An Extracellular Perspective on CNS Maturation: Perineuronal Nets and the Control of Plasticity.

Daniela Carulli,Joost Verhaagen

doi:10.3390/ijms22052434

Abstract

During restricted time windows of postnatal life, called critical periods, neural circuits are highly plastic and are shaped by environmental stimuli. In several mammalian brain areas, from the cerebral cortex to the hippocampus and amygdala, the closure of the critical period is dependent on the formation of perineuronal nets. Perineuronal nets are a condensed form of an extracellular matrix, which surrounds the soma and proximal dendrites of subsets of neurons, enwrapping synaptic terminals. Experimentally disrupting perineuronal nets in adult animals induces the reactivation of critical period plasticity, pointing to a role of the perineuronal net as a molecular brake on plasticity as the critical period closes. Interestingly, in the adult brain, the expression of perineuronal nets is remarkably dynamic, changing its plasticity-associated conditions, including memory processes. In this review, we aimed to address how perineuronal nets contribute to the maturation of brain circuits and the regulation of adult brain plasticity and memory processes in physiological and pathological conditions.

Highlights

The ability of brain connections to change in response to experience, i.e., plasticity, is high during discrete time windows of postnatal development, called critical periods
We address the role of perineuronal nets (PNNs) in restricting critical period plasticity
Direct proof was still missing showing that it is the PNNs, rather than the other forms of extracellular matrix (ECM), that restrict plasticity at the end of the critical period, especially when taking into account that 98% of CSPGs in the central nervous system (CNS) are present in the diffuse ECM and only 2% are in PNNs [46]

Summary

Introduction

During postnatal development the continuous interaction between the individual and the environment affects the formation and refinement of neural networks. The experience-dependent shaping of neuronal connections allows individuals to best adapt to the world around them. The ability of brain connections to change in response to experience, i.e., plasticity, is high during discrete time windows of postnatal development, called critical periods. Each one with its own timings, involve distinct brain regions across development. In many species, including humans, critical periods exist for the development of sensory systems, vocal behavior, cognitive functions, and emotional traits. The development of higher functions, such as language, may depend on the proper temporal alignment of critical periods for the development of lower functions [1].

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