Abstract

Despite the importance of the discharge frequency in neuronal communication, little is known about the firing-rate patterns of cortical populations. Using large-scale recordings from multiple layers of the entorhinal-hippocampal loop, we found that the firing rates of principal neurons showed a lognormal-like distribution in all brain states. Mean and peak rates within place fields of hippocampal neurons were also strongly skewed. Importantly, firing rates of the same neurons showed reliable correlations in different brain states and testing situations, as well as across familiar and novel environments. The fraction of neurons that participated in population oscillations displayed a lognormal pattern. Such skewed firing rates of individual neurons may be due to a skewed distribution of synaptic weights, which is supported by our observation of a lognormal distribution of the efficacy of spike transfer from principal neurons to interneurons. The persistent skewed distribution of firing rates implies that a preconfigured, highly active minority dominates information transmission in cortical networks.

Highlights

  • The dominant communication across neurons occurs via spikes

  • Local field potentials (LFP) and unit firing were recorded by multiple-shank silicon probes (Mizuseki et al, 2009; Fujisawa et al, 2008) from the hippocampal CA1 and CA3 pyramidal layers and dentate gyrus

  • Periods without theta were concatenated as immobility or consummatory behaviors (IMM)

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Summary

Introduction

The dominant communication across neurons occurs via spikes. Yet, despite the central role of spiking activity in transmitting information, only limited data is available about the firing rates of unbiased neuronal populations in intact networks (Hromadka et al, 2008; O'Connor et al, 2010). The term ‘sparse coding’ refers to a model in which a small fraction of neurons is engaged in any situation, as opposed to a dense population code in which firing rate fluctuations of individual members represents the input (Olhausen and Field, 1997). In this postulated high signal-to-noise ratio scheme, slow firing neurons contribute largely unwanted noise, viewed as an inevitable consequence of brain organization (Lisman, 1997; Shadlen and Newsome, 1998) rather than information. A largely heterogeneous group of neurons in each cortical layer may form a ‘skeleton’ network in which firing rates are largely determined by the intrinsic

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