Department of Cell Physiology, Nagoya University, Graduate School of Medicine, Nagoya, 466-8550, Japan.
Department of Cell Physiology, Nagoya University, Graduate School of Medicine, Nagoya, 466-8550, Japan
J Neurosci. 2021 Oct 27;41(43):8904-8916. doi: 10.1523/JNEUROSCI.0884-21.2021. Epub 2021 Sep 13.
GABAergic inhibition in neurons plays a critical role in determining the output of neural circuits. Neurons in avian nucleus magnocellularis (NM) use several tonotopic-region-dependent specializations to relay the timing information of sound in the auditory nerve to higher auditory nuclei. Previously, we showed that feedforward GABAergic inhibition in NM has a different dependence on the level of auditory nerve activity, with the low-frequency region having a low-threshold and linear relationship, while the high-frequency region has a high-threshold and step-like relationship. However, it remains unclear how the GABAergic synapses are tonotopically regulated and interact with other specializations of NM neurons. In this study, we examined GABAergic transmission in the NM of chickens of both sexes and explored its contributions to the temporal coding of sound at each tonotopic region. We found that the number and size of unitary GABAergic currents and their reversal potential were finely tuned at each tonotopic region in the NM. At the lower-frequency region, unitary GABAergic currents were larger in number but smaller in size. In addition, their reversal potential was close to the resting potential of neurons, which enabled reliable inhibition despite the smaller potassium conductance. At the higher-frequency region, on the other hand, unitary GABAergic currents were fewer, larger, and highly depolarizing, which enabled powerful inhibition via activating the large potassium conductance. Thus, we propose that GABAergic synapses are coordinated with the characteristics of excitatory synapses and postsynaptic neurons, ensuring the temporal coding for wide frequency and intensity ranges. We found in avian cochlear nucleus that the number and size of unitary GABAergic inputs differed among tonotopic regions and correlated to respective excitatory inputs; it was larger in number but smaller in size for neurons tuned to lower-frequency sound. Furthermore, GABAergic reversal potential also differed among the regions in accordance with the size of Kv1 current; it was less depolarized in the lower-frequency neurons with smaller Kv1 current. These differentiations of GABAergic transmission maximized the effects of inhibition at each tonotopic region, ensuring precise and reliable temporal coding across frequencies and intensities. Our results emphasize the importance of optimizing characteristics of GABAergic transmission within individual neurons for proper neural circuit function.
神经元中的 GABA 能抑制在确定神经回路的输出方面起着关键作用。鸟类中脑Magnocellularis 核（NM）的神经元使用几种与音调有关的区域特异性来将听觉神经中声音的时间信息传递到更高的听觉核。以前，我们发现 NM 中的前馈 GABA 能抑制对听觉神经活动水平有不同的依赖性，低频区具有低阈值和线性关系，而高频区具有高阈值和阶跃样关系。然而，目前尚不清楚 GABA 能突触如何在音调上受到调节以及与 NM 神经元的其他特异性相互作用。在这项研究中，我们检查了两性鸡的 NM 中的 GABA 能传递，并探讨了其对每个音调区域声音的时间编码的贡献。我们发现，NM 中的每个音调区域的 GABA 能突触的数量和大小以及它们的反转电位都被精细地调节。在低频区，单位 GABA 能电流的数量较大，但幅度较小。此外，它们的反转电位接近神经元的静息电位，尽管钾电导较小，但仍能实现可靠的抑制。另一方面，在高频区，单位 GABA 能电流较少，幅度较大且高度去极化，这使得通过激活大的钾电导来实现强大的抑制。因此，我们提出 GABA 能突触与兴奋性突触和突触后神经元的特性相协调，确保了广泛的频率和强度范围内的时间编码。我们在鸟类耳蜗核中发现，单位 GABA 能输入的数量和大小在音调区域之间存在差异，并与各自的兴奋性输入相关；对于调谐到低频声音的神经元，其数量较大，但幅度较小。此外，GABA 能反转电位也根据 Kv1 电流的大小在区域之间有所不同；在 Kv1 电流较小的低频神经元中，它的去极化程度较小。这些 GABA 能传递的差异使每个音调区域的抑制效果最大化，确保了在频率和强度范围内的精确和可靠的时间编码。我们的研究结果强调了在单个神经元中优化 GABA 能传递特性对于适当的神经回路功能的重要性。
