CHAPTER 4

Elements of the Normal Neonatal EEG

Visual analysis of the neonatal electroencephalogram (EEG) requires the recognition of the conceptional age-dependent features characteristic of specific epochs of development. These electrographic features are presented here in four different formats: a table that lists specific elements (Table 4.1), a narrative that describes the continuum of development, and a summary by epoch of conceptional age (CA) of the expected elements. In addition, representative samples of EEG recordings in each epoch are provided.

Visual analysis and interpretation require determination of the degree of continuity of background activity (Figure 4.1), and a degree of interhemispheric synchrony of the background activity (Figure 4.2). They also require recognition of specific waveforms and patterns that occur with increasing age (Figure 4.3), the appearance of wake/sleep cycles (Dos Santos et al., 2014; Dreyfus-Brisac, 1968; Scher, 2011), and the age-dependent response of the EEG to stimulation of the infant.

CONTINUUM OF DEVELOPMENT

Continuity

When the brain’s electrical activity, as revealed by the EEG first appears, it is discontinuous, with long periods of quiescence; this pattern is referred to as tracé discontinu (Dreyfus-Brisac, 1962). As age increases, periods of inactivity shorten (Figure 4.1) (Anderson et al., 1985; Connell et al., 1978; Hahn et al., 1989; Selton et al., 2000). The longest acceptable single interburst-interval durations in relation to CA have been reported to be: 24 to 26 weeks CA, 60 seconds (Vecchierini et al., 2003); 26 weeks CA, 46 seconds; 27 weeks CA, 36 seconds; 28 weeks CA, 27 seconds (Selton et al., 2000); less than 30 weeks CA, 35 seconds; 31 to 33 weeks CA, 20 seconds; 34 to 36 weeks CA, 10 seconds; and 37 to 40 weeks CA, 6 seconds (Clancy et al., 2003; Hahn et al., 1989).

At a CA of approximately 30 weeks, continuous activity appears and is present only during rapid eye movement (REM) sleep. At about 34 weeks CA, the EEG is also continuous in the awake state. This continuous polyfrequency pattern has been traditionally referred to as activité moyenne (Lamblin et al., 1999). Continuity appears in non-REM (NREM) sleep at about 36 to 37 weeks. However, from that time until about 5 to 6 weeks post-term, the EEG during periods of NREM sleep shows occasional semiperiodic episodes of generalized voltage, attenuation (not quiescence) lasting from 3 to 15 seconds; a pattern that has been called tracé alternant (Dreyfus-Brisac and Blanc, 1956). Examples of CA-dependent discontinuity are shown in Figures 4.4 to 4.39.

Bilateral Synchrony

Before 27 to 28 weeks CA, EEG activity typically occurs in generalized bisynchronous bursts with a discontinuous background in the interburst intervals (Selton et al., 2000). However, the bursts may also appear asynchronously (Figure 4.8). After 27 to 28 weeks CA, the activity is generally asynchronous in homologous regions of the hemispheres (the greater the distance from the midline, the greater the degree of asynchrony). With increasing maturity, the degree of asynchrony diminishes. The degree of asynchrony reflects not only maturation but also the wake/sleep state. Thus, asynchrony is most prominent in NREM sleep and is least prominent in REM sleep. The only exception to these general rules is that from the time frontal sharp waves first appear, at about 35 weeks CA, they are bilaterally synchronous. Examples of EEG demonstrating increasing interhemispheric synchrony with increasing CA are shown in Figures 4.6 to 4.39.

Table 4.1 Developmental EEG Characteristics of Premature and Term Infants

Figure 4.1 Average duration of discontinuous periods in NREM sleep in the EEG of a premature infant. Data points are taken from Verrichierni et al. (2003) (24–26 weeks CA), Selton et al. (2000) (26–28 weeks CA), and Hahn et al. (1987), Clancy et al. (2003) (30–40 weeks CA) and a curve derived from exponential regression.

Figure 4.2 Development of interhemispheric synchrony in the EEG of the premature infant. See text for details and references. (Hrachovy, 2000, with permission.)

Figure 4.3 Appearance and disappearance of developmental EEG landmarks from prematurity to 3 months post-term. See text for details and references. (Hrachovy, 2000, with permission.)

EEG Developmental Landmarks

An orderly appearance and disappearance of specific waveforms and patterns occurs with increasing CA (Figure 4.3).

Beta–Delta Complexes

The presence of these complexes constitutes the prime hallmark of prematurity and is present from about 26 to 38 weeks CA. They consist of random 0.3- to 1.5-Hz waves of 50 to 250 µV, with superimposed bursts of low- to moderate-voltage fast activity. The frequency of the fast activity may vary, even in the same infant. Two frequencies predominate: 8 to 12 Hz and, more commonly, 18 to 22 Hz. The voltage of the fast activity varies throughout each burst but rarely exceeds 75 µV. Figures 4.6 to 4.22 show typical beta–delta complexes at varying CAs. Various names have been given to these complexes: “spindle-delta bursts,” “brushes,” “spindle-like fast waves,” and “ripples of prematurity.” Dreyfus-Brisac et al. (1956), who first described the complexes, referred to them as “rapid bursts,” emphasizing, as in other names, the fast component. An important feature of beta–delta complexes is that they typically occur asynchronously in derivations from homologous areas and show a variable voltage asymmetry on the two sides.

These complexes first appear as a dominant feature in the EEG at about 26 weeks CA. When first present, these occur infrequently and largely in the central regions. During the next 5 to 6 weeks, they become progressively more persistent, and the voltage of the fast component usually increases. Until 32 weeks CA, the fast component has a predominant frequency of 18 to 22 Hz; thereafter, the slower frequency (8–12 Hz) is most often present. The special distribution of the beta–delta complexes also changes with CA, becoming more prominent in the occipital and temporal regions with increasing age.

From the time beta–delta complexes first appear and changes in the wake/sleep cycle can be appreciated, the presence of beta–delta complexes is a prominent feature during REM sleep—a state characterized by virtually continuous EEG activity after 30 weeks CA. At 33 weeks CA, beta–delta complexes are maximally expressed in NREM sleep, rather than REM sleep, and appear more prominently in the temporal-occipital areas. From 33 to 37 weeks CA, beta–delta complexes continue to occur primarily in NREM sleep.

Temporal Theta and Alpha Bursts

A useful developmental EEG marker is the appearance of rhythmic 4 to 6 Hz waves occurring independently in short bursts of rarely more than 2 seconds arising independently in the left and right midtemporal areas. Voltage varies from roughly 20 to 200 µV. Individual waves often have a sharp configuration (Hughes et al., 1987; Werner et al., 1977) (Figures 4.10, 4.11, 4.13–4.15). This activity appears at about 26 weeks CA, is expressed maximally between 30 and 32 weeks, and then rapidly disappears. It is replaced by temporal alpha bursts that otherwise have characteristics of amplitude, burst duration, and spatial distribution similar to temporal theta bursts (Figures 4.16–4.18). The presence of temporal alpha bursts can be considered a very specific marker for 33 weeks; they appear at that CA and are no longer present at 34 weeks CA.

Frontal Sharp Waves

Isolated sharp waves of blunt configuration, usually with an initial surface-negative phase followed by a surface-positive phase, have been referred to as encouche frontales (Dreyfus-Brisac, 1962; Kellaway and Crawley, 1964). They may be present at 34 weeks CA but attain maximum expression at about 35 weeks CA. They diminish in number and voltage after 44 weeks CA and are only rarely seen in infants older than 6 weeks post-term.

These frontal sharp transients are bilaterally synchronous and symmetrical from the time of their first appearance, although there may be some variable lateralization (Figures 4.19 and 4.27) (Crippa et al., 2007). The initial surface-negative component lasts about 200 msec. The succeeding surface-positive component lasts somewhat longer, but this is quite variable and is often difficult to measure because intervening background activity obscures the termination of the waveform (Figures 4.20 and 4.24–4.28). They typically occur randomly as single events, predominantly in transitional rather than in REM or NREM sleep. However, they may also recur in brief runs and may also be mixed with other normal features of near-term infants such as bifrontal delta activity (Figures 4.26 and 4.28–4.29).

Distinguishing Between the Waking and Sleep EEG

Until 36 to 37 weeks CA, distinguishing the various states of the wake/sleep cycle is based upon empirical factors such as behavior and polygraphic parameters. Eye opening is associated with the awake state, and eye closure is associated with sleep. Regular respiration, random eye movements, and variable muscle tone are associated with NREM sleep while irregular respiration, REMs and decreased muscle tone are associated with REM sleep.

Electrographically at about 30 weeks CA, the background activity is continuous in REM sleep and discontinuous during wakefulness and NREM sleep. However, the EEG activity in all states is characterized by the presence of beta–delta complexes with their CA-dependent abundance, spatial distribution, and degree of synchrony (Figures 4.21–4.23).

By 36 to 37 weeks CA, a clear distinction can be made between the waking EEG and the sleep EEG based upon their inherent features, without reliance on clinical or polygraphic data (Figures 4.31–4.37). In the awake EEG, beta–delta complexes are rarely present and the awake background activity consists chiefly of continuous polyfrequency activity, traditionally referred to as activité moyenne. This polyfrequency activity is characterized by random, very slow, low-voltage activity best described as baseline shifting, with superimposed semirhythmic 4 to 8 Hz activity in all regions. In addition generalized, very low voltage 18 to 22 Hz activity and anteriorly distributed, very low voltage 2 to 3 Hz activity may be present. From the standpoint of determining CA, disappearance of the beta–delta complexes when the infant appears behaviorally awake constitutes an important marker of 36 to 37 weeks CA.

Before about 36 weeks CA, the background activity in NREM sleep is discontinuous (Figure 4.22). Between 36 and 38 weeks CA, two NREM EEG patterns emerge. The first is continuous high-voltage slow-wave activity in all regions. The second pattern is known as tracé alternant and is characterized by a modulation of generalized activity with alternating periods of high and low voltage activity (Figures 4.33–4.35). This pattern may occur in infants through 44 weeks CA. After that period, NREM sleep is characterized by continuous slow-wave activity with the eventual emergence of sleep spindles after about 46 weeks CA—although rudimentary spindles may occur earlier (Figures 4.38 and 4.39).

The EEG character of REM sleep is similar to that of the awake recording from about 30 weeks CA. Infant behaviors and polygraphic recordings of respiration, eye movements, and submental EMG distinguish awake from REM sleep.

The terms transitional sleep or indeterminant sleep are used to characterize the state of the infant when it cannot be precisely determined by specific EEG criteria.

Reactivity to Stimulation

Changes in EEG activity in response to stimuli do not clearly emerge until about 33 to 34 weeks CA (Figure 4.23), and by 37 weeks CA, these responses can be easily elicited. The response to a stimulus is related to the character of the ongoing activity at the time of the stimulus. If high voltage, very slow activity is present, an effective stimulus may produce abrupt and pronounced generalized attenuation of voltage lasting as long as 5 to 10 seconds (Ellingson, 1958; Kellaway and Crawley, 1964).

Spontaneous episodes of attenuation may be associated with self-arousal (Figures 4.23 and 4.37). They occur in infants until about 2 months post-term, possibly in response to interoceptive stimuli. Such episodes should not be interpreted as evidence of immaturity or be confused with the repetitive episodes of generalized or regional attenuation that occur in abnormal conditions of diffuse cerebral dysfunction, such as neonatal encephalopathy.

Additional Special Waveforms and Patterns

Some special waveforms and patterns, particularly in the near-term and term infant, are considered to be within the range of normal variation although they are not developmental milestones, per se. They are bifrontal delta activity and some forms of temporal sharp waves.

Bifrontal Delta Activity

Bifrontal delta activity appears in the near-term or term infant as intermittent semirhythmic 1.5 to 2 Hz high-voltage activity in the frontal regions bilaterally (Figures 4.28 and 4.29). This activity may occur in close association with frontal sharp transients, most prominently during transitional sleep. This pattern has been referred to as “anterior dysrhythmia.” However, this is a misnomer, because its presence does not suggest abnormality and it is considered within the range of normal variation (Clancy et al., 2003).

Temporal Sharp Waves

Temporal sharp waves are discussed in detail in the following chapter that concerns findings of uncertain diagnostic significance. That discussion describes criteria used to differentiate normal temporal sharp waves from those that are clearly abnormal. Temporal sharp waves that can be considered to be normal have a simple diphasic morphology, with the initial component appearing as surface-negative polarity, and occur randomly, usually asynchronously on the two sides and during sleep (Figure 4.30). Complex morphology, positive polarity, persistent localization and occurrence during wakefulness, are criteria for abnormality (see Chapter 5).

SUMMARY OF CONCEPTIONAL AGE-DEPENDENT FINDINGS

24 to 26 Weeks Conceptional Age (Figures 4.4 and 4.5)

•  Continuity. There are brief bursts of activity between periods of electrical quiescence. The interburst interval is CA dependent and is at its longest at this age.

•  Synchrony. Bursts of activity during this epoch are typically synchronous, but may also appear asynchronously on the two sides.

•  Landmarks. Beta–delta complexes may be present during this epoch.

•  Wake/sleep cycles. Cycles are not well defined by behavior or polygraphic changes. No evidence is seen on EEG of wake/sleep cycling.

•  Reactivity. No reactivity to stimulation occurs.

27 to 28 Weeks Conceptional Age (Figures 4.6–4.8)

•  Continuity. Electrical activity is episodic. Brief periods of generalized moderate-voltage activity may appear between periods of generalized electrical quiescence. The interburst intervals are relatively long compared to those present at later ages.

•  Synchrony. The bursts of electrical activity are asynchronous on the two sides.

•  Landmarks. Beta–delta complexes are present in the central region and rudimentary temporal theta bursts are present.

•  Wake/sleep cycles. Cycles are not well defined by behavior or polygraphic changes. No evidence of wake/sleep cycles is found on EEG.

•  Reactivity. No reaction to stimulation occurs.

29 to 30 Weeks Conceptional Age (Figures 4.9–4.12)

•  Continuity

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