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The GABAergic anterior paired lateral neuron suppresses and is suppressed by olfactory learning

Abstract

GABAergic neurotransmitter systems are important for many cognitive processes, including learning and memory. We identified a single neuron in each hemisphere of the Drosophila brain, the anterior paired lateral (APL) neuron, as a GABAergic neuron that broadly innervated the mushroom bodies. Reducing GABA synthesis in the APL neuron enhanced olfactory learning, suggesting that the APL neuron suppressed learning by releasing the inhibitory neurotransmitter GABA. Functional optical-imaging experiments revealed that the APL neuron responded to both odor and electric-shock stimuli that was presented to the fly with increases of intracellular calcium and released neurotransmitter. Notably, a memory trace formed in the APL neuron by pairing odor with electric shock. This trace was detected as a reduced calcium response in the APL neuron after conditioning specifically to the trained odor. These results demonstrate a mutual suppression between the GABAergic APL neuron and olfactory learning, and emphasize the functional neuroplasticity of the GABAergic system as a result of learning.

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Figure 1: The APL neuron innervating the mushroom body neuropil is GABAergic.
Figure 2: Tissue-specific knockdown of GABA synthesis via Gad-RNAi.
Figure 3: Reducing GABA synthesis in the APL neuron enhances olfactory learning.
Figure 4: Calcium responses and neurotransmitter release of the APL neuron during odor or electric-shock stimulation.
Figure 5: The APL neuron forms a memory trace of reduced calcium response for the conditioned odor after training.

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Acknowledgements

We thank R. Axel, D. Reiff, G. Miesenböck, A. Ferrús and H. Nash for various fly stocks, L. Griffith for constructive suggestions, and W. Krause for assistance in functional optical imaging. This work was supported by US National Institutes of Health grant NS19904 to R.L.D. and the R. P. Doherty-Welch Chair in Science at the Baylor College of Medicine.

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X.L. carried out the experiments and analyzed the data. X.L. and R.L.D. designed the experiments and wrote the paper.

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Correspondence to Ronald L Davis.

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Liu, X., Davis, R. The GABAergic anterior paired lateral neuron suppresses and is suppressed by olfactory learning. Nat Neurosci 12, 53–59 (2009). https://doi.org/10.1038/nn.2235

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