Single synaptic inputs drive high-precision action potentials in parvalbumin expressing GABA-ergic cortical neurons in vivo

Jean-Sébastien Jouhanneau,James F A Poulet,Jens Kremkow

doi:10.1038/s41467-018-03995-2

Abstract

A defining feature of cortical layer 2/3 excitatory neurons is their sparse activity, often firing in singlets of action potentials. Local inhibitory neurons are thought to play a major role in regulating sparseness, but which cell types are recruited by single excitatory synaptic inputs is unknown. Using multiple, targeted, in vivo whole-cell recordings, we show that single uEPSPs have little effect on the firing rates of excitatory neurons and somatostatin-expressing GABA-ergic inhibitory neurons but evoke precisely timed action potentials in parvalbumin-expressing inhibitory neurons. Despite a uEPSP decay time of 7.8 ms, the evoked action potentials were almost completely restricted to the uEPSP rising phase (~0.5 ms). Evoked parvalbumin-expressing neuron action potentials go on to inhibit the local excitatory network, thus providing a pathway for single spike evoked disynaptic inhibition which may enforce sparse and precisely timed cortical signaling.

Highlights

A defining feature of cortical layer 2/3 excitatory neurons is their sparse activity, often firing in singlets of action potentials
Somatostatin-expressing (SST) GABA-ergic inhibitory interneurons can be recruited by single presynaptic PYR neurons and disynaptically inhibit neighboring neurons[8,9,10]
Neurons, requires trains of multiple unitary excitatory postsynaptic potentials and which cell types are recruited by single uEPSPs evoked by single PYR neurons is unclear

Summary

Introduction

A defining feature of cortical layer 2/3 excitatory neurons is their sparse activity, often firing in singlets of action potentials. Recruitment of SST neurons, requires trains of multiple unitary excitatory postsynaptic potentials (uEPSPs) and which cell types are recruited by single uEPSPs evoked by single PYR neurons is unclear This question is especially relevant for layer 2/3 (L2/3) of primary somatosensory cortex (S1) that contains PYR neurons with sparse firing rates[1,3,11,12]. UEPSPs in SSTs have especially high failure rates and are strongly facilitating in comparison to the faster and more reliable inputs to PV neurons[8,9,13,25,26,27] Whether these synaptic features translate into cell-type specific differences in the probability and timing of action potentials (APs) generated by uEPSPs has not been addressed in vivo. We provide a circuit for single spike evoked disynaptic inhibition in vivo and show that, unexpectedly, the net effect of a single L2/3 excitatory PYR neuron AP on the local network is inhibition

Methods

Results

Conclusion