Krächan Elisa G, Fischer Alexander U, Franke Jürgen, Friauf Eckhard
Animal Physiology Group, Department of Biology, University of Kaiserslautern, D-67663, Kaiserslautern, Germany.
Chair for Applied Mathematical Statistics, Department of Mathematics, University of Kaiserslautern, D-67663, Kaiserslautern, Germany.
J Physiol. 2017 Feb 1;595(3):839-864. doi: 10.1113/JP272799. Epub 2016 Dec 2.
Auditory brainstem neurons involved in sound source localization are equipped with several morphological and molecular features that enable them to compute interaural level and time differences. As sound source localization works continually, synaptic transmission between these neurons should be reliable and temporally precise, even during sustained periods of high-frequency activity. Using patch-clamp recordings in acute brain slices, we compared synaptic reliability and temporal precision in the seconds-minute range between auditory and two types of hippocampal synapses; the latter are less confronted with temporally precise high-frequency transmission than the auditory ones. We found striking differences in synaptic properties (e.g. continually high quantal content) that allow auditory synapses to reliably release vesicles at much higher rate than their hippocampal counterparts. Thus, they are indefatigable and also in a position to transfer information with exquisite temporal precision and their performance appears to be supported by very efficient replenishment mechanisms.
At early stations of the auditory pathway, information is encoded by precise signal timing and rate. Auditory synapses must maintain the relative timing of events with submillisecond precision even during sustained and high-frequency stimulation. In non-auditory brain regions, e.g. telencephalic ones, synapses are activated at considerably lower frequencies. Central to understanding the heterogeneity of synaptic systems is the elucidation of the physical, chemical and biological factors that determine synapse performance. In this study, we used slice recordings from three synapse types in the mouse auditory brainstem and hippocampus. Whereas the auditory brainstem nuclei experience high-frequency activity in vivo, the hippocampal circuits are activated at much lower frequencies. We challenged the synapses with sustained high-frequency stimulation (up to 200 Hz for 60 s) and found significant performance differences. Our results show that auditory brainstem synapses differ considerably from their hippocampal counterparts in several aspects, namely resistance to synaptic fatigue, low failure rate and exquisite temporal precision. Their high-fidelity performance supports the functional demands and appears to be due to the large size of the readily releasable pool and a high release probability, which together result in a high quantal content. In conjunction with very efficient vesicle replenishment mechanisms, these properties provide extremely rapid and temporally precise signalling required for neuronal communication at early stations of the auditory system, even during sustained activation in the minute range.
参与声源定位的听觉脑干神经元具有多种形态和分子特征，使它们能够计算双耳声级和时间差异。由于声源定位持续进行，即使在高频活动的持续期间，这些神经元之间的突触传递也应该可靠且在时间上精确。在急性脑片中使用膜片钳记录，我们比较了听觉突触与两种海马突触在秒到分钟范围内的突触可靠性和时间精度；与听觉突触相比，后两者较少面临时间精确的高频传递。我们发现突触特性存在显著差异（例如持续高量子含量），这使得听觉突触能够以比海马突触更高的速率可靠地释放囊泡。因此，它们不知疲倦，并且能够以极高的时间精度传递信息，其性能似乎得到非常有效的补充机制的支持。
在听觉通路的早期阶段，信息通过精确的信号定时和速率进行编码。即使在持续高频刺激期间，听觉突触也必须以亚毫秒精度维持事件的相对定时。在非听觉脑区，如端脑区域，突触以相当低的频率被激活。理解突触系统异质性的核心在于阐明决定突触性能的物理、化学和生物学因素。在本研究中，我们使用了来自小鼠听觉脑干和海马体中三种突触类型的脑片记录。听觉脑干核在体内经历高频活动，而海马回路以低得多的频率被激活。我们用持续高频刺激（高达200Hz持续60秒）挑战突触，发现了显著的性能差异。我们的结果表明，听觉脑干突触在几个方面与海马突触有很大不同，即对突触疲劳的抵抗力、低失败率和极高的时间精度。它们的高保真性能支持了功能需求，似乎是由于易于释放池的大尺寸和高释放概率，这共同导致了高量子含量。结合非常有效的囊泡补充机制，这些特性提供了听觉系统早期神经元通信所需的极其快速和时间精确的信号传递，即使在分钟范围内持续激活期间也是如此。
