Development of neonatal EEG activity: From phenomenology to physiology

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Summary

After having been in routine use for about half a century, neonatal EEG is currently facing unprecedented challenges in assessing and monitoring brain function during intensive care of preterm babies. It has therefore become increasingly important to understand the neurophysiological processes underlying EEG activity, as well as to identify those features of brain activity that are essential for brain development. By integrating the existing literature from basic neuroscience to neonatal EEG, the present review proposes a simple, neurophysiologically and neuroanatomically based framework for neonatal EEG interpretation. This is composed of two developmental trajectories: one related to discrete spontaneous activity transients (SAT) and the other to the ongoing, apparently oscillatory EEG activity. This framework can readily be applied to clinical use. It may open novel avenues to automated analysis in EEG monitoring and, moreover, it may facilitate genuine translational research.

Introduction

Neonatal electroencephalography (EEG) recordings have been routinely performed for over half a century. A major challenge in the early studies was to obtain readable EEG tracings from the non-cooperative preterm and full-term babies.1 In the course of this pioneering work, the recording configurations were fixed in a manner that permitted consistent observation of EEG signals with a stable baseline. In practice, this implied recordings based on bipolar derivations with four AC-coupled EEG electrodes over each hemisphere, usually combined with polygraphy (i.e. respiration, electro-oculogram, electrocardiogram and electromyogram) for assessing vigilance states.1, 2 Ever since, almost every study has directly adopted these recording specifications, and aimed at (1) refining the waveform (i.e. graphological) characterization of neonatal EEG features; (2) characterizing EEG features with various kinds of time series analyses; or (3) identifying novel EEG waveforms with potential clinical correlates. The overall result of this work is an extensive but largely phenomenological literature on neonatal EEG.

The traditional view of neonatal EEG activity has its main emphasis on the visually apparent developmental transformation from ‘discontinuous’ to ‘continuous’ EEG1, 2, 3, 4, while the interest in more detailed EEG features has been more variable. Neonatal EEG still has a clearly suboptimal sensitivity in detecting or predicting various milder neurocognitive defects.2, 5, 6

In this review we propose some ideas for increasing the information content and the clinical utility of the neonatal EEG. These include technical improvements related to the recording and analysis of data.7, 8, 9 Unfortunately, research on the neonatal EEG has diverged from basic developmental neuroscience. However, novel insights into the physiology and pathophysiology of human scalp-recorded EEG can be obtained from invasive experiments carried out in a large number of studies on experimental animals in vivo10, 11, 12, 13, 14, 15, 16, 17, 18 or in vitro.19, 20, 21, 22, 23, 24 An important goal is to merge the data on the human neonatal EEG with what is known from basic neuroscience. With this in mind, we propose below a simplified analysis framework, i.e. a rough model for EEG ontogeny during the neonatal period.

Section snippets

From basic neuroscience to neonatal EEG: functional aspects

Many studies on cortical structures (hippocampus and neocortex) in rodents and other experimental animals have shown that spontaneous, intermittent (i.e. ‘discontinuous’) activity is a robust, universal phenomenon during development, and that it commences at a time when sensory mechanisms have not yet become functional.24, 25, 26 These events have been called, inter alia, ‘giant depolarizing potentials’ (GDPs)23, 24, 27 or ‘early network oscillations’ (ENOs).14 Spontaneous activity of this kind

From basic neuroscience to neonatal EEG: structural aspects

The basic molecular, cellular and network mechanisms that are related to the development of the human brain in general, and of the human EEG in particular, are impossible to study directly and hence call for information from animal experiments. The situation is not as difficult for anatomical studies, which can often be performed in a satisfactory manner on postmortem tissue. Indeed, a number of major advances have recently been made in studies of the emerging connectivity of the immature human

A simplified model of EEG ontogeny

Fig. 3 shows a simplified model of EEG ontogeny which attempts to integrate the salient features of the development of EEG activity in the light of the data from both animal experiments and work on human neonates. The model proposes two developmental trajectories, one related to the discrete SATs and one to the ongoing (oscillatory) EEG activity.

First, the shape of SATs in the EEG changes throughout the last trimester, whereas their overall rate of occurrence is relatively stable. At the

Practical implications and future prospects

Integration of basic neuroscience and state-of-the-art recording and analysis techniques will open novel avenues for the progress in the field of neonatal EEG. At the moment, there is an unprecedented interest in the assessment of brain function in premature babies. This work is currently facing three major challenges.

First, the recording technique needs to have a high temporal and spatial resolution and fidelity. These are technically trivial problems and they have in fact already been solved

Acknowledgements

This work was supported by Arvo and Lea Ylppö Foundation, the Academy of Finland, and Juselius Foundation. We also want to thank Drs. M.-D. Lamblin, S. Schuchmann, S.T. Sipilä, and E.A. Tolner for their comments on the manuscript.

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