Neurodiagn J.

52:176203, 2012 ASET, Missouri

EEG Maturation: Viability through Adolescence

Terri L. Scraggs, R. EEG T., BA
Neurodiagnostic Technology Program Student Orange Coast College Costa Mesa, California

ABSTRACT. As our brain matures, the EEG patterns change in a predictable manner. These cortical developments create age-specic waveforms that help decipher the normal maturation of the EEG. The majority of these changes take place during the neonatal period when waveform alterations occur week to week from discontinuous bursts to a more continuous background. From the neonatal period to infancy, background patterns of sleep and awake begin to show the continuity seen in older children and adults. With further maturation, the neonatal patterns of awake and sleep develop into the posterior dominant rhythm and distinguishable sleep structures of childhood. While pediatric patterns mirror the mature waveforms of adult EEG, their morphology and reactive response differentiates them. The goal of this article is to illustrate the normal maturation and development of the EEG using the agespecic waveforms and patterns seen in neonates, infants, children, and adolescence. KEY WORDS. Asynchrony, conceptional age, discontinuity, EEG maturation, neonate, pediatric, posterior dominant rhythm.

INTRODUCTION
From viability through early adulthood a multitude of changes occur on the EEG. Some patterns evolve becoming clear and organized while others are only seen during certain developmental periods and age ranges. With neonatal EEGs, agespecific electrographic features appear and either disappear or evolve every week. Due to these constant changes, the technologist must be capable of correlating the
Author Email address: t.sweeney.1@hotmail.com Received: August 26, 2011. Accepted for publication: November 4, 2011.

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pattern development with correct conceptional age to establish the normal neonatal EEG. From full term to the first three months of life, the patterns of the neonate dissipate and evolve into immature adult patterns. Neonatal sleep cycles persist, but there is a decrease in the amount of time spent in each sleep cycle as well as a switch in the stage of sleep onset. Undeveloped forms of identifiable sleep patterns emerge. Further development of the adult patterns of awake, drowsy, and sleep occur throughout the infants first year of life. A posterior dominant rhythm is discernible and continues to increase in frequency. New mature drowsy and sleep patterns surface and develop. Due to the presence of recognizable developing adult sleep patterns, obtaining awake, drowsy, and sleep tracings is highly desirable. Through childhood and adolescence the early discontinuity of the neonatal EEG has subsided and mature, recognizable waveforms arise during awake, drowsy, and sleep. The posterior dominant rhythm reaches alpha frequencies, non-rapid eye movement (NREM) sleep stages are fully developed, and reactivity to activation procedures is possible. The ability to recognize developing patterns and correlate age specific waveforms is important when establishing the normal maturation of the EEG.

NEONATAL EEG PATTERNS

Neonatal EEG patterns are only prominent for several weeks at a time and correlate directly with the age of the neonate (Table 1). Knowledge of the conceptional age (CA) is essential for correct EEG interpretation. The conceptional age is determined by adding the gestational age (time in weeks calculated from first day of last menstrual period) and chronological age (age since birth). Active Sleep Active sleep is a normal sleep pattern of a neonatal and term infant. Neonates less than 37 weeks CA spend 50% or more of their sleep cycle in this state. This sleep pattern of continuous EEG activity correlates to the adult rapid eye movement (REM) sleep cycle. Active sleep is characterized by rapid eye movements, irregular heart rate and respirations, frequent body jerks or movements, atonic facial electromyogram (EMG) with occasional sucking, smiling or grimacing, and brief periods of apnea. Quiet Sleep Quiet sleep is a normal sleep pattern of a neonate and term infant. Quiet sleep develops into the NREM sleep cycles of adults. The EEG changes from a

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Table 1. NEONATAL PATTERNS: AGE OF OCCURANCE AGE OF ONSET 2445 WEEKS CA 3436 WEEKS CA 3637 WEEKS CA 3840 WEEKS CA 26 WEEKS CA 28 WEEKS CA 34 WEEKS CA 35 WEEKS CA 4144 WEEKS CA 3334 WEEKS CA 4448 WEEKS CA 37 WEEKS CA 3235 WEEKS CA 3234 WEEKS CA 35 WEEKS CA 3637 WEEKS CA 4546 WEEKS CA 3840 WEEKS CA 4145 WEEKS CA 2629 WEEKS CA PROMINENT AGE OF DEVELOPMENT AGE OF TERMINATION

NEONATAL PATTERN

DISCONTINUOUS/TRACE DISCONTINU

EEG MATURATION

TRACE ALTERNATE LOW VOLTAGE IRREGULAR/ACTIVITE MOYENNE CONTINUOUS SLOW WAVE SLEEP/HIGH VOLTAGE SLOW DELTA BRUSHES MULTIFOCAL SHARPS ENCOUCHE FRONTALIS ANTERIOR SLOW DYSRHYTHMIA/ MONORHYTHMIC FRONTAL SLOWING SLEEP SPINDLES REACTIVITY

34 WEEKS CA: WAKE; 36 WEEKS CA: QUIET SLEEP 4446 WEEKS CA 48 WEEKS DEVELOPS INTO ADULT REM STAGE SLEEP 46 WEEKS POST TERM DEVELOP INTO NREM PATTERNS 4243 WEEKS CA 44 WEEKS CA 44 WEEKS CA 46 WEEKS CA SYNCHRONOUS BY 2 YEARS CONTINUOUS

CA conceptional age; REM rapid eye movement; NREM non-rapid eye movement

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discontinuous pattern to a continuous high amplitude background. During this sleep stage, facial EMG is tonic but there is a decrease in eye and gross body movements. Regular heart rate and respirations are noted. Continuity-Discontinuity When the first electrical impulses from the brain are revealed, the activity is discontinuous. It consists of long periods of generalized attenuated or flat activity interrupted by high amplitude bursts of mixed frequencies and waveforms. The periods of quiescence between bursts can be as short as 6 seconds or as long as 25 to 30 seconds. As the conceptional age increases the interburst intervals decrease. This pattern of discontinuity is termed trace discontinu (TD). Trace discontinu is seen in all three stages of neonatal EEG (awake, active sleep, and quiet sleep) until ages 32 to 34 weeks. It remains the prominent pattern for quiet sleep until 36 weeks CA. Bilateral Synchrony Prior to 27 to 28 weeks CA, the discontinuous EEG activity consists of generalized bisynchronous bursts. After this age, the bursts become asynchronous over homologous hemispheres. However, as the brain matures, the bursts slowly begin to synchronize. By 37 weeks, 100% of the bursts are again synchronous (Lombroso 1985, Tharp 1990). Trace Alternant As the neonate ages, the trace discontinu activity in quiet sleep develops into another discontinuous pattern of high amplitude delta bursts, but with shorter interburst intervals. Trace alternant (TA) consists of 2 to 4 second interburst intervals with amplitude of 25 to 50 V (Figure 1); instead of the quiescence seen in trace discontinu. The synchronous bursts are in the delta range with amplitude as high as 300 V. This pattern of trace alternant appears between 34 to 36 weeks CA and persists as the dominant pattern of quiet sleep until around age 46 weeks CA, when it is replaced by more mature patterns (Husain 2005). Continuous Slow Wave Sleep/ High Voltage Slow Once a neonate reaches term, the interburst intervals shorten and the pattern of trace alternant advances into continuous 25 to 150 V slow delta activity termed continuous slow wave sleep or high voltage slow (HVS). Continuous slow wave sleep emerges around week 38 CA but is most prominent by 45 to 46 weeks. This pattern is thought to be the morphologic precursor to NREM adult sleep patterns (Fisch 1991, Quigg 2006).

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FIG. 1. Trace alternant pattern in a 36-week-old conceptional infant during quiet sleep. Synchronous bursts of high amplitude slow waves with interburst intervals of around 2 to 4 seconds and amplitude greater than 25 V are seen. Delta brushes are present during the bursts. Heart rate and respirations are regular.

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Activite Moyenne/ Low Voltage Irregular By week 36 CA, the trace discontinu of active sleep and awake are replaced by a continuous pattern of rather featureless generalized theta activity intermixed with lower amplitude delta activity. Delta Brushes Delta brushes are the telltale sign of prematurity. They consist of random 0.3 to 1.5 Hz delta waves with overriding bursts of 18 to 22 Hz beta giving the illusion of a brush or ripple (Figure 2). They are typically asynchronous and asymmetrical over homologous areas. They first present in awake and active sleep around 26 weeks CA, where they are infrequent and centrally dominant. Around 33 weeks delta brushes are more prominent in NREM or quiet sleep with temporal-occipital dominance. Delta brushes are infrequent at term and disappear by 42 to 43 weeks CA (Mizrahi et al. 2004). Monorhythmic Delta Activity These occipital dominant, monorhythmic, positive, 0.5 to 1 Hz delta waves form the delta wave in delta brushes. They can be synchronous and symmetrical and last from 2 to 60 seconds. They appear at 24 to 25 weeks CA, are dominant between 31 to 33 weeks and disappear around 35 weeks. Temporal Theta Rhythmic temporal theta bursts appear at 26 weeks CA, are maximal at 30 to 32 weeks and transition into temporal alpha around 33 to 34 weeks CA. In neonates, temporal theta bursts are short runs of 4 to 6 Hz with a sharp configuration resembling sawtooth waves (Figure 3). They arise independently over homologous hemispheres. Multifocal Sharps From 32 to 34 weeks CA there is an increase in the number of multifocal sharp transients in all sleep stages. While they occur in any area of the brain, they are most common in temporal areas. Normal multifocal sharp waves have amplitude of less than 75 V, duration of less than 100 msec and are biphasic (Husain 2005). By 37 weeks they are less abundant and seen only during quiet sleep. Multifocal sharps finally disappear by 44 weeks CA.

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FIG. 2. The patient is a 38-week-old conceptional age neonate. Asynchronous tempro-occipital dominant delta brushes are recorded.

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FIG. 3. 34-week-old conceptional age patient with background of low voltage irregular in active sleep. Bursts of rhythmic 5 Hz temporal theta are seen unilaterally over the right hemisphere (boxes). Encouche frontalis is present in the 12th second. EKG artifact is seen in many channels.

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Encouche Frontalis Encouche frontalis or frontal sharp transients (FST) are bi- or polyphasic, sharply contoured waves that can be unilateral, bilateral, asymmetric, or synchronous. They are seen maximally over the frontal and midfrontal region and are accentuated with transition from active to quiet sleep. While they can appear as early as 28 weeks, they are prominent at 34 to 35 weeks, and are rarely seen after 48 weeks CA. Anterior Slow Dysrhythmia/ Monorhythmic Frontal Slowing First seen around 35 weeks CA, anterior slow dysrhythmia consists of short runs of monophasic, rhythmic, bilateral 2 to 4 Hz delta activity seen in the anterior region. The pattern is seen in all sleep states but is most prominent in transitional sleep. Although its name may suggest an abnormality, anterior slow dysrhythmia is a normal neonatal pattern. It is seen quiet often in conjunction with frontal sharp transients.

INFANT, PEDIATRIC, AND ADULT EEG PATTERNS

Once a neonate reaches term, the background activity becomes continuous; developing into the structured waveforms of adult EEG. While most of the patterns that emerge during infancy and childhood are rudimentary type of adult waveforms, there are a few patterns only seen in childhood and adolescence (Table 2). Sleep Spindles Sleep spindles may emerge as early as 40 weeks CA in quiet sleep, but are not seen consistently until ages 2 to 3 months. They are predominantly found in the central and parasagittal regions during N2 sleep. At 2 to 3 months, they consist of lowmoderate amplitude 12 to 14 Hz rhythmic runs lasting about 4 seconds. Sleep spindles in infants and children can be sinusoidal, comb shaped, or have a spiky appearance; especially when combined with vertex waves. They can be asynchronous or have shifting symmetry until 2 years of age; after that any asynchrony may be perceived as abnormal. Vertex Waves Vertex waves (or V-waves) may appear around the vertex during N1 and N2 sleep as early as 3 to 4 months; however, they are well developed by 6 months. Compared to adults, the V-waves of children and adolescents are higher in amplitude, can be anterior dominant, have a spikier appearance, and a briefer duration. They usually

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Table 2. PEDIATRIC PATTERNS: AGE OF OCCURANCE

PEDIATRIC PATTERN REM SLEEP VERTEX VERTEX 812 MONTHS 23 YRS 12 YRS 814 YRS 816 yrs 918 YRS 1314 YRS 910 YRS 12 YRS 215 YRS 34 YRS 34 YRS 35 MONTHS GENERALIZED

STATE

AGE OF ONSET LOCATION

PROMINENT AGE OF DEVELOPMENT AGE OF TERMINATION

REM ONSET SLEEP

NREM STAGES 23 MONTHS I & II K COMPLEX NREM STAGES 23 MONTHS II & III HYPNOGOGIC/HYPNOPOMPIC NREM STAGES I 46 MONTHS HYPERSYNCHRONY WAKE 6 MONTHS NREM STAGES I 3 MONTHS & II WAKE 34 YRS OCCIPITAL C3 and C4 OCCIPITAL 5 YRS 4 YRS 34 YRS 3 MONTHS 56 MONTHS 23 YRS 10 YRS NREM NREM STAGE I & II NREM STAGES I & II WAKE NREM STAGE I WAKE NREM STAGE I POSTERIOR TEMPORAL REGION POSTERIOR POSTERIOR OCCIPITAL FRONTAL GENERALIZED ANTERIOR DOMINANT OCCIPITAL OCCIPITAL 10 YRS 5 YRS 21 YRS

VERTEX WAVES

ASSUMES ADULT RANGE AT 911 YRS AT 13 YRS REDUCTION IN AMPLITUDE AT 13 YRS REDUCTION IN AMPLITUDE 56 YRS

SHUT EYE WAVES CONE WAVES

EEG MATURATION

POSTERIOR SLOW WAVES OF YOUTH MU RHYTHM POSITIVE OCCIPITAL SHARP TRANSIENTS OF SLEEP 14 & 6 POSITIVE SPIKES

LATE ADULTHOOD 70 YRS DECREASES IN INCIDENCE REACHES ADULT RANGE OF 1013HZ BY AGE 10 36 YEARS 16 YRS 20 YRS

POSTERIOR DOMINANT RHYTHUM

POSTERIOR BETA LAMBDA FRONTAL RHYTHMIC THETA WITH DROWSY

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REM rapid eye movement; NREM non-rapid eye movements; YRS years

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appear in bursts or trains, which is not common in adults. Shifting asymmetries may be seen with V-waves in younger children. K-complex K-complexes consist of a broad V-wave accompanied by a run of sleep spindles (Figure 4). They also appear during the same age range as V-waves, and have the same topography but a longer time constant. K-complexes can be elicited by sensory stimulation, usually auditory. Positive Occipital Sharp Transients of Sleep (POSTS) POSTS are reported to appear around age 5 years as the occipital delta of sleep begins to decrease (Yamada and Meng 2010). These surface positive mono- or diphasic waves are bilaterally synchronous but can be asymmetric between posterior arrays. While they appear as transient sharp waves, in children they are mostly seen as high amplitude 4 to 5 Hz runs, lasting 1 to 2 seconds, and repeating every 4 to 6 seconds. They are seen during late N1 sleep stage and disappear with deep sleep. Hypnagogic Hypersynchrony Hypnagogic hypersynchrony (HH) is the pattern seen in infants and children during the transition from drowsiness to sleep. It consists of high amplitude, paroxysmal, bilateral, rhythmic bursts of 3 to 5 Hz waves (Figure 5). HH is a diffuse pattern, although it tends to be anterior dominant. It may emerge as early as 4 months but is seen in the majority of infants between 6 to 8 months old. HH may be continuous from ages 8 to 12 months but as the child ages a more paroxysmal type of HH is seen. The pattern begins to dissolve by age 2 years and is usually gone by age 12 years. Since this is only a transition pattern, it will disappear once N2 sleep is reached. Cone Waves Cone waves are another waveform seen during sleep. They appear around 6 months, when transition from quiet sleep to adult NREM patterns takes place. These positive, monophasic, high amplitude, cone shaped delta waves are posterior dominant. They are commonly observed during sleep stages N2 and N3 in patients up to 5 years of age.

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FIG. 4. High amplitude synchronous and symmetrical K-complex and sleep spindles are seen in this 20-month-old patient during NREM sleep. Circumferential and longitudinal bipolar montages are both displayed.

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FIG. 5. aly.

High amplitude anterior dominant hypnagogic hypersynchrony in a 2-year-old patient with global delay and microceph-

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Shut Eye Waves Shut eye waves are seen in the occipital region following the onset of eye blinks. They appear in children between 6 months and 2 years. The waveform is sharp, diphasic, and high amplitude. Lambda Waves Lambda waves are found mostly in patients 6 months to 10 years. These occipital dominant bi- or triphasic transients are only elicited with eyes open and visual stimulation such as scanning a busy picture. Once the lights are off or visual stimuli are removed, the waveforms disappear. Posterior Slow Waves of Youth Posterior slow waves of youth (PSOY) are occipital dominant 2 to 3 Hz delta waves and are considered part of the normal alpha rhythm (Figure 6). They are best seen with eyes closed in a relaxed wakeful state in adolescents 6 to 14 years old. PSOY are rarely seen before 2 years or after 21 years. They occur as sporadic single waves or as bursts of transient waves interspersed by one or several seconds or regular background activity. PSOY are usually bisynchronous but can have shifting symmetry (Stern 2005). Mu Rhythm Since mu rhythm occurs in only 20% of adolescents and young adults, the presence or absence of this rhythm is considered normal. 7 to 11 Hz mu rhythm is located in the central region and has a typical arciform or comb shaped appearance giving it the name rhythme rolandique en archeau (Yamada and Meng 2010). It occurs in trains or bursts which can be asynchronous and asymmetric. Mu should only be considered abnormal if frequent trains appear exclusively on one side. It can be seen with eyes open or closed and may extend into sleep stages N1 and N2. Mu rhythm can be confirmed by its blocking or attenuation with the intention to move or actual movement of a contralateral upper limb. It is rarely seen before age 4 years or in the elderly and is twice as common in girls (Swaiman et al. 1994). 14 and 6 Hz Positive Spikes 14 and 6 Hz positive spikes have their onset at ages 3 to 4 years, peak during adolescence (mostly at ages 12 to 13 years) and decrease with age. Sleep stages N1 and N2 best demonstrate 14 and 6 Hz spikes; wakefulness, N3, and REM sleep

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FIG. 6. EEG of an 8-year-old female in a bipolar longitudinal montage. Posterior slow waves of youth are intermixed with 8 to 9 Hz occipital alpha rhythm. In the 9th second there is attenuation of alpha and posterior slow waves with eye opening.

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suppress them. These spikes are seen as bisynchronous or unilateral positive runs of 14 Hz or 6 Hz or a combination of both. Their arciform appearance can resemble sleep spindles, especially the bursts of 14 Hz. The bursts last less than 2 seconds and are maximal over the posterior temporal region. Due to their broad field, they are best viewed in a referential montage. While typically considered a normal variant, 14 and 6 Hz positive spikes may indicate a metabolic encephalopathy if seen in great abundance (Stern and Engel 2005).

NORMAL AGE RELATED DEVELOPMENT OF EEG

Premature infants less than 29 weeks CA At this young age the EEG is completely discontinuous. This trace discontinu pattern shows long periods (10 to 20 seconds) of nearly flat background interrupted by bilaterally synchronous high amplitude posterior dominant bursts. Occasional bursts of rhythmic occipital delta and temporal theta activity are noted during this discontinuity. Delta brushes are characteristic of this age. They are infrequent and central or posterior dominant. There are relatively no behavioral changes between awake and sleep except, perhaps, a few gross body movements. Eye movements are very rare and respiration is irregular. Since there is no differentiation between awake and sleep, it is difficult to accurately determine the age of the neonate. Conceptional age 29 to 31 weeks Although the EEG is still discontinuous, there is an electrographic difference of wakefulness and active sleep from quiet sleep. The trace discontinu pattern is more prominent in quiet sleep. The occipital dominant bursts are now asynchronous and interburst intervals are shorter than in preceding periods. Monorhythmic occipital delta and temporal theta activity persist. During active sleep and awake, the interburst intervals are shorter than in quiet sleep. The majority of delta brushes are observed in active sleep. Rapid eye movement, obvious body movements, and the occasional regular respirations help to differentiate the stages; however, much of the recording is in transitional sleep. During transitional or intermediate periods, features of both sleep states are apparent and precise classification is often not possible (Pedley et al. 1981). Conceptional age 32 to 34 weeks Active sleep and quiet sleep become more distinguished as active sleep develops into a continuous pattern from 32 to 34 weeks conceptional age. Quiet sleep still presents as trace discontinu but the bursts are 80% synchronous and interburst

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intervals (IBI) are less than 10 seconds. Delta brushes are frequently present in active sleep and awake over the occipital and central areas. Temporal theta continues but transitions into temporal alpha bursts. Multifocal sharp transients appear infrequently in all states. There is a great increase in eye movement and decrease in electromyogram (EMG) during active sleep. Stimulation, mostly auditory and tactile, causes a reactive attenuation of the EEG in neonates 34 weeks. Conceptional age 34 to 37 weeks EEG is continuous during awake and active sleep making all three periods distinguishable at a conceptional age of 35 to 37 weeks. The continuous pattern of active sleep and awake develop into low voltage irregular (LVI) pattern (Figure 7). The increase in reactivity marks the distinction between awake and active sleep. Quiet sleep is still discontinuous, but as the IBI amplitude increases to more than 25 V, the pattern changes to trace alternant. The bursts are 85% synchronous between hemispheres. Delta brushes are seen less frequent and only in quiet sleep. Temporal alpha bursts disappear. Multifocal sharp transients are scarce and seem to be replaced with frontal sharp waves or encouche frontalis. Frontal sharps occur most often in sleep. Anterior slow dysrhythmia is present at this age as well. EEG reactivity is present in all states appearing as diffuse flattening. Conceptional age 37 to 40 weeks At a conceptional age of 37 to 40 weeks, there is a clear cut distinction between awake, active sleep, and quiet sleep. LVI continues to be the pattern during wakefulness. EEG activity during wakefulness is similar to sleep-onset REM but appears more organized with some rhythmic theta waves (Pedley et al. 1981). Active sleep consists of either LVI or a mixed pattern of irregular theta and delta frequencies. In quiet sleep, trace alternant is the dominant pattern; however, if quiet sleep persists high voltage slow waves of delta can be seen. The bursts in trace alternant are 100% synchronous at this age. Delta brushes are only seen in quiet sleep, if they are present at all. Encouche frontalis and monorhythmic frontal delta are numerous, particularly in the transition between active sleep and quiet sleep. Sporadic multifocal sharps are still normal but rare. Term infant to 3 months (40 to 48 weeks CA) A term infant is born between 37 and 42 weeks CA. During this age, neonatal patterns gradually disappear and are replaced with elementary adult patterns. When the infant is awake, the low voltage irregular pattern develops into a background of central dominant, non-reactive, rhythmical waves of 4 to 6 Hz. These waves appear

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FIG. 7.

Low voltage irregular pattern in a 37-week 2-day conceptional age female. Patient is in active sleep.

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synchronous and symmetrical by one month of age (Werner et al. 1977). During quiet sleep, continuous slow wave sleep replaces trace alternant as the dominant pattern (Figure 8). If trace alternant is present the bursts are 100% synchronous and the IBI are less than 4 seconds. Encouche frontalis, slow anterior dysrhythmia, and multifocal sharps disappear at the end of this epoch. Generalized slowing and an increase in amplitude may depict onset of drowsy; however, correlating the background with clinical observation is difficult at this age since infants may still have their eyes open when drowsy. A decrease in movement and muscle tone are also helpful in determining drowsiness. At term, the total amount of time spent in sleep is 50%, most of which has its onset in active sleep. By 46 weeks CA, the majority of sleep onset is in quiet sleep (Fisch 1991). This shift in sleep onset parallels the adult transition of awake to NREM sleep stages. Sleep spindles may be present, but will be underdeveloped and asynchronous. An infant EEG may show either diffuse flattening or a burst of theta and delta in response to tactile or auditory stimuli. Development of the Infant EEG: 3 Months to 12 Months: Awake, Drowsy, Sleep By three months of age, the awake portion of the EEG shows a distinguishable 3 to 4 Hz posterior dominant rhythm as well as a rhythmic central dominant 5 to 8 Hz background (Dreyfus-Brisac and Curzi-Dascaolva 1975). Because the infants eyes are usually open during the awake portion, central rhythmic activity is more identifiable than the posterior dominant rhythm. It may be necessary for the technologist to passively close the eyes for a few seconds in order to elicit the posterior dominant rhythm (Figure 9). As the infant ages, the posterior dominant rhythm becomes more regular and increases in frequency from 5 Hz at ages 5 to 6 months to 6 to 8 Hz by the end of the first year of life (Fisch 1991). At three months, the distinctive pattern of hypnagogic hypersynchrony emerges replacing the high amplitude 2 to 3 Hz rhythm seen during drowsiness. This high amplitude bisynchronous rhythmic 3 to 6 Hz activity can be paroxysmal or continuous for several minutes either at the beginning or end of the sleep cycle. When occurring at the end of sleep, the arousal transition is referred to as hypnopompic hypersynchrony. By 6 to 8 months, nearly 100% of normal infants display this drowsy pattern. Low amplitude posterior 20 to 25 Hz beta also appears during sleep stages N1 and N2 in infants 5 to 6 months of age. This rhythm shifts to the anterior regions as the infant ages. During the first year of life, several changes occur with sleep activity. Active sleep develops into REM sleep transforming the LVI pattern of neonates into the asynchronous low amplitude mixed frequencies of the adult REM sleep stages. The time spent in REM decreases from 40% of the sleep cycle at 3 to 5 months to only 30% by the

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FIG. 8. Continuous high voltage slow wave sleep in a 46-week-old patient. Overriding beta activity is caused by phenobarbital.

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FIG. 9. 3 to 4 Hz posterior dominant rhythm in a 5-month-old infant. Occipital rhythm is synchronous, symmetrical, and high amplitude.

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end of the first year of life. After 3 months, REM sleep is reached after 40 to 50 minutes are spent in NREM sleep. NREM sleep stages are clearly defined with the development of sleep spindles as well as the emergence of vertex waves and Kcomplexes. Sleep spindles become clearly expressed by 3 to 4 months of age, and are most abundant between 4 to 6 months occurring in runs lasting 8 seconds or more. Sleep spindles in children under 2 years are asynchronous but should have shifting asymmetry throughout the EEG (Figure 10). They appear comb shaped rather than the sinusoidal shape of adult spindles. While vertex waves and K-complexes may be apparent in a neonatal EEG, they are not well developed until 5 to 6 months of age. In contrast to adults, infant V-waves are higher in amplitude, have a spiky appearance, and often occur in spontaneous bursts or trains. V-waves are synchronous from birth, but may be asymmetric during early stages of sleep (Westmoreland and Stockard 1977). K-complexes tend to have a longer duration that V-waves. They appear suddenly during N2 and N3 sleep and can be elicited with auditory stimulation such as tapping a pen on the desk. Background sleep patterns also change as the transition is made from quiet sleep into NREM stages. High voltage slow develops into more generalized, posterior dominant delta activity featuring occasional isolated, monophasic occipital slow waves called cone waves. Cone waves appear only from infancy through mid-childhood and are prominent in N2 and N3 sleep. Pediatric to early Adult EEG: Ages 1 to 19 years: Awake, Drowsy, Sleep After the first year of life, the restful waking record shows major differentiation from immature waveforms into adult patterns. By three to four years of age, a visibly developed alpha rhythm of 8 Hz is present. The rhythm increases to 9 Hz by year 8 to 9 and reaches the mean frequency of 10 Hz by 15 years. The voltage of EEG activity in many young children is higher than that of older children and adults, and appropriate reduction of sensitivity (10 v/mm or 15 v/mm) should be used (ACNS 2006). The amplitude of the alpha rhythm also increases up to the age of 10 years; sometimes exceeding 100 V. Low amplitude is rarely seen in children. By 15 years, the mean amplitude should be within 50 to 60 V. The alpha rhythm is appreciated with eyes closed and is clearly attenuated with eyes open. With younger children, it may still be necessary to gently aid in eye closure to elicit the posterior rhythm and differentiate it from 7 to 10 Hz central rhythms. From ages 6 months to 2 years diphasic, sharply contoured waveforms may appear over the occipital regions following eye blinks. These posterior slow wave transients are termed Shut Eye Waves and should not be mistaken for abnormal activity. At 2 to 3 years lambda waves also emerge during wakefulness. Lambda waves are occipital sharps occurring only while awake and with eyes open, in a well-lit environment, while scanning a picture or complex design that includes visual details (Stern and Engel 2005). Discerning between shut eye waves and lambda waves may be difficult since blinking does occur

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FIG. 10.

Asymmetric sleep spindles in a 3-month-old full term male. The sleep spindles persist for several seconds.

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when scanning a picture; however, lambda waves will continue into early adulthood while shut eye waves are largely seen in ages 2 to 3 years. Around 8 years of age, when the alpha rhythm reaches about 9 Hz, occipital slow waves may be present intermixed or superimposed with the alpha rhythm. These posterior slow waves of youth most commonly occur during ages 6 to 12 years but can be seen up to age 20. They consist of a single slow wave interspersed with alpha waves or may occur in a train. PSOY are considered to be formed by the alpha rhythm and thus have the same amplitude and similar reactivity. As such, they are only visible with eyes closed in a waking restful state and attenuate upon alerting, open eyes and sleep. Around 5 years of age, rhythmic bursts of 7 to 11 Hz may be seen asynchronously over the centroparietal regions (Figure 11). Mu rhythm is present in 10 to 20% of EEGs, usually in younger female patients. Since it is a central rhythm unreactive to eye opening, mu is believed to have developed from the rhythmic central theta present in awake infants (Werner and Stockard 1977). In those who have mu, it will remain a awake pattern into adulthood (Stern and Engel 2005). Between 6 months and 2 years of age, the prominent pattern of drowsiness remains hypnagogic hypersynchrony. As a child ages, the patterns frequency will increase and become a less continuous more paroxysmal pattern. During this same age range,

FIG. 11. 9 Hz mu rhythm present over right hemisphere (maximal at C4). Patient is awake with eyes open.

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20 to 25 Hz beta activity increases with drowsiness and becomes more centrooccipital. Beta moves anteriorly and is frontocentral dominant in older children and adults. The normal adult patterns of drowsiness become established around 10 years of age. Slow lateral eye movement is the earliest sign of drowsiness. After that, alpha slows by 1 to 2 Hz and less muscle movement is observed on the EEG. At 10 years of age, frontal rhythmic theta activity dominates during drowsiness. After 3 months of age, all NREM and REM sleep stages show maturation as well as development of new patterns. REM now only occupies 25% of the total sleep time. During NREM sleep, patterns reach mature formations. Sleep spindles are fully developed, synchronous, and symmetrical by 2 years. The amplitude and incidence of V-waves and K-complexes decrease at 3 to 4 years until the adult waveform is attained. At 4 years of age positive occipital sharp transients of sleep are seen during late drowsiness and light sleep. In children, POSTS can have high amplitude and occur in trains or runs. With age, amplitude decreases and POSTS may occur spontaneously either bilaterally or independently over both hemispheres (Figure 12). POSTS persist through adulthood. Another phenomenon occurring in late drowsiness and light sleep are 14 and 6 Hz positive bursts with an onset around ages 3 to 4 years, maximal expression during adolescence, and a decrease in incidence with increasing age (Swaiman et al. 1994).

ACTIVATION PROCEDURES
Activation procedures are sensory stimulations intended to alter the physiological state of the patient. The most routine activation procedures in any EEG laboratory are hyperventilation, photic stimulation, and sleep (Yamada and Meng 2010). The first incidence of reactivity is seen with sleep in a 32 to 34 week CA neonate. At this age, sensory stimulation, usually tactile or auditory, is enough to elicit a change on the EEG. This activation can cause generalized attenuation of activity, bursts of high amplitude slowing, or a change in sleep state. Around 2 weeks post term, self arousal can also cause spontaneous episodes of attenuation (Mizrahi et al. 2004). Sleep itself is an important activation procedure because certain epilepsy syndromes have interictal discharges that appear more frequently during sleep (Quigg 2006). Since sleep is a powerful activation, it is often necessary to use sleep deprivation to promote the occurrence of sleep (Sweeney et al. 1997). Infants spend the majority of their time in sleep, so sleep deprivation is not useful until around 2 to 3 years of age. Sleep deprivation may cause the child to become agitated and uncooperative; however, crying will further exhaust the child and aid in reaching sleep. Other patients may fall asleep during the hook up so it may be essential to keep the child engaged until a posterior dominant alpha rhythm is obtained.

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FIG. 12. Trains of synchronous and symmetrical posterior occipital sharp transients of sleep (POSTS) in a 14-year-old female during N2 sleep. Sleep spindles are seen in the 7th second.

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Children 3 to 4 years and older can cooperate with hyperventilation (HV) and seem to have much more enthusiasm for the procedure than adults (Blume and Masako 1999). A normal response with hyperventilation is rhythmic, bisynchronous, high amplitude theta and delta waves termed HV build up. With children, HV build up is posterior dominant, high in amplitude and incidence, and occurs within 1 to 2 minutes of onset. After ages 7 or 8 years, the slow wave response is usually maximal over the anterior head region (Westmoreland and Stockard 1977). HV build up is lower in amplitude and is usually first noted at the beginning of the third minute of HV in teenagers and adults. The hyperventilation response can also be elicited with crying and sobbing if the child proves uncooperative. A normal photic stimulation response of photic driving can be elicited at low frequencies as early as 3 months of age (Stern and Engel 2005). At this early age, occipital bisynchronous sharply contoured transients are seen time locked with strobe flashings at frequencies less than 5 Hz. Young children have driving in the theta range. Driving at higher frequencies, between 8 to 20 Hz, usually appears at ages 7 to 8 years when the posterior dominant rhythm reaches the alpha range. The amplitude of the photic driving response is generally high in children and decreases with age.

CONCLUSION
Many changes occur during the maturation of the EEG; and while the waveforms may seem episodic, there is a natural flow and evolution of both the awake and sleep EEG. The first few months of life show a rapid maturation from the discontinuous patterns of active and quiet sleep into continuous waveforms. Within the continuous sleep patterns emerge sleep spindles and vertex waves that persist throughout childhood and into adolescence. During the first year these rudimentary signs of sleep become established NREM patterns. By the age of three months both a central rhythmic background and a reactive delta occipital rhythm are seen during awake. The background focus moves from central to occipital region and the discernable posterior dominant rhythm is formed. The delta waves that dominate the occipital EEG through the first year evolve into theta frequencies by ages 2 to 4 years, reach alpha frequencies by 5 years, and at 10 years the mean frequency of 10 Hz is attained. The voltage of the overall EEG also changes. Before the first year is reached the amplitude is generally low. Amplitude gradually increases over the first 10 years then decreases with age. Understanding the normal development of the neonatal and pediatric EEG is imperative for every astute technologist.

ACKNOWLEDGEMENTS
I would like to thank Walt Banoczi, R. EEG/EP T., CNIM, CLTM, RPSGT, Orange Coast College Neurodiagnostic Program Director, for all of his guidance,

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assistance, and encouragement. He is a very thoughtful, considerate, and giving individual. I appreciate his dedication to the Neurodiagnostic Program and to all of his students past, present, and future. I would like to also thank James Hong for his contribution and assistance. Finally, I would like to thank my husband, Doug, for his patience, love, and support.

REFERENCES
American Clinical Neurophysiology Society (ACNS). Guideline 2: minimum technical standards for pediatric electroencephalography. J Clin Neurophysiol 2006; 23:9296. Blume WT, Masako K. Atlas of Pediatric Electroencephalography: Second Edition. Philadelphia: Lippincott, Williams & Wilkins; 1999; p. 19. Dreyfus-Brisac C, Curzi-Dascaolva L. The EEG during the first year of life. In: Remond A (Editor). Handbook of Electroencephalography and Clinical Neurophysiology. Volume 6B. Amsterdam: Elsevier; 1975; p. 2430. Fisch BJ. The normal EEG from premature age to the age of 19 years. In: Fisch BJ. Spehlmanns EEG Primer: Second Edition. Amsterdam: Elsevier; 1991; p. 175205, 22123, 22930. Husain AM. Review of neonatal EEG. Am J Electroneurodiagnostic Technol 2005; 45:1235. Lombroso CT. Neonatal polygraphy in full term and preterm infants: a review of normal and abnormal findings. J Clin Neurophysiol 1985; 2:10555. Mizrahi EM. Neonatal electroencephalography: clinical features of the newborn, techniques of recording and characteristics of the normal EEG. Am J EEG Technol 1986; 26:81103. Mizrahi EM, Hrachovy R, Kellaway P. Atlas of Neonatal Electroencephalography: Third Edition. Philadelphia: Lippincott, Williams & Wilkins; 2004; p. 5561. Pedley TA, Lombroso CT, Hanley JH. Introduction to neonatal electroencephalography: interpretation. Am J EEG Technol 1981; 21:1529. Quigg M. Fundamentals of neonatal polygraphy. In: Quigg M. EEG Pearls. Philadelphia: Mosby; 2006; p. 95118. Stern JM, Engel J. Atlas of EEG Patterns. Philadelphia: Lippincott, Williams & Wilkins: 2005; p. 113114, 191192, 243248. Swaiman K, Ashwel S, Ferriero D. Pediatric Neurology Principals and Practice: 4th Edition: Volume 1. Amsterdam: Elsevier; 1994; p. 140247. Sweeney D, Beckman D, Calmese F, Kriess A. The use of modified sleep deprivation to facilitate pediatric electroencephalographic recordings. Am J Electroneurodiagnostic Technol 1997; 37:21830. Tharp BR. Electrophysiological brain maturation in premature infants: a historical perspective. J Clin Neurophysiol 1990; 7:32014. Westmoreland BF, Stockard JE. The EEG in infants and children: normal patterns. Am J EEG Technol 1977; 17:187206. Werner SS, Stocking JE, Bickford R. Atlas of Neonatal Electroencephalography. New York: Raven Press; 1977. Yamada T, Meng E. Practical Guide for Clinical Neurophysiological Testing: EEG. Philadelphia: Lippincott, Williams & Wilkins; 2010.

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