Atlas of Neonatal Electroencephalography, 3rd Edition

Chapter 4

Elements of the Normal Neonatal Electroencephalogram

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 (Fig. 4-1), and the degree of interhemispheric synchrony of the background activity (Fig. 4-2). They also require recognition of specific wave forms and patterns that occur with increasing age (Fig. 4-3), the appearance of sleep/wake cycles, and 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, and this pattern is referred to as tracé discontinu(Dreyfus-Brisac, 1956). As age increases, the periods of inactivity shorten (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 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 (Hahn et al., 1989; Clancy et al., 2003). At a CA of approximately 30 weeks, continuous activity appears, but is present only during rapid eye movement (REM) sleep. At about 34 weeks CA, the EEG is predominantly continuous in the awake state. Continuity appears in non-REM (NREM) sleep at about 36 to 37 weeks CA. However, from that time until about 5 to 6 weeks after term, the EEG during periods of NREM sleep shows occasional 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 Figs. 4-4, 4-5, 4-6, 4-7, 4-8, 4-9, 4-10, 4-11, 4-12, 4-13, 4-14, 4-15, 4-16, 4-17, 4-18, 4-19, 4-20, 4-21, 4-22,4-23, 4-24, 4-25, 4-26, 4-27, 4-28, 4-29, 4-30 and 4-31.

Bilateral Synchrony

Before 27 to 28 weeks CA, EEG activity occurs in generalized bisynchronous bursts (Selton et al., 2000). 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 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 EEGs demonstrating CA-dependent synchrony are shown in Figs. 4-4, 4-5, 4-6, 4-7, 4-8, 4-9, 4-10, 4-11, 4-12, 4-13, 4-14, 4-15, 4-16, 4-17, 4-18, 4-19, 4-20, 4-21, 4-22, 4-23, 4-24, 4-25, 4-26, 4-27, 4-28, 4-29, 4-30 and4-31.

EEG Developmental Landmarks

An orderly appearance and disappearance of specific waveforms and patterns occurs with increasing CA (Fig. 4-3).

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TABLE 4-1. Developmental EEG characteristics of premature and term infants

Conceptional age (wk)

Continuity of background activity

Synchrony of background activity between homologous leads

EEG difference between wakefulness and sleep

Appearance and disappearance of specific waveforms and patterns

Reactivity to stimulus

Awake

Quiet sleep

Active sleep

Awake

Quiet sleep

Active sleep

27-28

D

D

++++

++++

No

 

NR

29-30

D

D

D

0

0

0

No

1.    Temporal theta bursts (4-6 Hz)

2.    Beta-delta complexes in central regions

3.    Occipital very slow activity

NR

31-33

D

D

C

+

+

++

No

1.    Beta-delta complexes in occipitotemporal regions

2.    Rhythmic 1.5-Hz activity in frontal leads in transitional sleep

3.    Temporal alpha bursts replace 4- to 5-Hz bursts (33 wk)

NR

34-35

C

D

C

+++

+

+++

No

1.    Frontal sharp-wave transients

2.    Extremely high voltage beta activity during beta-delta complexes

3.    Temporal alpha bursts disappear

R

36-37

C

D

C

++++

++

++++

Yes

1.    Continuous bioccipital delta activity with superimposed 12- to 15-Hz activity during active sleep

2.    Central beta-delta complexes disappear

R

38-40

C

C

C

++++

+++

++++

Yes

1.    Occipital beta-delta complexes decrease and disappear by 39 wk

2.    Tracé alternant pattern during NREM sleep

R

D, discontinuous activity; C, continuous activity; + + + +, total synchrony; 0, total asynchrony; NR, nonreactive; R, reactive; NREM, non-rapid eye movement.

From Hrachovy RA, Mizrahi EM, Kellaway P. Electroencephalography of the newborn. In: Daly DD, Pedley PA, eds. Current practice of clinical neurophysiology, 2nd ed. Philadelphia: Lippincott-Raven, 1991:202, with permission.

Beta-Delta Complexes

These complexes constitute the prime landmarks of prematurity and are 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 4-4, 4-5, 4-6, 4-7, 4-8, 4-9, 4-10, 4-11, 4-12, 4-13, 4-14, 4-15, 4-16, 4-17 and 4-18 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 and colleagues (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 they occur infrequently, 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 to 12 Hz) is most often present. The spatial distribution of the

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beta-delta complexes also changes with CA, becoming more prominent in the occipital and temporal areas with increasing age.

FIG. 4-1. Average duration of discontinuous periods in NREM sleep in the EEG of the premature infant. See text for details and references. (From Hrachovy RA. Development of the normal electroencephalogram. In: Levin KH, Luders HO, eds. Comprehensive clinical neurophysiology. Philadelphia: WB Saunders, 2000:387-413, with permission.)

FIG. 4-2. Development of interhemispheric synchrony in the EEG of the premature infant. See text for details and references. Before 27-28 weeks CA, there are generalized bisynchronous bursts. (From Hrachovy RA. Development of the normal electroencephalogram. In: Levin KH, Luders HO, eds. Comprehensive clinical neurophysiology.Philadelphia: WB Saunders, 2000:387-413, with permission.)

FIG. 4-3. Appearance and disappearance of developmental EEG landmarks from prematurity to 3 months postterm. See text for details and references. (From Hrachovy RA. Development of the normal electroencephalogram. In: Levin KH, Luders HO, eds. Comprehensive clinical neurophysiology. Philadelphia: WB Saunders, 2000:387-413, with permission.)

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 temporooccipital 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 marker is the appearance of rhythmic 4 to 6-Hz waves occurring 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 may often have a sharp configuration (Hughes, 1987; Werner et al., 1977) (Figs. 4-7, 4-8, 4-10, and 4-11). This activity appears at

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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 as temporal theta bursts (Figs. 4-12, 4-13 and 4-14). The presence of temporal alpha bursts is a very specific marker for 33 weeks CA, because they appear at the CA and are no longer present at 34 weeks CA.

Frontal Sharp Waves

Frontal sharp waves are isolated sharp waves of blunt configuration, usually with an initial surface-negative phase followed by a surface-positive phase, and have been referred to asencouche frontales (Dreyfus-Brisac, 1962; Kellaway and Crawley, 1964). They may be present at 34 weeks CA but attain maximal 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 after term.

These frontal sharp transients are bilaterally synchronous and symmetrical from the time of their first appearance. The initial surface-negative component lasts about 200 milliseconds. 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 (Figs. 4-15, 4-16, 4-20, 4-21, 4-22 and 4-23). They typically occur randomly as single events, predominantly in transitional rather than in REM or NREM sleep. However, they also may recur in brief runs and may be mixed with another normal feature of near-term infants, bifrontal delta activity (Fig. 4-23).

Distinguishing between the Waking and Sleep EEG

Until 36 to 37 weeks CA, distinguishing the various states of the wake/sleep cycle is based on empiric 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, whereas irregular respiration, rapid eye movements, and decreased muscle tone are associated with REM sleep.

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 and manifested according to their CA-dependent abundance, spatial distribution, and degree of synchrony (Figs. 4-17, 4-18and 4-19).

By 36 to 37 weeks CA, a clear distinction can be made between the waking EEG and the sleep EEG based on their inherent features, without reliance on clinical or polygraphic data (Figs. 4-25, 4-26, 4-27 and 4-28). In the awake EEG, beta-delta complexes are rarely present, and the awake background activity consists chiefly of continuous polyfrequency activity. 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 found. From the standpoint of determining CA, disappearance of the beta-delta complexes when the infant appears behaviorally awake constitutes an important marker of 38 weeks CA.

Before about 36 weeks CA, the background activity in NREM sleep is discontinuous (Fig. 4-18). 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 activity with alternating periods of high- and low-voltage activity (Fig. 4-27). 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 (Figs. 4-30 and 4-31).

The terms transitional sleep and 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 (Fig. 4-19), and by 37 weeks of 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 produces abrupt and pronounced generalized attenuation of voltage lasting as long as 5 to 10 seconds. A pattern less often seen may occur if the background activity is of low voltage, with predominant theta activity; then an effective stimulus may elicit high-voltage, generalized delta waves lasting 5 to 15 seconds (Ellingson, 1958; Kellaway and Crawley, 1964).

Spontaneous episodes of attenuation may be associated with self-arousal (Fig. 4-29). They occur in infants until about 2 weeks after 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 may occur in abnormal conditions of diffuse cerebral dysfunction, such as neonatal hypoxic-ischemic encephalopathy.

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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 rhythmic 1.5- to 2-Hz high-voltage activity in the frontal regions bilaterally (Fig. 4-23). This activity may occur in close association with frontal sharp transients, most prominently during transitional sleep. This pattern, characterized by bifrontal delta activity, has been referred to as “anterior dysrhythmia.” However, this is a misnomer, because it does not suggest abnormality and 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 have a simple diphasic morphology, with the initial component appearing as surface-negative in polarity, that occur randomly and that usually appear asynchronously on the two sides and during sleep can be considered normal (Fig. 4-24). Complex morphology, positive polarity, persistent localization, and occurrence during wakefulness are criteria for abnormality.

SUMMARY OF CONCEPTIONAL AGE-DEPENDENT FINDINGS

24 to 26 Weeks Conceptional Age

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

Synchrony. Bursts of activity during this epoch are synchronous on the two sides.

Landmarks. Beta-delta complexes are present during this epoch.

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

Reactivity. No reactivity to stimulation occurs.

27 to 28 Weeks Conceptional Age (Figs. 4-4 and 4-5)

Continuity. Electrical activity is episodic. Brief periods of generalized moderate-voltage activity may appear between periods of generalized electrical quiescence. The interburst interval is relatively long compared with that 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 regions, 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 (Figs. 4-64-74-8 and 4-9)

Continuity. The EEG remains discontinuous. Although brief periods occur in which behavioral and physiologic parameters suggest REM sleep, the EEG activity is relatively continuous. The duration of the interburst intervals is less than that in preceding epochs.

Synchrony. Asynchrony between the two hemispheres is a predominant feature.

Landmarks. Beta-delta complexes are present in the central regions. Temporal theta bursts are a consistent feature during this epoch. Occipital slow (delta) activity emerges during this epoch.

Wake/sleep cycles. The EEG is continuous during periods when behavioral and physiologic parameters indicate REM sleep. No clear-cut relation is seen between the stages of wakefulness and sleep on EEG activity except for a tendency for greater continuity of the background activity during REM sleep.

Reactivity. No reaction to stimulation occurs.

31 to 33 Weeks Conceptional Age (Figs. 4-104-114-124-13 and 4-14)

Continuity. Continuous activity remains an aspect of REM sleep, but the EEG is discontinuous at other times.

Synchrony. The degree of synchrony between hemispheres increases; however,

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this epoch is still marked by asynchrony when compared with epochs of infants at later ages.

Landmarks. Beta-delta complexes are present and are more prominent in the occipital and temporal regions than in the central regions. Temporal theta bursts persist until 32 weeks CA and are largely replaced by temporal alpha bursts at 33 weeks CA, which, in turn, disappear by 34 weeks CA.

Wake/sleep cycles. The EEG is continuous during REM sleep and discontinuous during wakefulness and NREM sleep.

Reactivity. No reaction to stimulation occurs.

34 to 35 Weeks Conceptional Age (Figs. 4-154-164-17 and 4-18)

Continuity. During wakefulness and REM sleep, the EEG is continuous, but is still discontinuous during NREM sleep, although the degree of discontinuity is less than that during the previous epoch.

Synchrony. Synchrony continues to be greater during this epoch than in early epochs, but asynchrony persists, chiefly in NREM sleep.

Landmarks. Frontal sharp transients (encouche frontales) become well defined by week 35 CA, although they may appear in rudimentary form during the week 34 CA. During this epoch, beta-delta complexes persist. Temporal alpha bursts disappear by 34 weeks CA.

Wake/sleep cycles. The EEG is continuous during wakefulness and REM sleep, but discontinuous during NREM sleep.

Reactivity. The background activity is reactive to stimulation of the infant. The response and its character are dependent on the state of the infant at the time of stimulation (Figs. 4-10 and 4-29).

36 to 37 Weeks Conceptional Age (Figs. 4-19 and 4-20)

Continuity. During wakefulness and REM sleep, the EEG is continuous, but episodes of discontinuity may occur in NREM sleep.

Synchrony. Synchrony continues to be greater during this epoch than in early epochs, now with most of activity synchronous on the two sides.

Landmarks. Frontal sharp transients persist. During this epoch, beta-delta complexes become less frequent. No new characteristic waveforms emerge, although bifrontal delta activity (a normal phenomenon) may be present during this epoch.

Wake/sleep cycles. EEG and physiologic features of wakefulness, REM sleep, and NREM sleep are seen. At 36 weeks CA, a clear distinction can be made, based on EEG criteria, between wakefulness and NREM sleep.

Reactivity. The background is reactive to stimulation.

38 to 40 Weeks Conceptional Age (Figs. 4-214-224-234-244-254-264-274-28 and 4-29)

Continuity. The EEG is continuous in all states of sleep and in wakefulness.

Synchrony. All activity becomes synchronous on the two sides by 40 weeks CA.

Landmarks. Frontal sharp transients persist. During this epoch, beta-delta complexes disappear from NREM sleep and are not present after 38 weeks CA.

Wake/sleep cycles. EEG and physiologic features of wakefulness, REM sleep, and NREM sleep are present. During this epoch, during NREM sleep, a modulation of the amplitude of the slow activity occurs with alternating periods of high and low voltage (tracé alternant) (Fig. 4-27).

Reactivity. The background is reactive to stimulation.

41 to 44 Weeks Conceptional Age (Fig. 4-30)

Continuity. The EEG is continuous in wakefulness and all stages of sleep.

Synchrony. Synchrony is virtually complete, as in the previous epoch.

Landmarks. Frontal sharp transients persist. No other immature waveforms are present.

Wake/sleep cycles. All stages of sleep and wakefulness are present. Tracé alternant begins to resolve by 44 weeks CA. NREM sleep is otherwise characterized by continuous slow-wave activity. Toward the end of this epoch, rudimentary sleep spindles may appear (Fig. 4-30). By 46 weeks CA, they are seen in all infants (Fig. 4-31).

Reactivity. The background is reactive to stimulation.

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LIST OF FIGURES

Background

Fig. 4-1. Average duration of discontinuous periods in NREM sleep in the EEG of the premature infant

Fig. 4-2. Development of interhemispheric synchrony in the EEG of the premature infant

Fig. 4-3. Appearance and disappearance of developmental EEG landmarks from prematurity to 3 months postterm

27 to 28 Weeks Conceptional Age

Fig. 4-4. Tracé discontinu and a burst of bilaterally synchronous, polyfrequency activity

Fig. 4-5. Central beta-delta complexes

29 to 30 Weeks Conceptional Age

Fig. 4-6. Central beta-delta complexes and discontinuity of the background

Fig. 4-7. Central beta-delta complexes and temporal theta bursts

Fig. 4-8. Bilateral, independent temporal theta bursts

Fig. 4-9. Occipital slow activity and central beta-delta complexes

30 to 32 Weeks Conceptional Age

Fig. 4-10. Beta-delta complexes in temporal region and temporal theta bursts

Fig. 4-11. Beta-delta complexes in the occipital, temporal, and central regions and temporal theta bursts

33 Weeks Conceptional Age

Fig. 4-12. Bilateral, asynchronous, temporal alpha bursts

Fig. 4-13. Temporal alpha burst, occipital beta-delta complexes, and tracé discontinu

Fig. 4-14. Beta-delta complexes in the temporal regions

34 to 35 Weeks Conceptional Age

Fig. 4-15. Beta-delta complexes in the central and temporal regions and frontal sharp transients

Fig. 4-16. Frontal sharp transients

Fig. 4-17. Awake: relative continuous background activity with some interhemispheric asynchrony

Fig. 4-18. NREM (quiet) sleep: discontinuous background activity

36 to 37 Weeks Conceptional Age

Fig. 4-19. Arousal from NREM (quiet) sleep: generalized voltage attenuation associated with clinical arousal

Fig. 4-20. Frontal sharp transients, continuous polyfrequency activity, and a paucity of beta-delta complexes

38 to 40 Weeks Conceptional Age

Fig. 4-21. Frontal sharp transients with continuous background activity

Fig. 4-22. Repetitive frontal sharp transients

Fig. 4-23. Rhythmic bifrontal delta activity and frontal sharp transients in transitional sleep

Fig. 4-24. Temporal sharp waves

Fig. 4-25. Awake: continuous, synchronous polyfrequency activity

Fig. 4-26. NREM (quiet) sleep: continuous slow activity

Fig. 4-27. Tracé alternant in deep NREM (quiet) sleep

Fig. 4-28. REM (active) sleep

Fig. 4-29. Transient arousal: generalized voltage attenuation

41 to 44 Weeks Conceptional Age

Fig. 4-30. Rudimentary sleep spindles

45 to 48 Weeks Conceptional Age

Fig. 4-31. Sleep spindles

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FIG. 4-4. 26 to 27 weeks CA. Tracé discontinu and a burst of bilaterally synchronous, polyfrequency activity. The EEG demonstrates a tracé discontinu pattern. A burst of bilaterally symmetrical, somewhat asynchronous activity is present. This activity is slow, with superimposed waves of faster frequency that resemble beta-delta complexes.

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FIG. 4-5. 27 to 28 weeks CA. Central beta-delta complexes. The background is characterized by tracé discontinu. Beta-delta complexes are present, predominantly in the right central region.

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FIG. 4-6. 29 to 30 weeks CA. Central beta-delta complexes and discontinuity of the background. Beta-delta complexes are present in the central regions bilaterally, but occur asynchronously on the two sides. The background activity is discontinuous with some low-voltage activity superimposed.

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FIG. 4-7. 29 to 30 weeks CA. Central beta-delta complexes and temporal theta bursts. Theta bursts are present independently on the right and left temporal regions. Beta-delta complexes are present bilaterally, although asynchronous and more prominent on the left.

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FIG. 4-8. 29 to 30 weeks CA. Bilateral, independent temporal theta bursts. Temporal theta bursts are present bilaterally, but independently. The background activity is discontinuous. The low-voltage rhythmic slow activity present during periods of quiescence is electrocardiogram artifact. This sample is from the same recording as in Fig. 4-9.

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FIG. 4-9. 29 to 30 weeks CA. Occipital slow activity and central beta-delta complexes. Moderate-voltage, very slow activity appears in the occipital regions bilaterally in the early portion of the sample. Beta-delta complexes that are more central in location are present later. The recording then becomes discontinuous, with ECG artifact superimposed. This sample is from the same recording as that in Fig. 4-8.

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FIG. 4-10. 30 to 32 weeks CA. Beta-delta complexes in temporal region and temporal theta bursts. Beta-delta complexes are present in the temporal regions in the latter half of the sample. Earlier a beta-delta complex is seen in the right central region, with theta bursts in the temporal regions bilaterally, but asynchronously. The background activity is discontinuous.

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FIG. 4-11. 30 to 32 weeks CA. Beta-delta complexes in the occipital, temporal, and central regions and temporal theta bursts. In the early portion of the sample, a beta-delta complex is present in the right occipital region, and then bilateral, independent temporal theta bursts appear. Later, beta-delta complexes are found in the central regions bilaterally. The background activity is discontinuous.

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FIG. 4-12. 33 weeks CA. Bilateral, asynchronous, temporal alpha bursts. Alpha bursts are present in the temporal regions, appearing independently and asynchronously on the two sides.

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FIG. 4-13. 33 weeks CA. Temporal alpha burst, temporal occipital beta-delta complexes, and tracé discontinu. Temporal bursts with a frequency in the alpha range are present on the left. Beta-delta complexes are present in the occipital and temporal regions. The background activity is discontinuous, although less so than in recordings of infants of a younger CA.

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FIG. 4-14. 33 weeks CA. Beta-delta complexes in the temporal regions. Beta-delta complexes are present in the temporal regions, greater on the left. A brief run of alpha-frequency activity appears in the left temporal region. The background activity is discontinuous. Periods of discontinuity are shorter, and the periods of bursting activity are longer than those in infants with a younger CA.

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FIG. 4-15. 34 to 35 weeks CA. Beta-delta complexes in the central and temporal regions and frontal sharp transients. Beta-delta complexes are present in the right central region followed by beta-delta complexes in the right temporal region. Rudimentary frontal sharp transients, higher in amplitude and more well formed on the right side in the early portion of the sample, suggest that the CA of this infant is early in the 34- to 35-week epoch.

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FIG. 4-16. 34 to 35 weeks CA. Frontal sharp transients. Bilaterally, synchronous diphasic sharp transients are present in the frontal leads.

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FIG. 4-17. 34 to 35 weeks CA. Awake: relative continuous background activity with some interhemispheric asynchrony. The background activity is continuous, with intermittent beta-delta complexes in the occipital regions. This sample is from the same recording of the infant in Fig. 4-18.

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FIG. 4-18. 34 to 35 weeks CA. Non-rapid eye movement (NREM; quiet) sleep: discontinuous background activity. A period of discontinuity appears during NREM sleep. This sample is from the same recording of the infant from Fig. 4-17.

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FIG. 4-19. 36 to 37 weeks CA. Arousal from non-rapid eye movement (NREM; quiet) sleep: generalized voltage attenuation associated with clinical arousal. The early portion of the sample demonstrates the discontinuity of NREM (quiet) sleep. The infant then self-arouses. This is associated with generalized voltage attenuation (and electromyographic artifact from the temporalis muscles).

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FIG. 4-20. 36 to 37 weeks CA. Frontal sharp transients, continuous polyfrequency activity, and a paucity of beta-delta complexes. Frontal sharp transients occur synchronously and symmetrically on the two sides. The background activity is relatively continuous with polyfrequency activity throughout, although there is still betacomplex activity posteriorly.

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FIG. 4-21. 38 to 40 weeks CA. Frontal sharp transients with continuous background activity. Bilateral, synchronous, frontal sharp transients occur randomly. Their occurrence is similar to those of earlier CAs when they first emerge as developmental landmarks, but at this CA, frontal sharp transients occur with continuous background activity.

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FIG. 4-22. 38 to 40 weeks CA. Repetitive frontal sharp transients. As at younger CAs, frontal sharp transients may occur in brief runs.

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FIG. 4-23. 38 to 40 weeks CA. Rhythmic bifrontal delta activity and frontal sharp transients in transitional sleep. Intermittent bifrontal delta activity, at times, is mixed with frontal sharp transients. Bifrontal delta activity is not a developmental landmark, per se, but this activity is considered a normal variation typically occurring in transitional or indeterminant sleep. See text for further details to differentiate normal from abnormal bifrontal delta activity.

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FIG. 4-24. 38 to 40 weeks CA. Temporal sharp waves. A moderate-voltage sharp wave in the left temporal region occurs in isolation. The background activity is normal for CA. Randomly occurring, moderate-voltage sharp waves do occur in the EEGs that are otherwise normal and in neonates who also are normal. A continuum of the degree of normality-to-abnormality of these waveforms is discussed in Chapter 5. This sample is presented to indicate that some temporal sharp waves can be considered normal, although the presence of temporal sharp waves does not constitute a developmental landmark.

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FIG. 4-25. 38 to 40 weeks CA. Awake: continuous, synchronous polyfrequency activity. The continuous and synchronous polyfrequency activity includes a mixture of alpha, beta, theta, and delta activity. (From Hrachovy RA. Development of the normal electroencephalogram. In: Levin KH, Luders HO, eds. Comprehensive clinical neurophysiology.Philadelphia: WB Saunders, 2000:387-413, with permission.)

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FIG. 4-26. 38 to 40 weeks CA. Non-rapid eye movement (REM; quiet) sleep: continuous slow activity. Continuous, relatively slow activity is synchronous on the two sides. Respiration is regular, and no REMs occur. (From Hrachovy RA. Development of the normal electroencephalogram. In: Levin KH, Luders HO, eds. Comprehensive clinical neurophysiology. Philadelphia: WB Saunders, 2000:387-413, with permission.)

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FIG. 4-27. 38 to 40 weeks CA. Tracé alternant in deep non-rapid eye movement (NREM; quiet) sleep. Periods of discontinuity occur during periods of deep NREM. (From Hrachovy RA. Development of the normal electroencephalogram. In: Levin KH, Luders HO, eds. Comprehensive clinical neurophysiology. Philadelphia: WB Saunders, 2000:387-413, with permission.)

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FIG. 4-28. 38 to 40 weeks CA. Rapid eye movement (REM; active) sleep. Continuous, synchronous EEG activity occurs. Respiration is irregular, and REMs are recorded on the electrooculogram channel. (From Hrachovy RA. Development of the normal electroencephalogram. In: Levin KH, Luders HO, eds. Comprehensive clinical neurophysiology.Philadelphia: WB Saunders, 2000:387-413, with permission.)

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FIG. 4-29. 38 to 40 weeks CA. Transient arousal: generalized voltage attenuation. The background activity is consistent with non-rapid eye movement (NREM; quiet) sleep. A brief episode of generalized voltage attenuation is associated with clinical arousal (the electromyogram and respiration channels indicate movement). After about 2 seconds, the EEG returns to NREM background.

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FIG. 4-30. 41 to 44 weeks CA. Rudimentary sleep spindles. Rudimentary sleep spindles are present in the midline central region in this 43-week CA infant during non-rapid eye movement (NREM; quiet) sleep. The background activity is continuous. This is not a typical finding in this CA epoch because spindles are most consistently present after 6 weeks post-term. However, on rare occasions, rudimentary spindles occur earlier, and when they first appear are present in the midline central region as shown.

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FIG. 4-31. 45 to 48 weeks CA. Sleep spindles. A: Brief sleep spindles are present first in the right central and then in the left central regions in the EEG of this 46-week CA infant. Both bursts have some midline central localization. B: This sample is a continuation of the sample shown in A. Now the spindles are longer, with those on the right beginning first, overlapping in time with that on the left. The spindles on the two sides occur simultaneously for a few seconds, and then the spindle on the right subsides while that on the left persists for several seconds.

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FIG. 4-31. (Continued)