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Review
. 2022 Apr 26:16:875873.
doi: 10.3389/fncir.2022.875873. eCollection 2022.

Non-Cell-Autonomous Factors Implicated in Parvalbumin Interneuron Maturation and Critical Periods

Rachel Gibel-Russo  1 , David Benacom  1 , Ariel A Di Nardo  1
Affiliations
Review

Non-Cell-Autonomous Factors Implicated in Parvalbumin Interneuron Maturation and Critical Periods

Rachel Gibel-Russo et al. Front Neural Circuits. .

Abstract

From birth to adolescence, the brain adapts to its environmental stimuli through structural and functional remodeling of neural circuits during critical periods of heightened plasticity. They occur across modalities for proper sensory, motor, linguistic, and cognitive development. If they are disrupted by early-life adverse experiences or genetic deficiencies, lasting consequences include behavioral changes, physiological and cognitive deficits, or psychiatric illness. Critical period timing is orchestrated not only by appropriate neural activity but also by a multitude of signals that participate in the maturation of fast-spiking parvalbumin interneurons and the consolidation of neural circuits. In this review, we describe the various signaling factors that initiate critical period onset, such as BDNF, SPARCL1, or OTX2, which originate either from local neurons or glial cells or from extracortical sources such as the choroid plexus. Critical period closure is established by signals that modulate extracellular matrix and myelination, while timing and plasticity can also be influenced by circadian rhythms and by hormones and corticosteroids that affect brain oxidative stress levels or immune response. Molecular outcomes include lasting epigenetic changes which themselves can be considered signals that shape downstream cross-modal critical periods. Comprehensive knowledge of how these signals and signaling factors interplay to influence neural mechanisms will help provide an inclusive perspective on the effects of early adversity and developmental defects that permanently change perception and behavior.

Keywords: astrocyctes; epigenetics; homeoprotein; microglia; oligodedrocytes; parvalbumin (PV); perineuronal net (PNN).

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Summary of non-cell-autonomous factors involved in FS-PV cell physiology. (1) Dendrites: Non-cell-autonomous factors stabilize synapse number and strength of sensory inputs that drive CP onset and FS-PV cell synapse maturation. (2) Signaling pathways: Non-cell-autonomous factors bind specific receptors or glycosaminoglycan motifs in PNNs. BDNF-TRKB triggers activity-dependent pathways. OTX2 binding to CSPGs leads to cell internalization and translocation to the nucleus. SEMA3A interacts with CSPGs and stabilizes synapses on FS-PV cell soma. (3) PNN physiology: PNNs develop around FS-PV cells during CP, providing neuroprotection against oxidative damage induced by the fast-spiking activity of FS-PV cells. PNNs stabilize neural networks and limit synapses formation. Secreted ECM enzymes provide turnover for PNN dynamics, while other non-cell-autonomous factors participate in PNN stabilization. (4) Epigenetics: During the CP, the FS-PV cell transcriptome is regulated in response to the cellular environment via histone PTMs and DNA methylation. OTX2 affects gene expression and chromatin conformation in part through transcription regulation Gadd45b/g. (5) Axon: FS-PV cell outputs on principal cells generate gamma rhythms. Non-cell-autonomous factors participate in axon myelination and the stabilization of pre-synaptic receptors. Color code: In green, non-cell-autonomous factors contributing to CP onset; in red, non-cell-autonomous factors contributing to CP closure; in blue, non-cell-autonomous factors contributing in both opening and closure of CP. Abbreviations: CP, critical period; PNN, perineuronal net; FS-PV, fast-spiking-parvalbumin; CSPG, chondroitin sulfate proteoglycans; PTM, post-translational modification.
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