Impact of Perineuronal Nets on Electrophysiology of Parvalbumin Interneurons, Principal Neurons, and Brain Oscillations: A Review.

Jereme C Wingert,Barbara A Sorg

doi:10.3389/fnsyn.2021.673210

Abstract

Perineuronal nets (PNNs) are specialized extracellular matrix structures that surround specific neurons in the brain and spinal cord, appear during critical periods of development, and restrict plasticity during adulthood. Removal of PNNs can reinstate juvenile-like plasticity or, in cases of PNN removal during early developmental stages, PNN removal extends the critical plasticity period. PNNs surround mainly parvalbumin (PV)-containing, fast-spiking GABAergic interneurons in several brain regions. These inhibitory interneurons profoundly inhibit the network of surrounding neurons via their elaborate contacts with local pyramidal neurons, and they are key contributors to gamma oscillations generated across several brain regions. Among other functions, these gamma oscillations regulate plasticity associated with learning, decision making, attention, cognitive flexibility, and working memory. The detailed mechanisms by which PNN removal increases plasticity are only beginning to be understood. Here, we review the impact of PNN removal on several electrophysiological features of their underlying PV interneurons and nearby pyramidal neurons, including changes in intrinsic and synaptic membrane properties, brain oscillations, and how these changes may alter the integration of memory-related information. Additionally, we review how PNN removal affects plasticity-associated phenomena such as long-term potentiation (LTP), long-term depression (LTD), and paired-pulse ratio (PPR). The results are discussed in the context of the role of PV interneurons in circuit function and how PNN removal alters this function.

Highlights

Perineuronal nets (PNNs) are specialized extracellular matrix structures surrounding specific neurons in the brain and spinal cord that appear during development in an experience–dependent manner (Dityatev et al, 2007; Balmer et al, 2009; Carulli et al, 2010) and restrict plasticity in adulthood
PNNs have been described as part of the extracellular reticulum for over 100 years by Golgi, the seminal study that re-launched a precipitous increase in research on PNNs was a collaboration between Dr James Fawcett, whose research focus was on the repair of spinal cord injury, and Dr Tomasso Pizzorusso, whose focus was on critical period plasticity in the visual system
We review findings from several studies that examine the impact of PNN removal on brain plasticity, including long-term potentiation (LTP), long-term depression (LTD), and paired-pulse ratio (PPR; Supplementary Table 3) followed by a discussion of how PNN removal or modifications impact brain oscillations, most notably gamma oscillations, in which PV interneurons play an integral role (Cardin et al, 2009; Sohal et al, 2009; Buzsaki and Wang, 2012; Supplementary Table 4)

Summary

Introduction

Perineuronal nets (PNNs) are specialized extracellular matrix structures surrounding specific neurons in the brain and spinal cord that appear during development in an experience–dependent manner (Dityatev et al, 2007; Balmer et al, 2009; Carulli et al, 2010) and restrict plasticity in adulthood. The majority of studies used mice and examined the hippocampus or visual cortex, and the most consistent change across all studies was the inability of fast-spiking (PV) neurons to maintain high firing frequencies after PNN removal.

Results

Conclusion