Heil Peter, Neubauer Heinrich, Irvine Dexter R F, Brown Mel
Leibniz Institute for Neurobiology, 39118 Magdeburg, Germany.
J Neurosci. 2007 Aug 1;27(31):8457-74. doi: 10.1523/JNEUROSCI.1512-07.2007.
In several sensory systems, the conversion of the representation of stimuli from graded membrane potentials into stochastic spike trains is performed by ribbon synapses. In the mammalian auditory system, the spiking characteristics of the vast majority of primary afferent auditory-nerve (AN) fibers are determined primarily by a single ribbon synapse in a single inner hair cell (IHC), and thus provide a unique window into the operation of the synapse. Here, we examine the distributions of interspike intervals (ISIs) of cat AN fibers under conditions when the IHC membrane potential can be considered constant and the processes generating AN fiber activity can be considered stationary, namely in the absence of auditory stimulation. Such spontaneous activity is commonly thought to result from an excitatory Poisson point process modified by the refractory properties of the fiber, but here we show that this cannot be the case. Rather, the ISI distributions are one to two orders of magnitude better and very accurately described as a result of a homogeneous stochastic process of excitation (transmitter release events) in which the distribution of interevent times is a mixture of an exponential and a gamma distribution with shape factor 2, both with the same scale parameter. Whereas the scale parameter varies across fibers, the proportions of exponentially and gamma distributed intervals in the mixture, and the refractory properties, can be considered constant. This suggests that all of the ribbon synapses operate in a similar manner, possibly just at different rates. Our findings also constitute an essential step toward a better understanding of the spike-train representation of time-varying stimuli initiated at this synapse, and thus of the fundamentals of temporal coding in the auditory pathway.
在多个感觉系统中，刺激表征从分级膜电位转换为随机脉冲序列是由带状突触完成的。在哺乳动物听觉系统中，绝大多数初级传入听觉神经（AN）纤维的放电特性主要由单个内毛细胞（IHC）中的单个带状突触决定，因此为了解突触的运作提供了一个独特的窗口。在这里，我们研究了在IHC膜电位可视为恒定且产生AN纤维活动的过程可视为稳定的条件下，即无听觉刺激时，猫AN纤维的峰峰间隔（ISI）分布。这种自发活动通常被认为是由纤维的不应期特性修正的兴奋性泊松点过程引起的，但我们在此表明情况并非如此。相反，ISI分布用一个均匀的激发随机过程（递质释放事件）能得到更好且非常准确的描述，其中事件间时间的分布是指数分布和形状因子为2的伽马分布的混合，两者具有相同的尺度参数。虽然尺度参数在不同纤维间变化，但混合物中指数分布和伽马分布间隔的比例以及不应期特性可视为恒定。这表明所有带状突触的运作方式相似，可能只是速率不同。我们的发现也朝着更好地理解在此突触起始的随时间变化刺激的脉冲序列表征迈出了重要一步，从而有助于理解听觉通路中时间编码的基本原理。
