Group for Neural Theory, Laboratoire de Neurosciences Cognitives Computationnelles, Département d'Études Cognitives, École Normale Supérieure, INSERM U960, PSL University, Paris, France.
PLoS Comput Biol. 2019 Mar 21;15(3):e1006893. doi: 10.1371/journal.pcbi.1006893. eCollection 2019 Mar.
Neural activity in awake behaving animals exhibits a vast range of timescales that can be several fold larger than the membrane time constant of individual neurons. Two types of mechanisms have been proposed to explain this conundrum. One possibility is that large timescales are generated by a network mechanism based on positive feedback, but this hypothesis requires fine-tuning of the strength or structure of the synaptic connections. A second possibility is that large timescales in the neural dynamics are inherited from large timescales of underlying biophysical processes, two prominent candidates being intrinsic adaptive ionic currents and synaptic transmission. How the timescales of adaptation or synaptic transmission influence the timescale of the network dynamics has however not been fully explored. To address this question, here we analyze large networks of randomly connected excitatory and inhibitory units with additional degrees of freedom that correspond to adaptation or synaptic filtering. We determine the fixed points of the systems, their stability to perturbations and the corresponding dynamical timescales. Furthermore, we apply dynamical mean field theory to study the temporal statistics of the activity in the fluctuating regime, and examine how the adaptation and synaptic timescales transfer from individual units to the whole population. Our overarching finding is that synaptic filtering and adaptation in single neurons have very different effects at the network level. Unexpectedly, the macroscopic network dynamics do not inherit the large timescale present in adaptive currents. In contrast, the timescales of network activity increase proportionally to the time constant of the synaptic filter. Altogether, our study demonstrates that the timescales of different biophysical processes have different effects on the network level, so that the slow processes within individual neurons do not necessarily induce slow activity in large recurrent neural networks.
在清醒动物的行为中,神经活动表现出广泛的时间尺度,这些时间尺度可以比单个神经元的膜时间常数大几个数量级。有两种机制被提出来解释这个难题。一种可能性是,大时间尺度是由基于正反馈的网络机制产生的,但这种假设需要精细调整突触连接的强度或结构。另一种可能性是,神经动力学中的大时间尺度是从潜在的生物物理过程的大时间尺度中继承而来的,两个突出的候选者是内在适应离子电流和突触传递。然而,适应或突触传递的时间尺度如何影响网络动力学的时间尺度尚未得到充分探索。为了解决这个问题,我们在这里分析了具有额外自由度的随机连接的兴奋性和抑制性单元的大型网络,这些自由度对应于适应或突触滤波。我们确定了系统的平衡点、它们对扰动的稳定性以及相应的动力学时间尺度。此外,我们应用动力平均场理论来研究在波动状态下的活动的时间统计,并研究适应和突触时间尺度如何从单个单元传递到整个群体。我们的总体发现是,单个神经元中的突触滤波和适应在网络层面上有非常不同的影响。出乎意料的是,宏观网络动力学不会继承自适应电流中存在的大时间尺度。相反,网络活动的时间尺度与突触滤波器的时间常数成正比地增加。总之,我们的研究表明,不同生物物理过程的时间尺度对网络层面有不同的影响,因此单个神经元内的慢过程不一定会导致大递归神经网络中的慢活动。