Journal
JOURNAL OF NEUROSCIENCE
Volume 38, Issue 18, Pages 4329-4347Publisher
SOC NEUROSCIENCE
DOI: 10.1523/JNEUROSCI.3644-17.2018
Keywords
auditory neurons; courtship song; Drosophila melanogaster; feedforward inhibition; neural circuit
Categories
Funding
- Ministry of Education, Culture, Sports, Science, and Technology, Japan [16H04655, 25115007, 17K19450, 15K07147, 26870264, 15J04760]
- Inamori Foundation, Japan
- Grants-in-Aid for Scientific Research [25115007, 15J04760, 26870264, 17K19450, 16H04655, 15K07147] Funding Source: KAKEN
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Many animals use acoustic signals to attract a potential mating partner. In fruit flies (Drosophila melanogaster), the courtship pulse song has a species-specific interpulse interval (IPI) that activates mating. Although a series of auditory neurons in the fly brain exhibit different tuning patterns to IPIs, it is unclear how the response of each neuron is tuned. Here, we studied the neural circuitry regulating the activity of antennal mechanosensory and motor center (AMMC)-B1 neurons, key secondary auditory neurons in the excitatory neural pathway that relay song information. By performing Ca2+ imaging in female flies, we found that the IPI selectivity observed in AMMC-B1 neurons differs from that of upstream auditory sensory neurons [Johnston's organ (JO)-B]. Selective knock-down of a GABA(A) receptor subunit in AMMC-B1 neurons increased their response to short IPIs, suggesting that GABA suppresses AMMC-B1 activity at these IPIs. Connection mapping identified two GABAergic local interneurons that synapse with AMMC-B1 and JO-B. Ca2(+) imaging combined with neuronal silencing revealed that these local interneurons, AMMC-LN and AMMC-B2, shape the response pattern of AMMC-B1 neurons at a 15ms IPI. Neuronal silencing studies further suggested that both GABAergic local interneurons suppress the behavioral response to artificial pulse songs in flies, particularly those with a 15ms IPI. Altogether, we identified a circuit containing two GABAergic local interneurons that affects the temporal tuning of AMMC-B1 neurons in the song relay pathway and the behavioral response to the courtship song. Our findings suggest that feedforward inhibitory pathways adjust the behavioral response to courtship pulse songs in female flies.
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