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

Joana Lourenço; Simone Pacioni; Nelson Rebola; Geeske M van Woerden; Silvia Marinelli; David DiGregorio; Alberto Bacci

doi:10.1371/journal.pbio.1001903

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.

Authors

Joana Lourenço¹, Simone Pacioni², Nelson Rebola³, Geeske M van Woerden¹, Silvia Marinelli², David DiGregorio³, Alberto Bacci¹

Affiliations

¹ European Brain Research Institute, Rome, Italy; Sorbonne Universités UPMC Univ. Paris 06, UMR S 1127, Paris, France; Inserm U 1127, Paris, France; CNRS UMR 7225, Paris, France; ICM- Institut du Cerveau et de la Moelle épinière, Paris, France.
² European Brain Research Institute, Rome, Italy.
³ CNRS UMR 3571, Paris, France; Institut Pasteur, Unit of Dynamic Neuronal Imaging, Paris, France.

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

Grants and funding

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.