Perineuronal nets control visual input via thalamic recruitment of cortical PV interneurons.

Giulia Faini,Tommaso Pizzorusso,Charlotte Deleuze,Didi Lamers,Gian Michele Ratto,Alberto Bacci,Silvia Landi,Andrea Aguirre

doi:10.7554/elife.41520

Abstract

In the neocortex, critical periods (CPs) of plasticity are closed following the accumulation of perineuronal nets (PNNs) around parvalbumin (PV)-positive inhibitory interneurons. However, how PNNs tune cortical function and plasticity is unknown. We found that PNNs modulated the gain of visual responses and γ-oscillations in the adult mouse visual cortex in vivo, consistent with increased interneuron function. Removal of PNNs in adult V1 did not affect GABAergic neurotransmission from PV cells, nor neuronal excitability in layer 4. Importantly, PNN degradation coupled to sensory input potentiated glutamatergic thalamic synapses selectively onto PV cells. In the absence of PNNs, increased thalamic PV-cell recruitment modulated feed-forward inhibition differently on PV cells and pyramidal neurons. These effects depended on visual input, as they were strongly attenuated by monocular deprivation in PNN-depleted adult mice. Thus, PNNs control visual processing and plasticity by selectively setting the strength of thalamic recruitment of PV cells.

Highlights

During postnatal maturation, sensory processing goes through a critical period (CP), a developmental interval, in which neural circuits are shaped by sensory experience
These results suggest that the accumulation of perineuronal nets (PNNs) around PV cells during post-CP development determines a change in the excitation-to-inhibition ratio in this interneuron type, and ChABCmediated disruption of PNNs in adult animals (Figure 2) recapitulates some juvenile features of visual cortical circuits
This is associated to a selective increase of thalamic glutamatergic recruitment of PV interneurons in the absence of PNNs, without altering their excitability and the quantal properties of their GABAergic synapses

Summary

Introduction

Sensory processing goes through a critical period (CP), a developmental interval, in which neural circuits are shaped by sensory experience. Disrupting the nets allows the visual signals to get through and enables the connections between neurons to respond in a similar way to their behaviour during the postnatal critical period These changes in neural activity were much reduced in mice that had been prevented from seeing out of one eye. Faini et al propose that the build-up of nets helps to protect basket cells in the visual cortex from being over-activated by sensory circuits This comes at the cost of reducing the ability of the neurons to form new connections, making learning and acquiring new skills more difficult. Plasticity induced by short monocular deprivation (MD) strongly attenuated these effects, indicating that PNN-mediated modulation of thalamic input onto PV cells depends on visual activity These results reveal the synaptic and circuit mechanisms by which PNNs restrict sensory plasticity in the adult visual cortex

Results

Discussion

Materials and methods