Tone and Reflex Development Before Term

(1)

Reprint requests to (M.C.A.) CMSC 210, Johns Hopkins Hos-pital, 600 N Wolfe St, Baltimore, MD 21205.

Tone

and Reflex

Development

Before

Term

Marilee

C. Allen,

MD, and Arnold

J. Capute,

MD

From the Department of Pediatrics, Johns Hopkins Hospital and The Kennedy Institute for Handicapped Children, Baltimore, Maryland

ABSTRACT. The evolution of tone and reflexes from 25 weeks postmenstrual age (gestational age plus chrono-logic age) to term in a population of 42 surviving infants is described. The infants were born in 1983 at the Johns Hopkins Hospital, had birth weights <1300 g, were

ex-amined weekly until neonatal intensive care unit

cbs-charge, and did not develop cerebral palsy. Lower-ex-tremity flexor tone was first detectable at 29 weeks post-menstrual age by the popliteal angle and heel to ear maneuvers. Flexor tone, recoil, and hyperreflexia were all noted 2 to 3 weeks earlier in the lower extremities (33 to 35 weeks) than in the upper extremities (35 to 37 weeks). Hip tone (35 to 37 weeks) followed knee flexor tone, but preceded shoulder tone (37 to 38 weeks). Trunk tone on ventral suspension emerged closer to term (36 to 40 weeks), and more than half of infants evaluated at term continued to demonstrate head lag when pulled to sitting position. The emergence of the primitive and pathologic reflexes reflects (both in timing and pattern) the evolu-tion of tone: development of the reflexes in the lower extremities precedes that of those in the upper extremi-ties, and development of the distal reflexes precedes that ofthe proximal. Maturation oftone, deep tendon reflexes, pathologic reflexes, and primitive reflexes occurs in an orderly, sequential manner, with a well-defined pattern: caudocephalad (lower extremities to upper extremities) and centripetal (distal to proximal). Pediatrics 1990; 85:393-399; prematurity, muscle tone, primitive reflexes.

Although Gesell1 and Saint-Anne Dargassies2 each described the evolution of tone and reflexes

before term, their observations were limited by the

available technology, as survival of neonates born

at less than 28 to 32 weeks’ gestation was rare.

They were able to observe only more mature

pre-mature infants, a few viable premature infants born at 28 to 32 weeks’ gestation, and nonviable aborted fetuses. Improved obstetric and neonatal care has lowered the limit of viability to 23 to 24 weeks’

gestation, with the majority of survivors free of

major handicaps.3’4 These changes have allowed

observation of development before term in viable premature infants. This report details the evolution of tone, deep tendon reflexes, pathologic reflexes,

and primitive reflexes in extremely premature

in-fants who were examined weekly, from birth to

discharge from a neonatal intensive care unit, who

had no evidence of cerebral palsy when followed up.

METHODS

All 69 premature infants born at The Johns

Hopkins Hospital in 1983 whose birthweights were

<1300 g were examined sequentially from 1 week of age until discharge from the neonatal intensive care unit. A total of 13 died during the first month,

and the remaining 56 had sequential examinations.

Of these 56, 5 died during infancy (at 4 to 22

months, of severe chronic lung disease and/or

sep-sis) and in 6 cerebral palsy developed. The survivors

were observed at The John Hopkins Hospital and/

or The Kennedy Institute for Handicapped

Chil-then. Of 3 lost to follow-up, 2 had been transferred

back to community hospitals within several weeks

after birth. The study group consists of the

remain-ing 42, who were observed for 12 to 61 months

(mean 32 months) and had no evidence of cerebral

palsy. Table 1 lists the perinatal and demographic characteristics of this study group, which reflect the predominance of inner city blacks in the base neonatal intensive care unit population. Gesta-tional age of the majority (>90%) of these ex-tremely premature infants (two thirds were born at 28 weeks’ gestation) was determined from infor-mation elicited from their mothers and was

gener-ally confirmed by obstetric examination,

sono-graphic data, and the neonatologist’s estimate.

Lung disease was common: 95% were initially

in-tubated, and 24% required prolonged oxygen

(2)

976 (460-1280) 27.8 (24-32) 10 55 4 (1-8) 7 (1-9) 2.7 (0-9.3) 1.8 (0-12) 24 26 71 40 25 (14-38) 60 43 42

TABLE 1. Perinatal Characteristics of Study

Popula-tion (N = 42)

Mean birth weight, g (range) Mean gestational age, wk

(range)

Intrauterine growth retardation,

%

Vaginal delivery, % Median 1-mm Apgar score

(range)

Median 5-mm Apgar score (range)

Mean duration of mechanical ventilation, wk (range)

Mean duration of oxygen

ad-ministration, mo (range) Discharged from neonatal

in-tensive care unit while receiv-ing oxygen, %

Intraventricular hemorrhage, % Race: black, %

Sex: male, %

Mean maternal age, y (range) Medical assistance, % Parents not high school

gradu-ates, %

Parents unemployed, %

Preliminary data analysis showed that the

devel-opment of tone and reflexes in these 42 infants was

similar to that of the entire group who received

sequential examinations. Other studies have shown

that early neurologic development correlates better

with cerebral palsy than with mental retardation.5

Therefore, data for all infants who did not develop

cerebral palsy were included in the analysis in an

attempt to make the findings as generalizable as

possible.

A neonatologist/developmental pediatrician

per-formed weekly neurodevelopmental examinations on all infants, from 1 week of age until neonatal intensive care unit discharge. If the infant’s condi-tion was unstable (eg, with sepsis, pneumothorax, or necrotizing enterocolitis), examination was

de-ferred; examinations were resumed when the

in-fant’s condition was stable. A total of 390

exami-nations were performed, with a mean of 9.3 per

infant. Data were analyzed in terms of the mean postmenstrual age (gestational age plus chronologic age) at which a response was first observed and was consistently observed during subsequent examina-tions. Although the majority had their last exami-nation at term (mean postmenstrual age 38 weeks), 37% were discharged at 33 to 36 weeks

postmen-strual age. The frequency of each response was

calculated as the number of infants with the

re-sponse divided by the number of infants examined at the mean postmenstrual age of the response. Frequencies of <90% are specifically mentioned in the text.

The sequential neurodevelopmental

examina-tions consisted of assessments of posture, extremity

and axial tone, deep tendon reflexes, pathologic

reflexes, primitive reflexes, behavior, and sensory

responses.5 The appearance of early sensory

re-sponses and the grading of the primitive reflexes in

this population have been reported elsewhere.6’7

Posture in supine and prone positions was

deter-mined by noting the degree of flexion/extension of

each limb and the degree of hip adduction. For

subjective assessment of extremity flexor and hip

adductor tone, the examiner integrated posture and

active and passive tone and graded the result as

none, minimal, mild, moderate, or strong. Other

measures of extremity and axial tone were drawn

from the work of Thomas et al, Saint-Anne

Dar-gassies, Amiel-Tison, and Dubowitz et al.2’5’’2 The

degree of lower-extremity flexion on vertical

sus-pension (0 = none, 1 = semiflexion, 2 = flexion of at least 90#{176})was an additional measure of

lower-extremity flexor tone. Neck tone was assessed by

noting the degree of modulation of head movement

when the infant was rocked in the sitting positio&#{176}

and the pull to sit from supine maneuver2’8”12

(scored in the manner of Dubowitz et al8 and by

the angle of forward head movement).

The pectoralis, biceps, brachioradialis, knee

jerks, and ankle jerks were summarized (on a 0 to

5 scale, with 4 for unsustained clonus and 5 for

sustained clonus) for upper-extremity and

lower-extremity deep tendon reflexes. Pathologic reflexes

included the Babinski sign, Chaddock sign, mass

reflex, and crossed adduction (scored as absent,

equivocal, or present). The primitive reflexes were

graded in the manner of Capute et al,’3 but because

their evolution in this population has been

de-scribed elsewhere,6 only those aspects of the

prim-itive reflexes that relate to the acquisition of tone

will be described here. These include the Moro

(grades 2 and 3), the upper-extremity grasp (grades

2 and 3), the lower-extremity grasp (grade 2),

lower-extremity placing (grade 2), and the change in

posture of upper extremities vs lower extremities

with the asymmetric tonic neck reflex (grade 2).

Generally, infants were initially asleep when

sen-sory responses5 and posture were assessed. The

examination was performed in a defined order

(as-sessment of extremity and axial tone, then deep

tendon reflexes, pathologic reflexes, primitive

re-flexes), and the infant’s state of alertness was

re-corded during the examination. Most were awake

during the assessment of tone and deep tendon

reflexes; most were crying during the primitive

re-flex maneuvers. However, because the usual

con-cept of state should not be applied to premature

infants and fetuses before 36 weeks’ gestation (as

(3)

TABLE 2. Age of Attainment of Extremity Flexor Tone*

Measure of Flexor Tone Age of Attainment Age of Attainment P Value

in Upper Extremi- in Lower

Extremi-ties ties

33.9 (2.0) 31.5 (1.9) <.00001

35.8 (2.2) 34.7 (2.0) <.0005

36.8 (1.8) 36.1 (2.1) <.05

33.8 (1.6) 31.3 (1.7) <.000001

35.4 (2.1) 33.8 (2.0) <.000001

* Results are given in mean weeks (±SD) postmenstrual age.

appear to be independent of each other),14”5 no

vigorous analysis of behavioral state was attempted

in the data analysis.

Paired t tests were used to compare upper and

lower extremities for the timing of first consistent response for extremity flexor tone, recoil, deep ten-don reflexes, pathologic reflexes, asymmetric tonic neck reflex, and grasp reflex.

RESULTS

Extremity

Tone

Mean ages of first consistent response and SDs

for all the measures of flexor tone are listed in

Table 2. Mean age of acquisition of minimal flexor

tone (flexor posture but no appreciable flexor tone) was not calculated because it was noted in most

infants during the initial examination, especially in the lower extremities. Passive lower-extremity flexor tone, as measured by the popliteal angle and heel to ear maneuver, was weak but present as early as 29 weeks postmenstrual age and progressively improved with increasing postmenstrual age. Only 60% to 75% achieved a score of 4 on the popliteal angle and heel to ear maneuvers by term, and less

than 10% demonstrated a popliteal angle less than

900 (a score of 5) before neonatal intensive care

unit discharge. Appreciable flexor tone, as

meas-ured subjectively and by recoil, appeared at 31

weeks in the lower extremities and at 34 weeks in the upper extremities and increased with postmen-strual age. For each degree of flexor tone, tone in the lower extremities preceded tone in the upper

extremities by 2 to 3 weeks (P < .05 to P < .000001).

Lower-extremity flexor tone against gravity, as

measured on vertical suspension, appeared closer to term (at 37 weeks postmenstrual age), with less than half of the infants demonstrating 90#{176}of

lower-extremity flexion by neonatal intensive care unit discharge.

Hip Tone

Mild hip adductor tone could be appreciated at a

mean postmenstrual age of 33 weeks and was

mod-erate at 35 weeks (Table 3). Hip adductor tone

began to be strong enough to overcome gravity in

supine and prone positions at 31 weeks with a loss of frog-legged posture by 37 weeks postmenstrual age.

Shoulder

Tone

All of these extremely premature infants initially

had shoulder hypotonia, as manifested by anterior

and posterior scarf sign and slip through at the

shoulders (Table 3). They began to lose the poste-rior scarf sign first (it became equivocal at 32 weeks postmenstrual age), then the anterior scarf sign (equivocal, or scored as 1 on the Dubowitz maneu-ver, at 35 weeks postmenstrual age). Although the majority (>90%) lost both the anterior and poste-rior scarf sign at term (37 to 38 weeks postmen-strual age), only 69% lost slip through at the shoul-ders, at a mean postmenstrual age of 38 weeks.

Subjective assessment Mild

Moderate Strong Recoil score8

1 (90#{176}-180#{176}) 2 (<90#{176}) Popliteal angle score8

1 (160#{176}) 2 (130#{176}) 3 (110#{176}) 4 (90#{176}) Heel to ear score8

1 2 3 4

Vertical suspension Semiflexion

Flexion ± 90#{176}

(4)

TABLE 3. Age of Attainment of Tone*

Shoulder and Hip

Measure of Shoulder and Hip Tone

Age of At-tainment Shoulder tone

Anterior scarf sign8

2 (equivocal) 35.3 (2.2)

3 (absent) 38.3 (2.1)

Posterior scarf sign

Equivocal 31.7 (2.2)

Absent 37.5 (2.5)

Slip through

Equivocal 37.7 (2.1)

Absent 38.2 (1.9)

Hip adductor tone Subjective assessment

Mild 33.1 (2.5)

Moderate 35.4 (2.3)

Posture

Mild (mildly frog-legged) 31.3 (3.3)

Moderate (not frog-legged) 36.7 (2.1)

Trunk Tone

TABLE 4. Age of Attainment of Axial Tone*

Measure of Axial Tone Age of

At-tainment Neck tone

Pull to sit score

1 33.4 (2.7)

2 37.0 (2.7)

Angle of forward movement (on pull to sit)

100#{176} 31.1 (2.4)

90#{176} 34.2 (2.5)

80#{176} 36.6 (2.9)

70#{176} 37.3 (2.5)

Rock in sitting position score’#{176}

2 (some modulation) 35.5 (2.6)

3 (good modulation) 38.3 (2.4)

Trunk tone

Ventral suspension score8

1 32.4 (1.9)

2 36.5 (2.1)

3 39.7 (2.4)

(a score of 3) until term (38 weeks postmenstrual age).

Mild trunk tone on ventral suspension appeared

at 32 weeks postmenstrual age and progressively

improved with age (Table 4). These premature

in-fants were able to attain almost a horizontal posi-tion on ventral suspension (score of 2) at 36.5 weeks postmenstrual age. All of the infants observed until term were able to attain a completely horizontal position on ventral suspension (a score of 3), at a mean postmenstrual age of 40 weeks.

Neck Tone

Some neck flexion, as measured by a score of 1

on the pull to sit maneuver,8 appeared as early as

33 weeks postmenstrual age (Table 4). Eleven

in-fants were able to keep their heads in line with their bodies (a score of 2) at a mean age of 37 weeks postmenstrual age, but the majority (54%) of those observed until term did not achieve that skill before neonatal intensive care unit discharge. The angle of forward neck flexion on the pull to sit maneuver was 90#{176} (indicating that the head came forward only with gravity) before 34 to 36 weeks

postmen-strual age. The majority were able to bring their

heads forward against gravity (<90#{176})by term, at a

mean postmenstrual age of 37 weeks. These

pre-mature infants had enough neck control to begin to

modulate head movement when rocked in the

sit-ting position1#{176} (a score of 2) by 35 to 36 weeks postmenstrual age, but it was generally not mature

Deep Tendon

Reflexes

Consistently elicited deep tendon reflexes (2+)

and hyperreflexia (3+) emerged 3 weeks earlier in

the lower extremities than in the upper extremities (P < .05 to P < .000001; Table 5). Unstained clonus (4+ deep tendon reflexes) at the knees and/or an-kles could be elicited in all of the infants observed

until term, at a mean postmenstrual age of 34

weeks.

Pathologic

Reflexes

The vast majority of infants (95%) demonstrated

the Babinski sign, Chaddock sign, mass reflex, and crossed adduction before neonatal intensive care unit discharge (Table 6). The Babinski and

Chad-dock signs could be elicited much earlier than the

mass reflex and crossed adduction (29 weeks vs 33

to 34 weeks; P < .000001).

Primitive Reflexes

Position changes with the asymmetric tonic neck

reflex (grade 2 asymmetric tonic neck reflex) could

be elicited at a mean postmenstrual age of 34 weeks in the upper extremities and 31 weeks in the lower extremities (P < .000001; Table 6). Strong finger and toe flexion with the grasp reflex was frequently elicited during the initial examination and could be consistently elicited on all infants, at a mean

(5)

TABLE 5. Age of Attainment of Deep Tendon Re-flexes*

Measure of Deep Age of Attain- Age of Attain- P Value Tendon Reflexes ment in

Up-per Extremi-ties

ment in Lower

Ex-tremities

2+ 33.2 (2.0) 29.9 (1.8) <.000001

3+ 36.2 (2.7) 32.9 (1.7) <.05

4+ ... 34.3 (2.5)

* Results are given in mean weeks (±SD) postmenstrual

age.

TABLE 6. Age of Attainment of Pathologic and

Prim-itive Reflexes*

Measure of Pathologic and Primitive Re-flexes

Age of At-tainment Pathologic reflexes

Babinski sign 29.5 (2.0)

Chaddock sign 29.2 (2.0)

Mass reflex 33.4 (2.6)

Crossed adduction 34.3 (2.0)

Primitive reflexes Upper extremity

Asymmetric tonic neck reflex7’13: 34.3 (2.7) grade 2

Grasp7

Grade 2 30.5 (2.4)

Grade 3 35.7 (2.7)

Moro7

Grade 2 30.4 (2.3)

Grade 3 34.7 (2.5)

Lower extremity

Asymmetric tonic neck reflex7”3: 30.7 (2.4) grade 2

Grasp7: grade 2 30.0 (2.8)

Placing7: grade 2 32.9 (2.0)

mean postmenstrual age of 36 weeks, upward

trac-tion elicited elbow flexion (grade 3 upper-extremity

grasp reflex). Weak upper-extremity flexion and

adduction (grade 2 Moro) occurred as early as 30

weeks postmenstrual age, but strong, complete

flex-ion and adduction (grade 3 Moro) occurred at 35

weeks postmenstrual age. Stimulation of the

dor-sum of the foot elicited strong, prompt lower-ex-tremity flexion followed by some lower-extremity extension (grade 2 lower-extremity placing reflex)

at a mean postmenstrual age of 33 weeks.

DISCUSSION

Development is a dynamic process that implies

order, complexity, sequential and interweaving

pat-terns, and a timetable. The evolution of extremity

flexor and axial tone, deep tendon reflexes,

patho-logic reflexes, and primitive reflexes before term certainly proceeds in an orderly, sequential manner, with a defined timetable in accordance with

post-menstrual age. The reflection of extremity flexor

tone in the completion of various primitive reflexes

demonstrates the complexity and interweaving of

the various aspects of development. Two patterns

of normal development before term can be

dis-cerned: tone and reflexes all emerge in a caudoce-phalad (lower extremities to upper extremities) and in a centripetal (distal to proximal) manner.

Saint-Anne Dargassies2”6 has emphasized the

importance of viewing the premature infant’s

de-velopment in terms of postmenstrual age. This

study confirms the importance of postmenstrual

age by detailing the orderly, sequential acquisition of extremity and axial tone, deep tendon reflexes,

pathologic reflexes, and primitive reflexes with

re-spect to a postmenstrual age timetable. For the

mean postmenstrual age of acquisition of individual test items, the SDs of 2 weeks suggest significant individual variability. As Illingworth’7 has empha-sized, normal development is characterized by its sequence, with considerable normal individual var-iability with respect to rate. At term, the extremely

premature infants had tone and reflexes that were

remarkably similar to those of full-term newborns.

In contrast with the flaccid extended posture

attributed to infants born before 30 weeks’ gesta-tion,”2”2 virtually all the extremely premature

in-fants examined in this study were semiflexed during their initial examination, 1 week after birth, well past the influence of in utero position. The only

extended posture observed was associated with a

spontaneously assumed asymmetric tonic neck pos-ture (extension of the limbs on the face side). The

infant’s spontaneously assumed posture often

changed during the course of the examination and

was related to the infant’s state of alertness. No

summary measure adequately defined posture, but

the dynamic quality of the infant’s posture was

integrated with active and passive flexor tone for the examiner’s subjective assessment of degree of extremity flexor tone.

The timing of the emergence of some measures

of upper-extremity and lower-extremity flexor tone slightly preceded that described by Saint-Anne Dargassies2 and Amiel-Tison.’#{176}” The earliest sign

of emerging flexor tone (a score of 1 on the

pop-liteal angle and heel to ear maneuvers) and both mild and moderate upper-extremity and lower-ex-tremity recoil all occurred 1 to 2 weeks earlier in this population than observedby Saint-Anne Dar-gassies2 and Amiel-Tison.’2 This earlier emergence of flexor tone and the consistent finding of a

sem-iflexed resting posture may be due to the relative

good health and/or the large proportion of black

(6)

The timing of the development of axial tone is more consistent with the general descriptions of the

emergence of shoulder, trunk, and neck tone

re-ported in the literature.2”0”2 Hip adductor tone,

however, emerged somewhat earlier than previously reported. These infants were not as frog-legged at

34 to 35 weeks as the infants described by

Saint-Anne Dargassies2 and Amiel-Tison,’#{176} although SDs (2.1 to 3.3 weeks) indicate much individual

varia-bility. Data on many of the specific measures of

tone used in this study and the range of individual

variability observed have not been previously

re-ported (especially with respect to later neuromotor

outcome). Nor has the development of

hyperre-flexia and the emergence of the pathologic reflexes

been previously reported, although it is widely

ap-preciated that they are common findings in the

newborn.

Saint-Anne Dargassies2”6 has repeatedly empha-sized the caudocephalad development of flexor tone,

which is an unusual pattern in embryology. This

study demonstrates that not only flexor tone, but

also axial tone, deep tendon reflexes, pathologic reflexes, and primitive reflexes all emerge in a

cau-docephalad pattern. As with the tone items, deep

tendon reflexes and pathologic reflexes have not

previously been studied before term. The emergence of the primitive reflexes in a caudocephalad direc-tion contradicts the findings of Saint-Anne

Dar-gassies,2”6 who based her conclusions on the

ce-phalocaudal progression of the primary (ie, primi-tive) reflexes on the traction response

(upper-extremity grasp), Moro, root, and crossed extension

reflex. The crossed extension reflex was not studied

here, but it involves a complex sequence of flexion,

adduction, and extension that is often difficult to

discern. The root does emerge early (at 32 weeks postmenstrual age in this study), and it may reflect

the importance of early oromotor development for

survival. Nevertheless, in this study, the traction

response of the upper-extremity grasp and Moro

clearly emerged as upper-extremity flexor tone was emerging and the flexion component of the lower-extremity placing emerged earlier, in conjunction with lower-extremity flexor tone. Analysis of the

emergence of consistent posture changes with the

asymmetric tonic neck reflex clearly demonstrated a caudocephalad pattern.

The centripetal development of tone and reflexes

has not been emphasized previously, although it

has clearly been recognized that extremity tone

emerges before axial tone.2”#{176}”2Finger and toe flex-ion with the grasp were generally present more than

5 weeks before elbow flexion with upward traction.

Hip and shoulder tone emerged just before trunk

and nuchal tone. The more distal pathologic

re-flexes (Babinski, Chaddock) were generally

detect-able 4 weeks before the proximal ones (mass reflex, crossed adduction).

This study reveals the complex interweaving of

the development of muscle tone, deep tendon

re-flexes, pathologic reflexes, and primitive reflexes.

This interweaving of seemingly independent

sys-tems suggests the existence of an underlying order.

The neuroanatomic, neurophysiologic, and

neuro-chemical aspects of these interrelationships should be explored to better define that order.

IMPLICATIONS

Knowledge of the signs of normal development

in infants before term allows one to detect abnor-mality, and knowledge of the extent of individual variability in normal infants and of the factors that

affect this variability allows one to define more

precisely abnormal delay. In addition, deviant

pat-terns can be detected. The significance of a single finding cannot be assessed without first evaluating

its relationship to the other aspects of development.

Sequential examinations, which allow one to

differ-entiate between an abnormal timetable and an

ab-normal pattern of development, add another dimen-sion to the evaluation.

REFERENCES

1. Gesell A. The Embryology of Behavior. New York, NY: Harper and Brothers; 1945:289

2. Saint-Anne Dargassies S. Neurological Development in the Full-Term and Premature Neonate. New York, NY: Ex-cerpta Medica; 1977:323

3. Bennett FC, Robinson NM, Sells CJ. Growth and develop-ment of infants weighing less than 800 grams at birth.

Pediatrics. 1983;71:319-323

4. Hirata T, Epcar JT, Walsh, A, et al. Survival and outcome

of infants 501 to 750 gm: a six year experience. J Pediatr.

1983;102:741-748

5. Allen MC, Capute AJ. The neonatal neurodevelopmental examination as a predictor of neurologic handicap in

pre-mature infants. Pediatrics. 1989;83:498-506

6. Allen MC, Capute AJ. Assessment of early auditory and visual abilities of extremely premature infants. Dev Med Child Neurol. 1986;28:458-466

7.Allen MC, Capute AJ. Evolution of primitive reflexes in extremely premature infants. Pediatr Res. 1986;20:1284-1289

8. Dubowitz LMS, Dubowitz V, Goldberg C. Clinical assess-ment of gestational age in the newborn infant. J Pediatr.

1970;77:1-10

9. Thomas A, Chesni Y, Saint-Anne Dargassies S. The Neu-rological Examination of the Infant. Little Club Clinics in

Developmental Medicine No 1.London, England: National

Spastics Society: 1960:31

10. Amiel-Tison C. Neurological evaluation of the small

neo-nate: the importance of head straightening reactions. In:

Gluck L, ed. Modern Perinatal Medicine. Chicago, IL: Year

(7)

11. Amiel-Tison C. Neurological evaluation of the maturity of

newborn infants. Arch Dis Child. 1965;43:89-93

12. Amiel-Tison C. Neurological Assessment During the First Year of Life. New York, NY: Oxford University Press; 1986 13. Capute AJ, Palmer FB, Shapiro BK, et al. Primitive reflex

profile: a quantification ofprimitive reflexes in infancy. Dev Med Child Neurol. 1984;26:375-383

14. Prechtl, HFR, Fargel JW, Weinmann HM, et al. Postures,

motility and respiration of low-risk preterm infants. Dev Med Child Neurol. 1979;21:3-7

15. Nijhuis JG, Martin CB Jr, Prechtl HFR. Behavioral states

of the human fetus. In: Prechtl HFR, ed. Continuity of

Neural Functions. Philadelphia, PA: JB Lippincott Co;

1984:65-78

16. Saint-Anne Dargassies S. The Development of the Nervous System in the Fetus. Switzerland: Documents Scientifiques

Guigoz; 1968

17. Illingworth RS. The Development of the Infant and Young Child, Normal and AbnormaL Baltimore, MD: Williams &

(8)

1990;85;393

Pediatrics

Marilee C. Allen and Arnold J. Capute