Strong preference for autaptic self-connectivity of neocortical PV interneurons facilitates their tuning to γ-oscillations

Charlotte Deleuze, Gary S Bhumbra, Antonio Pazienti, Joana Lourenço, Caroline Mailhes, Andrea Aguirre, Marco Beato, Alberto Bacci

Research output: Contribution to journalArticlepeer-review

Abstract

Parvalbumin (PV)-positive interneurons modulate cortical activity through highly specialized connectivity patterns onto excitatory pyramidal neurons (PNs) and other inhibitory cells. PV cells are autoconnected through powerful autapses, but the contribution of this form of fast disinhibition to cortical function is unknown. We found that autaptic transmission represents the most powerful inhibitory input of PV cells in neocortical layer V. Autaptic strength was greater than synaptic strength onto PNs as a result of a larger quantal size, whereas autaptic and heterosynaptic PV-PV synapses differed in the number of release sites. Overall, single-axon autaptic transmission contributed to approximately 40% of the global inhibition (mostly perisomatic) that PV interneurons received. The strength of autaptic transmission modulated the coupling of PV-cell firing with optogenetically induced γ-oscillations, preventing high-frequency bursts of spikes. Autaptic self-inhibition represents an exceptionally large and fast disinhibitory mechanism, favoring synchronization of PV-cell firing during cognitive-relevant cortical network activity.

Original languageEnglish
Pages (from-to)e3000419
JournalPLoS Biology
Volume17
Issue number9
DOIs
Publication statusPublished - Sep 2019
Externally publishedYes

Keywords

  • Computational physics
  • neuron
  • Synaptic transmission
  • Simulation methods and programs

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