Graduate School of Systemic Neurosciences, Ludwig-Maximilians-Universität, Munich, Germany.
Bernstein Center for Computational Neuroscience, Munich, Germany.
PLoS Comput Biol. 2019 Jan 2;15(1):e1006666. doi: 10.1371/journal.pcbi.1006666. eCollection 2019 Jan.
The release of neurotransmitters from synapses obeys complex and stochastic dynamics. Depending on the recent history of synaptic activation, many synapses depress the probability of releasing more neurotransmitter, which is known as synaptic depression. Our understanding of how synaptic depression affects the information efficacy, however, is limited. Here we propose a mathematically tractable model of both synchronous spike-evoked release and asynchronous release that permits us to quantify the information conveyed by a synapse. The model transits between discrete states of a communication channel, with the present state depending on many past time steps, emulating the gradual depression and exponential recovery of the synapse. Asynchronous and spontaneous releases play a critical role in shaping the information efficacy of the synapse. We prove that depression can enhance both the information rate and the information rate per unit energy expended, provided that synchronous spike-evoked release depresses less (or recovers faster) than asynchronous release. Furthermore, we explore the theoretical implications of short-term synaptic depression adapting on longer time scales, as part of the phenomenon of metaplasticity. In particular, we show that a synapse can adjust its energy expenditure by changing the dynamics of short-term synaptic depression without affecting the net information conveyed by each successful release. Moreover, the optimal input spike rate is independent of the amplitude or time constant of synaptic depression. We analyze the information efficacy of three types of synapses for which the short-term dynamics of both synchronous and asynchronous release have been experimentally measured. In hippocampal autaptic synapses, the persistence of asynchronous release during depression cannot compensate for the reduction of synchronous release, so that the rate of information transmission declines with synaptic depression. In the calyx of Held, the information rate per release remains constant despite large variations in the measured asynchronous release rate. Lastly, we show that dopamine, by controlling asynchronous release in corticostriatal synapses, increases the synaptic information efficacy in nucleus accumbens.
神经递质从突触释放遵循复杂的随机动力学。根据突触激活的近期历史，许多突触会降低释放更多神经递质的概率，这被称为突触抑制。然而，我们对突触抑制如何影响信息功效的理解是有限的。在这里，我们提出了一个可同时处理同步尖峰诱发释放和异步释放的数学上易于处理的模型，该模型可以量化突触传递的信息。该模型在通信通道的离散状态之间转换，当前状态取决于许多过去的时间步长，模拟了突触的逐渐抑制和指数恢复。异步和自发释放对突触信息功效的形成起着至关重要的作用。我们证明，只要同步尖峰诱发释放的抑制作用（或恢复速度）比异步释放慢（或恢复速度），抑制作用就可以提高信息率和单位能量消耗的信息率。此外，我们还探索了作为超可塑性现象一部分的短期突触抑制在较长时间尺度上的理论意义。特别是，我们表明，突触可以通过改变短期突触抑制的动力学来调整其能量消耗，而不会影响每个成功释放所传递的净信息。此外，最优输入尖峰率与突触抑制的幅度或时间常数无关。我们分析了三种类型的突触的信息功效，对于这三种类型的突触，同步和异步释放的短期动力学已经在实验中进行了测量。在海马体的自动突触中，抑制期间异步释放的持续存在不能弥补同步释放的减少，因此信息传输率随突触抑制而下降。在 Held 触须中，尽管测量到的异步释放率有很大变化，但每个释放的信息率保持不变。最后，我们表明，多巴胺通过控制皮质纹状体突触中的异步释放，增加了伏隔核中的突触信息功效。
