GABAergic Local Interneurons Shape Female Fruit Fly Response to Mating Songs
GABAergic Local Interneurons Shape Female Fruit Fly Response to Mating Songs
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DOI：
10.1523/jneurosci.3644-17.2018
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发表时间：
2018-05
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影响因子：
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通讯作者：
Daichi Yamada;H. Ishimoto;Xiaodong Li;T. Kohashi;Yuki Ishikawa;Azusa Kamikouchi
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文献类型：
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作者：
Daichi Yamada;H. Ishimoto;Xiaodong Li;T. Kohashi;Yuki Ishikawa;Azusa Kamikouchi
许多动物使用声音信号来吸引潜在的交配伙伴。在果蝇(果蝇)中，求偶脉冲歌曲有一个物种特定的脉冲间隔(IPI)，可以激活交配。尽管苍蝇脑中的一系列听觉神经元对IPIs表现出不同的调谐模式，但尚不清楚每个神经元的反应是如何调谐的。在这里，我们研究了调节触角机械感觉和运动中枢(AMMC)-B1神经元活动的神经回路，这是传递歌曲信息的兴奋性神经通路中的关键二级听觉神经元。通过对雌性果蝇进行钙离子成像，我们发现在AMMC-B1神经元中观察到的IPI选择性不同于上游听觉感觉神经元[约翰斯顿器官(JO)-B]。选择性地敲除AMMC-B1神经元中的GABAA受体亚基增强了它们对短IPI的反应，这表明GABA抑制了AMMC-B1在这些IPI上的活动。连接图谱确定了两个与AMMC-B1和JO-B突触的GABA能局部中间神经元。结合钙离子成像和神经元沉默显示，这些局部中间神经元，AMMC-LN和AMMC-B2，在15ms IPI时形成AMMC-B1神经元的反应模式。神经元沉默研究进一步表明，两个GABA能局部中间神经元都抑制了果蝇对人工脉冲歌曲的行为反应，特别是那些具有15ms IPI的果蝇。总之，我们确定了一个含有两个GABA能局部中间神经元的电路，它影响了歌曲传递路径中AMMC-B1神经元的时间调谐和对求爱歌曲的行为反应。我们的发现表明，前馈抑制通路调节雌性果蝇对求偶脉冲歌曲的行为反应。为了了解大脑如何检测声音元素之间的时间间隔，我们研究了雌性黑腹果蝇传递特定物种求爱歌曲信息的神经路径。我们证明了听觉感觉神经元到关键的次级听觉神经元--触角机械感觉和运动中枢(AMMC)-B1的信号传递是在SONG传递通路中产生神经元的时间间隔选择性的第一步。两个GABA能局部中间神经元通过接受听觉输入，进而对AMMC-B1神经元提供前馈抑制，从而形成AMMC-B1神经元的间期选择性。此外，这些GABA能局部中间神经元以间隔依赖的方式抑制歌唱反应行为。我们的结果为神经回路基础提供了新的见解，以调节神经元和行为对特定物种的交流声音的反应。
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 GABAA 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 15 ms 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 15 ms 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. SIGNIFICANCE STATEMENT To understand how the brain detects time intervals between sound elements, we studied the neural pathway that relays species-specific courtship song information in female Drosophila melanogaster. We demonstrate that the signal transmission from auditory sensory neurons to key secondary auditory neurons antennal mechanosensory and motor center (AMMC)-B1 is the first-step to generate time interval selectivity of neurons in the song relay pathway. Two GABAergic local interneurons are suggested to shape the interval selectivity of AMMC-B1 neurons by receiving auditory inputs and in turn providing feedforward inhibition onto AMMC-B1 neurons. Furthermore, these GABAergic local interneurons suppress the song response behavior in an interval-dependent manner. Our results provide new insights into the neural circuit basis to adjust neuronal and behavioral responses to a species-specific communication sound.