Abstract

The cortical layer 1 (L1) contains a population of GABAergic interneurons, considered a key component of information integration, processing, and relaying in neocortical networks. In fact, L1 interneurons combine top–down information with feed-forward sensory inputs in layer 2/3 and 5 pyramidal cells (PCs), while filtering their incoming signals. Despite the importance of L1 for network emerging phenomena, little is known on the dynamics of the spike initiation and the encoding properties of its neurons. Using acute brain tissue slices from the rat neocortex, combined with the analysis of an existing database of model neurons, we investigated the dynamical transfer properties of these cells by sampling an entire population of known “electrical classes” and comparing experiments and model predictions. We found the bandwidth of spike initiation to be significantly narrower than in L2/3 and 5 PCs, with values below 100 cycle/s, but without significant heterogeneity in the cell response properties across distinct electrical types. The upper limit of the neuronal bandwidth was significantly correlated to the mean firing rate, as anticipated from theoretical studies but not reported for PCs. At high spectral frequencies, the magnitude of the neuronal response attenuated as a power-law, with an exponent significantly smaller than what was reported for pyramidal neurons and reminiscent of the dynamics of a “leaky” integrate-and-fire model of spike initiation. Finally, most of our in vitro results matched quantitatively the numerical simulations of the models as a further contribution to independently validate the models against novel experimental data.

Highlights

  • Layer 1 (L1) is the most superficial neocortical layer and holds a key role in the hierarchy of information processing within neocortical networks

  • We describe the firing response properties of L1 cortical interneurons based on a set of whole-cell patch-clamp recordings in N = 65 cells from slices of the rat somatosensory cortex

  • We studied the encoding properties of L1 interneurons by measuring their dynamical transfer function in the Fourier domain (Figures 1B–E)

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Summary

INTRODUCTION

Layer 1 (L1) is the most superficial neocortical layer and holds a key role in the hierarchy of information processing within neocortical networks. For L1, we know that several subpopulations of L1 interneurons can be distinguished on the basis of their firing in response to constant amplitude currents (Muralidhar et al, 2013), displaying quite heterogeneous electrical phenotypes It is still not clear how these different electrical signatures contribute to the distinct properties in the network dynamics of information processing within L1. Allowing a comparison with previous studies in principal cells, we adopted a simple and established experimental protocol (Higgs and Spain, 2009; Ilin et al, 2013) This is equivalent (Tchumatchenko and Wolf, 2011) to our previous probing strategy of the dynamical excitable properties of cortical neurons (Kondgen et al, 2008; Linaro et al, 2018). A set of previously released multicompartmental mathematical models of L1 interneurons (Markram et al, 2015) was studied under the same stimulation protocols in vitro, aiming at further validating them and at supporting the interpretation of the experimental data

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