Non-associative potentiation of perisomatic inhibition alters the temporal coding of neocortical layer 5 pyramidal neurons

PLoS Biol. 2014 Jul 8;12(7):e1001903. doi: 10.1371/journal.pbio.1001903. eCollection 2014 Jul.

Abstract

In the neocortex, the coexistence of temporally locked excitation and inhibition governs complex network activity underlying cognitive functions, and is believed to be altered in several brain diseases. Here we show that this equilibrium can be unlocked by increased activity of layer 5 pyramidal neurons of the mouse neocortex. Somatic depolarization or short bursts of action potentials of layer 5 pyramidal neurons induced a selective long-term potentiation of GABAergic synapses (LTPi) without affecting glutamatergic inputs. Remarkably, LTPi was selective for perisomatic inhibition from parvalbumin basket cells, leaving dendritic inhibition intact. It relied on retrograde signaling of nitric oxide, which persistently altered presynaptic GABA release and diffused to inhibitory synapses impinging on adjacent pyramidal neurons. LTPi reduced the time window of synaptic summation and increased the temporal precision of spike generation. Thus, increases in single cortical pyramidal neuron activity can induce an interneuron-selective GABAergic plasticity effectively altering the computation of temporally coded information.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / physiology
  • Animals
  • Calcium Channels, L-Type / physiology
  • Long-Term Potentiation / physiology
  • Long-Term Synaptic Depression / physiology
  • Mice, Inbred C57BL
  • Neocortex / cytology
  • Neuronal Plasticity / physiology
  • Neurons
  • Patch-Clamp Techniques
  • Pyramidal Cells / physiology*
  • gamma-Aminobutyric Acid / physiology

Substances

  • Calcium Channels, L-Type
  • gamma-Aminobutyric Acid

Grant support

This work was supported by the Giovanni Armenise-Harvard Foundation: Career Development Award, European Research Council (ERC) under the European Community's 7th Framework Programmme (FP7/2007–2013)/ERC grant agreement No 200808), “Investissements d'avenir” ANR-10-IAIHU-06, and a grant from the Institut du Cerveau et de la Moelle épinière (Paris) (AB). Experiments by NR and DD were funded by a grant from the Ile de France (NeRF) and the Agence Nationale de la Recherche (ANR-2010-BLANC-1411) to DD. NR is in mobility from CNRS UMR 5297, Institut Interdisciplinaire de Neurosciences, Université de Bordeaux, Bordeaux, F-33000 France. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.