High-frequency EEG covaries with spike burst patterns detected in cortical neurons

Bartosz Telenczuk,Stuart N Baker,Andreas V M Herz,Gabriel Curio

doi:10.1152/jn.00327.2010

Abstract

Invasive microelectrode recordings measure neuronal spikes, which are commonly considered inaccessible through standard surface electroencephalogram (EEG). Yet high-frequency EEG potentials (hf-EEG, f > 400 Hz) found in somatosensory evoked potentials of primates may reflect the mean population spike responses of coactivated cortical neurons. Since cortical responses to electrical nerve stimulation vary strongly from trial to trial, we investigated whether the hf-EEG signal can also echo single-trial variability observed at the single-unit level. We recorded extracellular single-unit activity in the primary somatosensory cortex of behaving macaque monkeys and identified variable spike burst responses following peripheral stimulation. Each of these responses was classified according to the timing of its spike constituents, conforming to one of a discrete set of spike patterns. We here show that these spike patterns are accompanied by variations in the concomitant epidural hf-EEG. These variations cannot be explained by fluctuating stimulus efficacy, suggesting that they were generated within the thalamocortical network. As high-frequency EEG signals can also be reliably recorded from the scalp of human subjects, they may provide a noninvasive window on fluctuating cortical spike activity in humans.

Highlights

EIGHT DECADES after Berger (1929) first described the electroencephalogram (EEG), this noninvasive measure still serves as the main tool for recording human brain activity at high temporal resolution
Since the focus of this study was on the relation between response patterns of single neurons and high-frequency burst of EEG oscillations (hf-EEG), we manually discriminated clusters of spike waveforms from extracellular traces and selected only clusters that clearly corresponded to single-unit activity
We show that high-frequency components of evoked macroscopic EEG potentials provide a measure of varying cortical spike responses to peripheral nerve stimulation: 1) peaks of the hf-EEG waveform represent discrete windows of opportunity for single-cell spike generation; 2) the amplitude of hf-EEG covaries with spike patterns originating from differential emissions/omissions of spikes in those windows; and 3) a significant part of this correlated variability arises in the thalamocortical loop and not solely in lower levels of the somatosensory pathway

Summary

Introduction

EIGHT DECADES after Berger (1929) first described the electroencephalogram (EEG), this noninvasive measure still serves as the main tool for recording human brain activity at high temporal resolution. The timing of spikes generated by both types of neuronal responses has a close relation to the hf-EEG: the peaks of the population peristimulus time histogram (PSTH) calculated from those responses align with peaks of the averaged hf-EEG (Baker et al 2003) This coupling between average single-cell and hf-EEG responses suggests that surface hf-EEG components reflect either synchronous action potentials of cortical neurons or ultrafast postsynaptic potentials (Baker et al 2003; Barth 2003; Curio et al 1994; Hashimoto et al 1996; Shimazu et al 2000; Stern et al 1992). In the present study we demonstrate this to be the case, validating hf-EEG as a noninvasive probe for fluctuating cortical spike output

Methods

Results

Conclusion