Holmes William R, Huwe Janice A, Williams Barbara, Rowe Michael H, Peterson Ellengene H
Department of Biological Sciences and Neuroscience Program, Ohio University, Athens, Ohio
Department of Biological Sciences and Neuroscience Program, Ohio University, Athens, Ohio.
J Neurophysiol. 2017 May 1;117(5):1969-1986. doi: 10.1152/jn.00895.2016. Epub 2017 Feb 15.
Vestibular bouton afferent terminals in turtle utricle can be categorized into four types depending on their location and terminal arbor structure: lateral extrastriolar (LES), striolar, juxtastriolar, and medial extrastriolar (MES). The terminal arbors of these afferents differ in surface area, total length, collecting area, number of boutons, number of bouton contacts per hair cell, and axon diameter (Huwe JA, Logan CJ, Williams B, Rowe MH, Peterson EH. 113: 2420-2433, 2015). To understand how differences in terminal morphology and the resulting hair cell inputs might affect afferent response properties, we modeled representative afferents from each region, using reconstructed bouton afferents. Collecting area and hair cell density were used to estimate hair cell-to-afferent convergence. Nonmorphological features were held constant to isolate effects of afferent structure and connectivity. The models suggest that all four bouton afferent types are electrotonically compact and that excitatory postsynaptic potentials are two to four times larger in MES afferents than in other afferents, making MES afferents more responsive to low input levels. The models also predict that MES and LES terminal structures permit higher spontaneous firing rates than those in striola and juxtastriola. We found that differences in spike train regularity are not a consequence of differences in peripheral terminal structure, per se, but that a higher proportion of multiple contacts between afferents and individual hair cells increases afferent firing irregularity. The prediction that afferents having primarily one bouton contact per hair cell will fire more regularly than afferents making multiple bouton contacts per hair cell has implications for spike train regularity in dimorphic and calyx afferents. Bouton afferents in different regions of turtle utricle have very different morphologies and afferent-hair cell connectivities. Highly detailed computational modeling provides insights into how morphology impacts excitability and also reveals a new explanation for spike train irregularity based on relative numbers of multiple bouton contacts per hair cell. This mechanism is independent of other proposed mechanisms for spike train irregularity based on ionic conductances and can explain irregularity in dimorphic units and calyx endings.
根据其位置和终末分支结构，海龟椭圆囊中的前庭终扣传入神经末梢可分为四种类型：外侧纹外（LES）、纹状区、近纹状区和内侧纹外（MES）。这些传入神经的终末分支在表面积、总长度、收集面积、终扣数量、每个毛细胞的终扣接触数量以及轴突直径等方面存在差异（休伊 JA、洛根 CJ、威廉姆斯 B、罗 MH、彼得森 EH。113: 2420 - 2433，2015）。为了了解终末形态差异以及由此产生的毛细胞输入如何影响传入神经的反应特性，我们使用重建的终扣传入神经，对每个区域的代表性传入神经进行了建模。收集面积和毛细胞密度用于估计毛细胞与传入神经的汇聚情况。非形态学特征保持恒定，以分离传入神经结构和连接性的影响。模型表明，所有四种终扣传入神经类型在电紧张方面都是紧密的，并且兴奋性突触后电位在 MES 传入神经中比在其他传入神经中要大两到四倍，这使得 MES 传入神经对低输入水平更敏感。模型还预测，MES 和 LES 终末结构允许比纹状区和近纹状区更高的自发放电率。我们发现，放电序列规律性的差异本身并非外周终末结构差异的结果，而是传入神经与单个毛细胞之间多个接触的比例更高会增加传入神经放电的不规则性。每个毛细胞主要有一个终扣接触的传入神经比每个毛细胞有多个终扣接触的传入神经放电更规律这一预测，对双形和花萼传入神经的放电序列规律性具有启示意义。海龟椭圆囊不同区域的终扣传入神经具有非常不同的形态以及传入神经 - 毛细胞连接性。高度详细的计算建模为形态学如何影响兴奋性提供了见解，并且还基于每个毛细胞多个终扣接触的相对数量，揭示了对放电序列不规则性的一种新解释。这种机制独立于基于离子电导提出的其他放电序列不规则性机制，并且可以解释双形单元和花萼末梢中的不规则性。
