessary for appetitive memory.

Dataset Information

Drosophila alpha/beta mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning.

Publications

Drosophila alpha/beta mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning.

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