Bernstein Center for Computational Neuroscience Berlin, 10115 Berlin, Germany.
Institute for Theoretical Biology, Department of Biology, Humboldt Universität zu Berlin, 10115 Berlin, Germany.
Proc Natl Acad Sci U S A. 2022 Jun 7;119(23):e2118448119. doi: 10.1073/pnas.2118448119. Epub 2022 Jun 3.
During vocal exchanges, hearing specific auditory signals can provoke vocal responses or suppress vocalizations to avoid interference. These abilities result in the widespread phenomenon of vocal turn taking, yet little is known about the neural circuitry that regulates the input-dependent timing of vocal replies. Previous work in vocally interacting zebra finches has highlighted the importance of premotor inhibition for precisely timed vocal output. By developing physiologically constrained mathematical models, we derived circuit mechanisms based on feedforward inhibition that enable both the temporal modulation of vocal premotor drive as well as auditory suppression of vocalization during listening. Extracellular recordings in HVC during the listening phase confirmed the presence of auditory-evoked response patterns in putative inhibitory interneurons, along with corresponding signatures of auditory-evoked activity suppression. Further, intracellular recordings of identified neurons projecting to HVC from the upstream sensorimotor nucleus, nucleus interfacialis (NIf), shed light on the timing of auditory inputs to this network. The analysis of incrementally time-lagged interactions between auditory and premotor activity in the model resulted in the prediction of a window of auditory suppression, which could be, in turn, verified in behavioral data. A phasic feedforward inhibition model consistently explained the experimental results. This mechanism highlights a parsimonious and generalizable principle for how different driving inputs (vocal and auditory related) can be integrated in a single sensorimotor circuit to regulate two opposing vocal behavioral outcomes: the controlled timing of vocal output or the suppression of overlapping vocalizations.
在声音交流中，听觉特定的声音信号可以引发声音反应或抑制发声以避免干扰。这些能力导致了广泛存在的声音轮流现象，但对于调节输入相关声音反应时间的神经回路知之甚少。之前在相互发声的斑马雀中的研究强调了前运动抑制对于精确定时发声输出的重要性。通过开发受生理限制的数学模型，我们基于前馈抑制推导出了电路机制，这些机制既能调节发声前运动驱动的时间调制，也能在聆听时抑制发声。在聆听阶段的 HVC 中的细胞外记录证实了在假定的抑制性中间神经元中存在听觉诱发的反应模式，以及听觉诱发活动抑制的相应特征。此外，对来自上游感觉运动核、核间界面（NIf）投射到 HVC 的已识别神经元进行细胞内记录，揭示了听觉输入到该网络的时间。对模型中听觉和前运动活动的递增时间延迟相互作用的分析导致了听觉抑制窗口的预测，反过来又可以在行为数据中得到验证。一个阶段性的前馈抑制模型一致地解释了实验结果。这种机制突出了一种简洁且可推广的原则，即不同的驱动输入（与声音相关的听觉和声音）如何可以在单个感觉运动回路中整合，以调节两种相反的发声行为结果：发声输出的受控定时或重叠发声的抑制。
