Endocannabinoid Signaling Contributes to Experience-Induced Increase of Synaptic Release Sites From Parvalbumin Interneurons in Mouse Visual Cortex.

Shiyong Huang,Alfredo Kirkwood

doi:10.3389/fncel.2020.571133

Abstract

During postnatal development of the visual cortex between eye-opening to puberty, visual experience promotes a gradual increase in the strength of inhibitory synaptic connections from parvalbumin-positive interneurons (PV-INs) onto layer 2/3 pyramidal cells. However, the detailed connectivity properties and molecular mechanisms underlying these developmental changes are not well understood. Using dual-patch clamp in brain slices from G42 mice, we revealed that both connection probability and the number of synaptic release sites contributed to the enhancement of synaptic strength. The increase of release site number was hindered by dark rearing from eye-opening and rescued by 3-days re-exposure to the normal visual environment. The effect of light re-exposure on restoring synaptic release sites in dark reared mice was mimicked by the agonist of cannabinoid-1 (CB1) receptors and blocked by an antagonist of these receptors, suggesting a role for endocannabinoid signaling in light-induced maturation of inhibitory connectivity from PV-INs to pyramidal cells during postnatal development.

Highlights

Parvalbumin-expressing interneurons (PV-INs) are the prominent subtype of interneurons in the cortex (Rudy et al, 2011)
Since parvalbumin-positive inhibitory interneurons (PV-INs) contribute the majority of perisomatic inhibitory inputs (Kruglikov and Rudy, 2008), we addressed these questions by performing paired recordings of pyramidal cells (Pyr) and PV-INs in the layer 2/3 of acute visual cortical slices of G42 mice, a line that expresses GFP in PV-INs (Chattopadhyaya et al, 2004)
Action potentials were induced in the PV-INs and the unitary inhibitory postsynaptic current (uIPSC) were recorded in pyramidal cells

Summary

Introduction

Parvalbumin-expressing interneurons (PV-INs) are the prominent subtype of interneurons in the cortex (Rudy et al, 2011). Distinct anatomical and functional features allow PV-INs to provide fast feedforward and feedback inhibition. PV basket cells form perisomatic inhibitions onto pyramidal cells (Tremblay et al, 2016), highly connected with neighbor pyramidal cells and themselves (Holmgren et al, 2003; Packer and Yuste, 2011; Avermann et al, 2012; Gu et al, 2013; Pfeffer et al, 2013), and are uniquely poised to control network firing (Rudy et al, 2011; Bridi et al, 2020b). PV-INs are crucial for several cortical functions. They are essential for gain control (Atallah et al, 2012), play a role on feature selectivity (Lee et al, 2012; Duan et al, 2017; Goel et al, 2018), participate in gamma rhythms (Cardin et al, 2009; Sohal et al, 2009).

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