Widely Different Correlation Patterns Between Pairs of Adjacent Thalamic Neurons In vivo.

Anders Wahlbom,Hannes Mogensen,Henrik Jörntell

doi:10.3389/fncir.2021.692923

Abstract

We have previously reported different spike firing correlation patterns among pairs of adjacent pyramidal neurons within the same layer of S1 cortex in vivo, which was argued to suggest that acquired synaptic weight modifications would tend to differentiate adjacent cortical neurons despite them having access to near-identical afferent inputs. Here we made simultaneous single-electrode loose patch-clamp recordings from 14 pairs of adjacent neurons in the lateral thalamus of the ketamine-xylazine anesthetized rat in vivo to study the correlation patterns in their spike firing. As the synapses on thalamic neurons are dominated by a high number of low weight cortical inputs, which would be expected to be shared for two adjacent neurons, and as far as thalamic neurons have homogenous membrane physiology and spike generation, they would be expected to have overall similar spike firing and therefore also correlation patterns. However, we find that across a variety of thalamic nuclei the correlation patterns between pairs of adjacent thalamic neurons vary widely. The findings suggest that the connectivity and cellular physiology of the thalamocortical circuitry, in contrast to what would be expected from a straightforward interpretation of corticothalamic maps and uniform intrinsic cellular neurophysiology, has been shaped by learning to the extent that each pair of thalamic neuron has a unique relationship in their spike firing activity.

Highlights

Thalamic neurons have a tendency to produce oscillatory behavior and the relative synchronization of such oscillatory output can be directly read out using EEG (Steriade et al, 1991; Hirata and Castro-Alamancos, 2010)
We find that the correlation patterns differ extensively between pairs, regardless of location within the extent of the lateral thalamus, which suggests that adjacent thalamic neurons have different input connectivity and/or resonant oscillatory frequencies
The correlation pattern could be plotted as raw peri-spike time histograms (PSpTH) of the responding spike, or as spiketriggered kernel density estimators (SpT-kernel density estimations (KDEs)) of the same correlation

Summary

Introduction

Thalamic neurons have a tendency to produce oscillatory behavior and the relative synchronization of such oscillatory output can be directly read out using EEG (Steriade et al, 1991; Hirata and Castro-Alamancos, 2010). Oscillatory EEG waves can be detected in the relaxed state as well as in sleep (Sachdev et al, 2015). Under such circumstances, a critical factor is likely that thalamic neurons are induced to hyperpolarize, which leads to a relative unmasking of the intrinsic oscillatory behavior in the thalamic neurons (McCormick and Pape, 1990). When a sufficient number of thalamic projection neurons synchronize their oscillatory behavior, cortical synaptic activation becomes at least partly synchronized, and the resulting field potentials can become so large that they can even be measured on the outside of the skull as an EEG.

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