Modulation of Coordinated Activity across Cortical Layers by Plasticity of Inhibitory Synapses

• Main Authors: Joana Lourenço, Angela Michela De Stasi, Charlotte Deleuze, Mathilde Bigot, Antonio Pazienti, Andrea Aguirre, Michele Giugliano, Srdjan Ostojic, Alberto Bacci
• Format: Article
• Language: English
• Published: Elsevier 2020-01-01
• Series: Cell Reports
• Online Access: http://www.sciencedirect.com/science/article/pii/S2211124719317097

Summary: In the neocortex, synaptic inhibition shapes all forms of spontaneous and sensory evoked activity. Importantly, inhibitory transmission is highly plastic, but the functional role of inhibitory synaptic plasticity is unknown. In the mouse barrel cortex, activation of layer (L) 2/3 pyramidal neurons (PNs) elicits strong feedforward inhibition (FFI) onto L5 PNs. We find that FFI involving parvalbumin (PV)-expressing cells is strongly potentiated by postsynaptic PN burst firing. FFI plasticity modifies the PN excitation-to-inhibition (E/I) ratio, strongly modulates PN gain, and alters information transfer across cortical layers. Moreover, our LTPi-inducing protocol modifies firing of L5 PNs and alters the temporal association of PN spikes to γ-oscillations both in vitro and in vivo. All of these effects are captured by unbalancing the E/I ratio in a feedforward inhibition circuit model. Altogether, our results indicate that activity-dependent modulation of perisomatic inhibitory strength effectively influences the participation of single principal cortical neurons to cognition-relevant network activity. : Lourenço et al. demonstrate that burst firing of layer 5 pyramidal neurons (PNs) induces long-term potentiation of inhibition (LTPi). LTPi strongly affects PN input/output spikes, prevents transfer of information across cortical layers, and affects phase locking of PN firing to cognition-relevant rhythmic activity. Keywords: neocortex, GABAergic plasticity, PV cells, gamma oscillations, E/I ratio, feedforward inhibition, layer 5