Group for Neural Theory, LNC INSERM Unité 960, Département d'Études Cognitives, École Normale Supérieure, PSL Research University, Paris, France.
Centre de recherche sur l'inflammation UMR 1149, INSERM-Université Paris Diderot, Paris, France.
J Neurophysiol. 2020 May 1;123(5):1583-1599. doi: 10.1152/jn.00402.2019. Epub 2020 Feb 12.
Nervous system maturation occurs on multiple levels-synaptic, circuit, and network-at divergent timescales. For example, many synaptic properties mature gradually, whereas emergent network dynamics can change abruptly. Here we combine experimental and theoretical approaches to investigate a sudden transition in spontaneous and sensory evoked thalamocortical activity necessary for the development of vision. Inspired by in vivo measurements of timescales and amplitudes of synaptic currents, we extend the Wilson and Cowan model to take into account the relative onset timing and amplitudes of inhibitory and excitatory neural population responses. We study this system as these parameters are varied within amplitudes and timescales consistent with developmental observations to identify the bifurcations of the dynamics that might explain the network behaviors in vivo. Our findings indicate that the inhibitory timing is a critical determinant of thalamocortical activity maturation; a gradual decay of the ratio of inhibitory to excitatory onset time drives the system through a bifurcation that leads to a sudden switch of the network spontaneous activity from high-amplitude oscillations to a nonoscillatory active state. This switch also drives a change from a threshold bursting to linear response to transient stimuli, also consistent with in vivo observation. Thus we show that inhibitory timing is likely critical to the development of network dynamics and may underlie rapid changes in activity without similarly rapid changes in the underlying synaptic and cellular parameters. Relying on a generalization of the Wilson-Cowan model, which allows a solid analytic foundation for the understanding of the link between maturation of inhibition and network dynamics, we propose a potential explanation for the role of developing excitatory/inhibitory synaptic delays in mediating a sudden switch in thalamocortical visual activity preceding vision onset.
神经系统的成熟发生在多个层次上——突触、回路和网络——在不同的时间尺度上。例如,许多突触特性逐渐成熟,而新兴的网络动态变化可能会突然发生。在这里,我们结合实验和理论方法来研究视知觉发展所必需的自发和感觉诱发的丘脑-皮层活动中的突然转变。受体内突触电流的时间尺度和幅度的测量启发,我们扩展了威尔逊和考恩模型,以考虑抑制性和兴奋性神经元群体反应的相对起始时间和幅度。我们研究了这个系统,因为这些参数在与发育观察一致的幅度和时间尺度内变化,以确定可能解释体内网络行为的动力学分岔。我们的发现表明,抑制性时间是丘脑-皮层活动成熟的关键决定因素;抑制性到兴奋性起始时间比的逐渐衰减驱动系统通过分岔,导致网络自发活动从高幅度振荡突然转变为非振荡活动状态。这种转变还导致从阈值爆发到对瞬态刺激的线性响应的转变,这也与体内观察一致。因此,我们表明抑制性时间可能对网络动力学的发展至关重要,并且可能在没有类似的突触和细胞参数快速变化的情况下引起活动的快速变化。基于威尔逊-考恩模型的推广,该模型为理解抑制成熟与网络动力学之间的联系提供了坚实的分析基础,我们提出了一个潜在的解释,即发育中的兴奋性/抑制性突触延迟在介导视知觉发生前丘脑-皮层视觉活动的突然转变中的作用。