Lensjø Kristian Kinden, Lepperød Mikkel Elle, Dick Gunnar, Hafting Torkel, Fyhn Marianne
Department of Biosciences.
Center for Integrative Neuroplasticity, University of Oslo, 0370 Oslo, Norway.
J Neurosci. 2017 Feb 1;37(5):1269-1283. doi: 10.1523/JNEUROSCI.2504-16.2016. Epub 2016 Dec 30.
Perineuronal nets (PNNs) are extracellular matrix structures mainly enwrapping parvalbumin-expressing inhibitory neurons. The assembly of PNNs coincides with the end of the period of heightened visual cortex plasticity in juveniles, whereas removal of PNNs in adults reopens for plasticity. The mechanisms underlying this phenomenon remain elusive. We have used chronic electrophysiological recordings to investigate accompanying electrophysiological changes to activity-dependent plasticity and we report on novel mechanisms involved in both induced and critical period plasticity. By inducing activity-dependent plasticity in the visual cortex of adult rats while recording single unit and population activity, we demonstrate that PNN removal alters the balance between inhibitory and excitatory spiking activity directly. Without PNNs, inhibitory activity was reduced, whereas spiking variability was increased as predicted in a simulation with a Brunel neural network. Together with a shift in ocular dominance and large effects on unit activity during the first 48 h of monocular deprivation (MD), we show that PNN removal resets the neural network to an immature, juvenile state. Furthermore, in PNN-depleted adults as well as in juveniles, MD caused an immediate potentiation of gamma activity, suggesting a novel mechanism initiating activity-dependent plasticity and driving the rapid changes in unit activity.
Emerging evidence suggests a role for perineuronal nets (PNNs) in learning and regulation of plasticity, but the underlying mechanisms remain unresolved. Here, we used chronic in vivo extracellular recordings to investigate how removal of PNNs opens for plasticity and how activity-dependent plasticity affects neural activity over time. PNN removal caused reduced inhibitory activity and reset the network to a juvenile state. Experimentally induced activity-dependent plasticity by monocular deprivation caused rapid changes in single unit activity and a remarkable potentiation of gamma oscillations. Our results demonstrate how PNNs may be involved directly in stabilizing the neural network. Moreover, the immediate potentiation of gamma activity after plasticity onset points to potential new mechanisms for the initiation of activity-dependent plasticity.
神经周网（PNNs）是细胞外基质结构，主要包裹表达小白蛋白的抑制性神经元。神经周网的组装与幼年视觉皮层可塑性增强期的结束同时发生，而在成体中去除神经周网则会重新开启可塑性。这一现象背后的机制仍不清楚。我们使用慢性电生理记录来研究与活动依赖可塑性相关的电生理变化，并报告了诱导可塑性和关键期可塑性中涉及的新机制。通过在成年大鼠视觉皮层诱导活动依赖可塑性的同时记录单个神经元和群体活动，我们证明去除神经周网会直接改变抑制性和兴奋性放电活动之间的平衡。没有神经周网时，抑制性活动减少，而放电变异性增加，这与布鲁内尔神经网络模拟的预测一致。结合眼优势的改变以及单眼剥夺（MD）最初48小时内对神经元活动的显著影响，我们表明去除神经周网会将神经网络重置为不成熟的幼年状态。此外，在去除神经周网的成年动物以及幼年动物中，MD都会立即增强γ活动，这表明存在一种启动活动依赖可塑性并驱动神经元活动快速变化的新机制。
新出现的证据表明神经周网（PNNs）在学习和可塑性调节中发挥作用，但其潜在机制仍未解决。在这里，我们使用慢性体内细胞外记录来研究去除神经周网如何开启可塑性，以及活动依赖可塑性如何随时间影响神经活动。去除神经周网会导致抑制性活动减少，并将网络重置为幼年状态。通过单眼剥夺实验诱导的活动依赖可塑性会导致单个神经元活动快速变化以及γ振荡显著增强。我们的结果证明了神经周网可能如何直接参与稳定神经网络。此外，可塑性开始后γ活动的立即增强指向了活动依赖可塑性启动的潜在新机制。
