Shocking Revelations and Saccharin Sweetness in the Study of Drosophila Olfactory Memory

Abstract

It is now almost forty years since the first description of learning in the fruit fly Drosophila melanogaster. Various incarnations of the classic mutagenesis approach envisaged in the early days have provided around one hundred learning defective mutant fly strains. Recent technological advances permit temporal control of neural function in the behaving fly. These approaches have radically changed experiments in the field and have provided a neural circuit perspective of memory formation, consolidation and retrieval. Combining neural perturbations with more classical mutant intervention allows investigators to interrogate the molecular and cellular processes of memory within the defined neural circuits. Here, we summarize some of the progress made in the last ten years that indicates a remarkable conservation of the neural mechanisms of memory formation between flies and mammals. We emphasize that considering an ethologically-relevant viewpoint might provide additional experimental power in studies of Drosophila memory.

What the fly’s nose tells the fly’s brain

“…We know that the Kenyon cells decode the combinatorial odor code-that is, they provide the tag associated with any odor-because flies have been shown to use the output of Kenyon cells to learn odors that have been paired with reward or punishment (26). The previous section demonstrated that odors are represented in a distributed way over the population of Kenyon cells, but to see how these cells provide a (close to) unique output for each odor, we need to know properties of the combinatorial code produced by the antennal lobe.…”

<em>Drosophila</em> Adult Olfactory Shock Learning

“…The exposure of flies to repetitive training cycles with gaps between the training cycles (spaced training) leads to a consolidated form of long-term memory that is CREB transcription dependent and lasts up to a week. Training without gaps (massed training) leads to the formation of anesthesia-resistant memory (ARM), which similar to long-term memory, is typically measured 24 hr after 5 cycles of training 7,13,[15][16][17]20,21 .…”

“…The promoter-driven expression of light-or temperature-sensitive transgenes to activate or block the neural activity of specific neurons allows one to investigate which neurons are required for memory acquisition, consolidation and retrieval 3,4,11,15,16,20,[22][23][24] . Memory at 1 hr is typically measured when studying age-related memory impairment because this form of memory appears particularly vulnerable to the effects of ageing [11][12][13] .…”

“…The length of the adult stage accommodates longer-term genetic, behavioral, dietary and pharmacological manipulations of memory, in addition to determining the effect of aging and neurodegenerative disease on memory [3][4][5][6][11][12][13][15][16][17][18][19][20][21] . Classical conditioning is induced by the simultaneous presentation of a neutral odor cue (conditioned stimulus, CS + ) and a reinforcement stimulus, e.g., an electric shock or sucrose, (unconditioned stimulus, US), that become associated with one another by the animal 1,16 . A second conditioned stimulus (CS -) is subsequently presented without the US.…”

“…Studying memory in adult Drosophila allows for a detailed analysis of the behavior and circuitry involved and a measurement of long-term memory [15][16][17] . The length of the adult stage accommodates longer-term genetic, behavioral, dietary and pharmacological manipulations of memory, in addition to determining the effect of aging and neurodegenerative disease on memory [3][4][5][6][11][12][13][15][16][17][18][19][20][21] .…”