Abstract

Neuroanatomy suggests that adjacent neocortical neurons share a similar set of afferent synaptic inputs, as opposed to neurons localized to different areas of the neocortex. In the present study, we made simultaneous single-electrode patch clamp recordings from two or three adjacent neurons in the primary somatosensory cortex (S1) of the ketamine-xylazine anesthetized rat in vivo to study the correlation patterns in their spike firing during both spontaneous and sensory-evoked activity. One difference with previous studies of pairwise neuronal spike firing correlations was that here we identified several different quantifiable parameters in the correlation patterns by which different pairs could be compared. The questions asked were if the correlation patterns between adjacent pairs were similar and if there was a relationship between the degree of similarity and the layer location of the pairs. In contrast, our results show that for putative pyramidal neurons within layer III and within layer V, each pair of neurons is to some extent unique in terms of their spiking correlation patterns. Interestingly, our results also indicated that these correlation patterns did not substantially alter between spontaneous and evoked activity. Our findings are compatible with the view that the synaptic input connectivity to each neocortical neuron is at least in some aspects unique. A possible interpretation is that plasticity mechanisms, which could either be initiating or be supported by transcriptomic differences, tend to differentiate rather than harmonize the synaptic weight distributions between adjacent neurons of the same type.

Highlights

  • At the macroscopic level, anatomically specific thalamocortical (Jones, 2000) and corticocortical (Malach et al, 1993; Négyessy et al, 2013) connectivity combined with dense intracortical connectivity that gradually tapers off with distance (Fino and Yuste, 2011; Packer and Yuste, 2011) indicate that within a given volume of cortex, the available afferent inputsAbbreviations: ECoG, electrocorticogram; Kernel Density Estimations (KDEs), kernel density estimation; MDS, multidimensional scaling; PSpTHs, peri-spike triggered time histograms; S1, primary somatosensory cortex; SpT-KDE, spike-triggered KDE.Neuronal Correlation Patterns in Neocortex should be highly similar between adjacent neurons

  • Pyramidal cells are present in all layers of the neocortex, except layer I (Harris and Shepherd, 2015), but are believed to have particular properties and functions depending on their layer location (Brecht, 2017)

  • For the decoding of tactile afferent input patterns in primary somatosensory cortex (S1) neurons, it was recently shown that adjacent neurons differ widely in terms of their decoding performance and that layer location has no predictive value for the decoding performance of the neuron (Oddo et al, 2017)

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Summary

Introduction

Anatomically specific thalamocortical (Jones, 2000) and corticocortical (Malach et al, 1993; Négyessy et al, 2013) connectivity combined with dense intracortical connectivity that gradually tapers off with distance (Fino and Yuste, 2011; Packer and Yuste, 2011) indicate that within a given volume of cortex, the available afferent inputsNeuronal Correlation Patterns in Neocortex should be highly similar between adjacent neurons. Clear differences exist in the output targets of their axons and in the sources of their afferent inputs (Helmstaedter et al, 2007; Harris and Shepherd, 2015). Based on these and other findings, it has been suggested that there is a canonical microcircuitry in the neocortex, where the subtype and layer identity of the constituent neurons are important determinants of the structure of that microcircuitry (Helmstaedter et al, 2007; Harris and Mrsic-Flogel, 2013; Reimann et al, 2015). For the decoding of tactile afferent input patterns in primary somatosensory cortex (S1) neurons, it was recently shown that adjacent neurons differ widely in terms of their decoding performance and that layer location has no predictive value for the decoding performance of the neuron (Oddo et al, 2017)

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