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Altered brain development following global neglect :::: Welcome to Child Trauma Academy ::::::::::: Altered brain development following global neglect in early childhood Bruce D. Perry, M.D., Ph.D. Ronnie Pollard, M.D. The ChildTrauma Academy www.ChildTrauma.org *This is an Academy version of a paper presented at Society for Neuroscience Annual Meeting, New Orleans, 1997 Official citation: Perry, BD and Pollard, D. Altered brain development following global neglect in early childhood. Society For Neuroscience: Proceedings from Annual Meeting,New Orleans, 1997 Introduction Each year in the United States alone, over 500,000 children suffer from some version of "neglect." Neglected children brought to the attention of the Child Protective Services has a much higher probability of emotional, behavioral, cognitive, social and physical delays and dysfunction than "comparison" children. It is becoming increasingly clear that the nature, timing and extent of neglect in childhood are critical in determining the nature and extent of these deficits (Perry et al., 199 5; Courchesne et al., 1994). This observation may seem somewhat obvious to individuals familiar with the principles of neurodevelopment and the animal studies documenting the critical role of sensory stimulation in organizing the developing central nervous system. Indeed, use (or activity) dependent development and modification of neural systems is one of the core principles of neurodevelopment (see Singer, 1995). In animals raised in sensory depriving situations, a host of abnormalities in neurochemical and neuroarchitectural organization have been documented (e.g., Darwin, 1868; Ebinger, 1974; Cragg, 1975). The functional consequences of sensory deprivation during neurodevelopment can be significant. Indeed , in some severe deprivation situations, sensory deprivation or sensory disorganization during critical or sensitive periods can result in permanent dysfunction (e.g., Spitz & Wolf, 1946; Perry, 1997). This has ominous implications for human development. While many studies have described various functional consequences following neglect in childhood, few have examined aspects of neurodevelopment in neglected children. The present study reports a preliminary examination of measures of brain growth in a large group of neglected children. Method Children (ages 0 to 17) were referred to our specialty clinic for evaluation by Child Protective Service or other agencies working with children following http://www.childtrauma.org/CTAMATERIALS/neuros~1.asp (1 of 7)11/13/2006 3:59:16 PM

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Altered brain development following global neglect in early childhood

Bruce D. Perry, M.D., Ph.D. Ronnie Pollard, M.D.

The ChildTrauma Academy www.ChildTrauma.org

*This is an Academy version of a paper presented at Society for Neuroscience Annual Meeting, New Orleans, 1997

Official citation: Perry, BD and Pollard, D. Altered brain development following global neglect in early childhood. Society For Neuroscience: Proceedings from Annual Meeting,New Orleans, 1997

Introduction

Each year in the United States alone, over 500,000 children suffer from some version of "neglect." Neglected children brought to the attention of the Child Protective Services has a much higher probability of emotional, behavioral, cognitive, social and physical delays and dysfunction than "comparison" children. It is becoming increasingly clear that the nature, timing and extent of neglect in childhood are critical in determining the nature and extent of these deficits (Perry et al., 199 5; Courchesne et al., 1994).

This observation may seem somewhat obvious to individuals familiar with the principles of neurodevelopment and the animal studies documenting the critical role of sensory stimulation in organizing the developing central nervous system. Indeed, use (or activity) dependent development and modification of neural systems is one of the core principles of neurodevelopment (see Singer, 1995). In animals raised in sensory depriving situations, a host of abnormalities in neurochemical and neuroarchitectural organization have been documented (e.g., Darwin, 1868; Ebinger, 1974; Cragg, 1975). The functional consequences of sensory deprivation during neurodevelopment can be significant. Indeed , in some severe deprivation situations, sensory deprivation or sensory disorganization during critical or sensitive periods can result in permanent dysfunction (e.g., Spitz & Wolf, 1946; Perry, 1997). This has ominous implications for human development.

While many studies have described various functional consequences following neglect in childhood, few have examined aspects of neurodevelopment in neglected children. The present study reports a preliminary examination of measures of brain growth in a large group of neglected children.

Method

Children (ages 0 to 17) were referred to our specialty clinic for evaluation by Child Protective Service or other agencies working with children following http://www.childtrauma.org/CTAMATERIALS/neuros~1.asp (1 of 7)11/13/2006 3:59:16 PM

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abuse or neglect. Comprehensive physical, developmental and neuropsychiatric evaluations were conducted to assist in placement and treatment planning. As part of this evaluation, comprehensive pre- and perinatal history were obtained, as were various measures of growth (height, weight and frontal-occipital circumference: FOC).

Charts were reviewed for evidence of pre-natal drug exposure (PND) and neglect. Neglect was considered global neglect when a history of relative sensory deprivation in more than one domain was obtained (e.g., minimal exposure to language, touch and social interactions). Chaotic neglect is far more common and was considered present if history was obtained that was consistent with physical, emotional, social or cognitive neglect. When possible history was obtained from multiple sources (e.g., investigating CPS workers, family, police).

Based upon these reviews, the neglected children (n= 122) were divided into four groups: Global Neglect (GN; n=40); Global Neglect with Prenatal Drug Ex posure (GN+PND; n=18); Chaotic Neglect (CN; n=36); Chaotic Neglect with Prenatal Drug Exposure (CN+PND; n=28). Measures of growth were compared across group and compared to standard norms developed and used in all major pediatric settings.

In cases where neuroimaging studies had been conducted as part of a medical or neurological evaluation, these images were examined in a retrospective fashion. Neuroradiologists had read the scans in context of the original medical or neurological referral and, typically, were unaware of the neglect or psychosocial situation of the child.

Results

Growth

Dramatic differences from the norm were observed in FOC (suggesting de creased brain growth) for the globally neglected children (see Figures). This group 6;s mean FOC was only in the 10th percentile, while height and weight measures of growth demonstrated less difference (30-40th percentile). In contrast , the chaotically-neglected children did not demonstrate this marked group difference in FOC.

Pre-natal drug exposure appeared to have an interactive, but complex effect on growth. In the global neglect population, it appeared to exacerbate the observed growth differences. In the chaotic neglect group, however, no differences in growth were observed.

Neuroimaging

Neuroradiologists interpreted 3 of 26 scans abnormal from the children with chaotic neglect (11.5 %) and in 11 of 17 of the children with global neglect (64. 7 %). The majority of the readings were "enlarged ventricles" or "cortical atrophy." Few focal abnormalities were noted.

Normal vs. Abnormal CT or MRI Scans in Neglected Children

Normal Abnormal

Chaotic Neglect 18 1

Chaotic Neglect + PND 5 2

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Global Neglect 3 8

Global Neglect + PND 3 3

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Discussion These findings strongly suggest that when early life neglect is characterized by decreased sensory input (e.g., relative poverty of words, touch and socia l interactions) it will have a similar effect on humans as it does in other mammalian species. Sensory deprivation has been demonstrated to alter the physical growth and organization of the brain in animals.

The present studies suggest that the same is true for children globally neglected in the first three years of life. It is important to emphasize the timing of the neglect. The brain is undergoing explosive growth in the first years of life, and, thereby, is relatively more vulnerable to lack of organizing experiences during these periods. These unfortunate globally neglected children (some literally were raised in cages in dark rooms for the first years of their lives) appear to have altered brain growth.

There are likely many factors contributing to this observation. Nutrition is one key aspect. Based upon the relative impact on the brain as opposed to other growth, a total nutritional explanation is inadequate. It is likely that the actual lack of experiences (sound, smell, touch) associated with global neglect in these children plays a major role.

While the actual size of the brain in chaotically neglected children did not appear to be different from norms, it is reasonable to hypothesize that organizational abnormalities exist.

Volumetric studies of key areas are indicated, as are MRI studies to examine the functional impact of neglect; global or chaotic.

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All rights for reproduction of the above image are reserved, Bruce Perry, M.D., Ph.D. Baylor College of Medicine.

These images illustrate the negative impact of neglect on the developing brain. In the CT scan on the left is an image from a healthy three year old with an average head size. The image on the right is from a three year old child suffering from severe sensory-deprivation neglect. This child’s brain is significantly smaller than average and has abnormal development of cortex.

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References

Courchesne, E., Chisum, H., & Townsend, J. (1994). Neural activity -dependent brain changes in development: Implications for psychopathology. Development and Psychopathology, 6, 697-722.

Cragg, B. G. (1975). The development of synapses in kitten visual cortex during visual deprivation. Experimental Neurology, 46, 445-451.

Darwin, C. (1868). The variations of animals and plants under domestication. London:

Ebinger, P. (1974). A cytoachitectonic volumetric comparison of brains in wild and domestic sheep. Z Anat Entwicklungsgesch, 144, 267-302.

Perry BD, Pollard RA, Blakley TL, Baker WL, Vigilante D: (1995) Childhood trauma, the neurobiology of adaptation and use-dependent development of the brain: How states become traits. Infant Mental Health Journal 16:271-291

Perry, BD (1997) Incubated in Terror: Neurodevelopmental Factors in th e ‘Cycle of Violence’ In: Children in a Violent Society (J Osofsky , Ed.). Guilford Press, New York, pp 124-148, 1997

Singer, W. (1995). Development and plasticity of cortical processing architectures. Science, 270, 758-764.

Spitz, R. A., & Wolf, K. M. (1946). Anaclitic depression: an inquiry into the genesis of psychiatric conditions in early childhood. II. Psychoanalyt ic Study of the Child, (2), 313-342.

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Infant Growth and DevelopmentChris Plauche Johnson, MEd, MD* and Peter A. Blasco, MD†

Introduction“Infant” is derived from the Latinword, “infans,” meaning “unable tospeak.” Thus, many define infancyas the period from birth to approxi-mately 2 years of age, when lan-guage begins to flourish. It is anexciting period of “firsts”—firstsmile, first successful grasp, firstevidence of separation anxiety, firstword, first step, first sentence. Theinfant is a dynamic, ever-changingbeing who undergoes an orderly andpredictable sequence of neurodevel-opmental and physical growth. Thissequence is influenced continuouslyby intrinsic and extrinsic forces thatproduce individual variation andmake each infant’s developmental

path unique. Intrinsic influencesinclude the child’s physical charac-teristics, state of wellness or illness,temperament, and other geneticallydetermined attributes. Extrinsicinfluences during infancy originateprimarily from the family: the per-sonalities and style of caregiving byparents and siblings, the family’seconomic status with its impact onresources of time and money, andthe cultural milieu into which theinfant is born.

Neurodevelopmental sequencescan be viewed broadly in terms ofthe traditional developmental mile-stones. Developmental milestonesprovide a systematic approach bywhich to observe the progress of the infant over time. Attainment of a particular skill builds on theachievement of earlier skills; onlyrarely are skills skipped. When thishappens, the advanced skill mayrepresent a “splinter” skill, that is, a deviant developmental pattern.

For example, five-word sentences ina 2-year-old child who does not fol-low simple commands may repre-sent echolalia typical of autism. The sentences are not meaningfuland have no communicative intent.Delays in one developmentaldomain may impair development in another domain. For example,immobility due to neuromusculardisorders prevents exploration of theenvironment and, in turn, impedescognitive development arisingthrough manipulation of objects.Last, a deficit in one domain maycompromise the assessment of skilllevels in another domain, eventhough development in the seconddomain is normal. For example, it is difficult to assess problem-solving skills in a child who hascerebral palsy because the child may understand the concept ofmatching geometric forms, yet beunable to insert them physically into a formboard.

Developmental milestones serveas the basis of most standardizedassessment and screening tools.Although these screening tools pro-vide the clinician with a structuredmethod of observing the infant’sprogress and help define a develop-mental delay, many lack sensitivity.Parental concern in the face of normal results in developmentalscreening should not be disregarded.Focusing narrowly on discrete milestones may fail to reveal atypical organizational processesthat are involved in the child’sdevelopmental progress. Thus, it is important to analyze all mile-stones within the context of thechild’s history, growth, and physicalexamination as part of an ongoingsurveillance program. Only then is it possible to formulate an overallimpression of the child’s true devel-opmental status and the need forintervention.

Although milestones form thefoundation of the discussion, the primary intent of this article is toprovide broader insights into infantdevelopmental processes and to helpthe clinician recognize warningbehaviors (“red flags”) indicative

ARTICLE

224 Pediatrics in Review Vol. 18 No. 7 July 1997

IMPORTANT POINTS

1. Infant development occurs in an orderly and predictable manner thatis determined intrinsically. It proceeds from cephalic to caudal andproximal to distal as well as from generalized reactions to stimuli tospecific, goal-directed reactions that become increasingly precise.Extrinsic forces can modulate the velocity and quality of develop-mental progress.

2. Each developmental domain must be assessed during ongoing developmental surveillance within the context of health supervision.Generalizations about development cannot be based on the assessmentof skills in a single developmental domain (ie, one cannot describeinfant cognition based on gross motor milestones). However, skills inone developmental domain do influence the acquisition and assessmentof skills in other domains.

3. Speech delays are the most common developmental concern seen bythe general pediatrician, yet they often are not well understood ordiagnosed expediently. A sound understanding of the distinctionbetween an isolated speech delay (usually environmental and often can be alleviated) and a true language delay (a combined expressiveand receptive problem that implies more significant pathology) willhelp the clinician refer appropriately for precise diagnosis and appropriate management.

4. It is essential to understand normal development and acceptable variations in normal developmental patterns to recognize early patterns that are pathologic and that may indicate a possible developmental disability.

5. Assessment of the quality of skills and monitoring the attainment of developmental milestones are essential to early diagnosis of developmental disabilities and expedient referral to early interventionprograms.

* Associate Professor of Pediatrics, The University of Texas Health Sciences Center,San Antonio, TX.† Associate Professor of Pediatrics, Johns Hopkins University, Baltimore, MD.

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of developmental deficits. The mile-stone ages are not repeated in thetext to allow a more fluid discussionof developmental themes withineach domain. Milestones have beenorganized into domains to assist theclinician in recognizing their inde-pendence as well as their interrela-tionships. Tables illustrating alldomains at each age can be found inVaughan (see Suggested Reading).Problem-solving and language mile-stones facilitate early identificationof cognitive deficits. Adaptive skills(ie, skills related to independence in feeding, dressing, toileting) tradi-tionally have been included withinthe fine motor domain. However,because these milestones are influ-enced by the social environment, we have included them in a “psycho-social domain.” Lists for emotionaland socialization milestones also areincluded in this domain. In contrastto motor and cognitive milestones,psychosocial behaviors are influ-enced more by extrinsic factors,making them less well-defined.

Evolution of Developmental TheoryDevelopmental theory has beenshaped by the persistent debate ofwhether nature (intrinsic forces) ornurture (extrinsic forces) is the pre-dominant influence. At the turn ofthe century, developmental theoriespromoted nature as the major influ-ence. Gesell (early 1900s) was oneof the first to study infant develop-ment systematically and establishdevelopmental norms. Developmentwas seen as a function of neurologicmaturation and growth. Becauseadvancing age and genetic endow-ment were the chief mechanisms for change, babies were believed todevelop at a predetermined biologi-cal pace, with parents needing todo little more than provide a goodnurturing environment.

By mid-century, theories thatstressed the importance of nurturebegan to prevail. Pavlov (1930s),Watson (1950s), and Skinner (1960s)promoted the opposing view thatdevelopment was a function oflearning. Operant conditioning (positive and negative reinforce-ments through social interactions orenvironmental changes) promoted

learning and shaped the child’sdevelopment. This line of thinkingformed the philosophical basis forthe Head Start program of the1960s. Freud (1920s) and Erikson(1950s) promoted developmentalprogress as a function of the resolu-tion of conflict. The quality of theinfant’s relationships with key indi-viduals was considered central tofuture development.

During the second half of thecentury, the name of Piaget becamealmost synonymous with childdevelopment. Piaget was the first todescribe the infant as having intelli-gence. For centuries, it had beenassumed that the infant’s mind was a “blank tablet waiting to be writtenon.” Because infants could not tellus what they were experiencing, itwas believed that they saw and

heard little and thought even less,with consciousness as adults knew it not existing. Piaget revealed thatinfants were, indeed, capable ofthinking, analyzing, and assimilat-ing. He viewed development asstage-like cognitive changes. Thechild actively explores objects in aneffort to understand his or her envi-ronment. Depending on the develop-mental stage, a child organizes thisinformation to form new theoriesabout the way the world works.

It was not until the last part ofthis century that emotional andsocial development began to receivethe same degree of attention as thatgiven to the motor and cognitivedomains. Research has revolvedaround theories regarding infantexpression of emotion (Mandler,1970s), attachment (Bowlby, 1960s;Mahler, 1970s; and Ainsworth,1980s), and temperament (Thomasand Chess, 1970s). Once it was rec-ognized that newborns could demon-strate distress (pain and hunger),interest, and disgust, these facialexpressions have been used to studyinformation processing in infancyprior to the age when thoughts canbe verbalized. As the 20th centurycomes to a close, remarkable

advances in behavioral genetics,together with recent discoveriesregarding innate infant abilities,have swung the pendulum back in favor of nature as the primaryinfluence on the developmentalprocess.

Developmental Snapshots:The First Two Years of LifeBefore dissecting infant develop-ment into discrete steps within each developmental domain, it isvaluable to view the infant at discrete intervals. These 6-month“snapshots” are displayed graphi-cally in Figure 1. This gestaltapproach may help the clinicianmake sense of the interrelatedness of the precise changes within eachdevelopmental domain.

These four snapshots illustrateseveral generalizations about neuro-developmental maturationover time:

1. Responses to stimuli proceedfrom generalized reflexes involv-ing the entire body, as seen in thenewborn (and fetus), to discretevoluntary actions that are undercortical direction. This specializa-tion allows the child to movefrom obligatory symmetric reac-tions when attending to a stimu-lus (ie, vocalizations, arm wav-ing, and kicking) to voluntary,asymmetric, and precise move-ments toward a stimulus (ie,grasping with one hand andinspecting with the other).

2. Development proceeds fromcephalic to caudal and proximalto distal. Thus, arm movementcomes under cortical directionand visual guidance before legmovement. With this, the childprogresses from hand-mouth tofoot-mouth play. The upperextremities become increasinglyaccurate in reaching, grasping,transferring, and manipulating.Distal development is seen whenthe infant can isolate and use the

Pediatrics in Review Vol. 18 No. 7 July 1997 225

CHILD DEVELOPMENTInfancy

One principle of development in infancy is that it proceedsfrom head-to-toe — thus, arm movement comes before leg movement.

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index finger to poke and exploreobject parts. When this occurs inconcert with thumb opposition, the fine pincer grasp is mastered.Precise release of tiny objects follows, so that fundamentalmanipulative skills reach adultlevels by the end of infancy.

3. Developmental progression isfrom dependence to indepen-dence. The totally dependentnewborn progresses to a toddlerwho has mobility and manipula-tive skills that enable him or herto explore most of the environ-ment. Toddlers can move about

the house independently, openingdoors, maneuvering stairs, and fetching desired objects. Theycan feed and undress themselvesand even may be toilet trained.This new autonomy becomes the foundation for the challeng-ing “twos.”

226 Pediatrics in Review Vol. 18 No. 7 July 1997

CHILD DEVELOPMENTInfancy

FIGURE 1. Developmental “snapshots” at 6, 12, 18, and 24 months.

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Physical GrowthGrowth milestones are the mostpredicable, although they must beviewed within the context of eachchild’s specific genetic and ethnicinfluences. It is essential to plot thechild’s growth on gender- and age-appropriate charts. Charts now areavailable for some ethnic groups aswell as for a few genetic syndromes(eg, Down and Turner syndromes).Fetal weight gain is greatest duringthe third trimester. During the firstfew months of life, this rapid growthcontinues, after which the growthrate decelerates (Table 1). Birth-weight is regained by 2 weeks of ageand doubles by 5 months. Heightdoes not double until between 3 and4 years of age. Head growth duringthe first 5 or 6 months is due to continued neuronal cell division.Later, increasing head size is due to neuronal cell growth and support-ing tissue proliferation.

RED FLAGS IN PHYSICAL GROWTHOccipitofrontal Circumference

Large and small head size both arerelative red flags for developmentalproblems. Microcephaly is associ-ated with an increased incidence ofmental retardation, but there is nostraightforward relationship betweensmall head size and depressed intel-ligence. As a reflection of normalvariation, microcephaly is not asso-ciated with structural pathology ofthe nervous system or with lowintelligence. Furthermore, micro-

cephaly can be seen with above-average cognitive capability. Micro-cephaly associated with genetic oracquired disorders reflects cerebralpathology and almost always has cognitive implications.

Macrocephaly may be due tohydrocephalus, which is associatedwith an increased incidence of cog-nitive deficits, especially learningdisabilities. Macrocephaly withouthydrocephalus, far from being a predictor of advanced intelligence,also is associated with a higherprevalence of cognitive deficits. It may be due to metabolic oranatomic abnormalities. In about50% of cases, macrocephaly isfamilial, and the implications arebenign in terms of intellect. Whenevaluating infants whose macro-cephaly is isolated, the finding of a large head size in one or both parents can be reassuring.

Height and Weight

Although the majority of individualswho are of below- or above-averagesize are otherwise normal, there isan increased prevalence of develop-mental disabilities in these two subpopulations. Many genetic syn-dromes are associated with shortstature; large stature syndromes areless common. Again, when consider-ing deviation from the norm in thespecific child, family characteristicsmust be reviewed. The concept ofmid-parental height is useful indetermining whether a given child’ssize is appropriate for his or herfamilial growth pattern.

Dysmorphism

Although most isolated minor dys-morphic features are inconsequen-tial, the presence of three or moremay indicate the presence of devel-opmental dysfunction. Almost 75%of these minor superficial dysmor-phisms can be found by examiningthe face, skin, and hands. The presence of both minor and majorabnormalities may indicate a moreserious genetic syndrome. In manyinstances, dysmorphic features willlead to the diagnosis of a clinicalsyndrome during the neonatal periodand predate the recognition of anyneurodevelopmental deficits.

Motor DevelopmentTo make a meaningful statementabout an infant’s motor competence,the pediatrician should organize data gathered from the history, physical examination, and neuro-developmental examination accord-ing to the following schema: 1) motor developmental milestones,2) the classic neurologic examina-tion, and 3) cerebral neuromotormaturational markers (primitivereflexes and postural reactions).Motor milestones are extracted from the developmental history aswell as from observations during the neurodevelopmental examina-tion. Reference tables of sequentialgross and fine motor milestones are necessary (Table 2).

Results of assessment in anydomain is summarized best as indi-cating a developmental age for the

Pediatrics in Review Vol. 18 No. 7 July 1997 227

CHILD DEVELOPMENTInfancy

TABLE 1. Average Physical Growth Parameters

OCCIPITOFRONTALAGE CIRCUMFERENCE HEIGHT WEIGHT DENTITION

Birth 35.0 cm 50.8 cm 3.0 to 3.5 kg Central incisors—6 mo(13.8 in) (20.0 in) (6.6 to 7.7 lb) Lateral incisors—8 mo

+2 cm/mo (0 to 3 mo) +25.4 cm Regains birthweight by 2 wk+1 cm/mo (3 to 6 mo) Doubles birthweight by 5 mo+.5 cm/mo (6 to 12 mo)Mean = 1 cm/mo

1 year 47.0 cm 76.2 cm 10.0 kg First molars—14 mo(18.5 in) (30.0 in) (22 lb) Canines—19 mo

+2 cm +12.7 cm Triples birthweight

2 years 49.0 cm 88.9 cm 12.0 to 12.5 kg Second molars—24 mo(19.3 in) (35.0 in) (26.4 to 27.5 lb)

Quadruples birthweight

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CHILD DEVELOPMENTInfancy

TABLE 2. Motor Development

MOS.

1

2

3

4

5

6

7

8

9

GROSS MOTOR SKILLS

Head up in prone

Chest up in prone positionHead bobs erect if held

sitting

Partial head lagRests on forearms in

prone

Up on hands in proneRolls front to backNo head lag

Rolls back to frontLifts head when pulled

to sitSits with pelvic supportAnterior protection

Sits-props on hands

Sits without supportSupports weight and

bounces while standingCommando crawlsFeet to mouthLateral protection

Gets into sitting positionReaches with one hand

while 4-point kneeling

Pulls to standCreeps on hands and

knees

FINE MOTOR SKILLS

Hands tightly fisted

Retains rattle (briefly) if placed in handHands unfisted half of time

Hands unfisted most of timeBats at objectsSustained voluntary grasp possible if

object placed in ulnar side of hand

Obtains/retains rattleReaches/engages hands in supineClutches at objects

Transfers objects hand-mouth-handPalmar grasp of dowel, thumb

adducted

Transfers objects hand-handImmature rake of pellet

Radial-palmar grasp of cubePulls round peg out

Inferior scissors grasp of pellet; rakesobject into palm

Scissors grasp of pellet held betweenthumb and side of curled index finger

Takes second block; holds 1 block in eachhand

Radial-digital grasp of cube held withthumb and finger tips

Inferior pincer grasp of pellet heldbetween ventral surfaces of thumband index finger

RED FLAGS

Rolling prior to 3 months mayindicate hypertonia

Poor head control

W-sitting and bunnyhopping, mayindicate adductorspasticity orhypotonia

Persistence ofprimitive reflexesmay indicateneuromotordisorder

continued

228 Pediatrics in Review Vol. 18 No. 7 July 1997

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CHILD DEVELOPMENTInfancy

TABLE 2. Motor Development (continued)

MOS.

10

11

12

14

16

18

20

22

24

GROSS MOTOR SKILLS

Cruises around furnitureWalks with 2 hands held

Stands aloneWalks with 1 hand held

Independent stepsPosterior protection

Walks wellindependently

Creeps up stairsRuns stiff-leggedClimbs on furnitureWalks backwardsStoops and recovers

Push/pulls large objectThrows ball while

standingSeats self in small chair

Walks up stairs with hand held

Walks up stairs with rail,marking time

Squats in play

Jumps in placeKicks ballWalks down stairs with

rail, marking timeThrows overhand

FINE MOTOR SKILLS

Isolates index finger and pokesClumsy release of cube into box;

hand rests on edge

Pincer grasp, held between distal padsof thumb and index finger

Fine pincer grasp of pellet betweenfinger tips

Marks with crayonAttempts tower of 2 cubesPrecise release of cubeAttempts release of pellet into bottle

Tower of 2 cubesAttains third cube

Precise release of pellet into smallcontainer

Tower of 3 cubes

Imitates scribble

Tower of 4 cubesCrudely imitates single strokeScribbles spontaneously

Completes square pegboard

Tower of 6 cubes

Train of cubes without stackImitates vertical stroke

RED FLAGS

Failure to developprotective reactionsmay indicateneuromotordisorder

Hand dominanceprior to 18 monthsmay indicatecontralateralweakness

Inability to walk upand down stairsmay be the resultof lack ofopportunity

Illustrations and accompanying text modified with permission from the Erhardt Developmental Prehension Assessment. In Erhardt RP.Developmental Hand Dysfunction: Theory Assessment, Treatment. 2nd ed. San Antonio, Tex: Therapy Skill Builders; 1994.

Pediatrics in Review Vol. 18 No. 7 July 1997 229

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child. This approach makes it pos-sible to consider the child in termsof his or her level of functioningcompared against chronologic age.For example, the developmentalquotient (DQ) is the developmentalage divided by chronologic agetimes 100 (see Example below).This provides a simple expression of deviation from the norm. Aquotient above 85 in any domain is considered within normal limits; a quotient below 70 is consideredabnormal. A quotient between 70and 85 represents a gray area thatwarrants close follow-up. Values inthe upper limit of normal do notparticularly indicate supernormalabilities. Whether truly gifted ath-letes can be recognized early by useof this method is thought-provokingbut speculative.

GROSS MOTOR DEVELOPMENT

Gross motor development proceedsfrom a sequence of prone milestones(beginning with head up and ending

with rolling), to sitting, and thenthrough a standing/ambulatingsequence (Fig. 2). Motor milestonesdo not take into account the qualityof a child’s movement. Thesesequences must be considered in thecontext of the motor portion of theneurologic examination, includingobservations of station and gait,where qualitative features can beassessed. However, the neurologicevaluation of tone, strength, deeptendon reflexes, and coordination is difficult in very young infantsbecause of the subjective nature of the assessments and the infant’slimited ability to cooperate. Clinicalexperience is essential for obtainingaccurate and useful information.

Eliciting reflexes requirespatience and repeated, yet gentle,trial and error. Muscle tone (passiveresistance) and strength (active resis-tance) are a challenge to distinguishin the contrary infant. The best cluescan be obtained from observation, not handling. Spontaneous or

prompted motor activities (eg,weight-bearing in sitting or stand-ing) require adequate strength. Thus, weakness may be appreciatedbest from observing the quality ofstationary posture and transitionmovements. The Gower sign (arisingfrom sitting on the floor to standing,using the hands to “walk up” one’slegs) is a classic example andindicative of pelvic girdle andquadriceps muscular weakness. Not until 2 to 3 years of age doesthe neurologic examination becomeeasier and more meaningful as cooperation improves.

Station refers to the postureassumed in sitting or standing andshould be viewed from anterior, lateral, and posterior perspectives,looking for body alignment. Gaitrefers to walking and is examined in progress. Initially, the toddlerwalks on a wide base, slightlycrouched, with the arms abductedand slightly elevated. Forward progression is more staccato thansmooth. Movements graduallybecome more fluid, the base narrows,and arm swing evolves, leading to an adult pattern of walking by 3 years of age.

The motor neuromaturationalmarkers are the primitive reflexes,which develop during gestation and generally disappear between the third and sixth month after birth, and the postural reactions,which are not present at birth butdevelop sequentially between 3 and10 months of age (Fig. 3). TheMoro, tonic labyrinthine, asymmet-ric tonic neck, and positive supportreflexes are the most useful clini-cally (Fig. 4). As with all truereflexes, each requires a specific sensory stimulus to generate thestereotyped motor response. Normalinfants demonstrate these postures

230 Pediatrics in Review Vol. 18 No. 7 July 1997

65431 20 Months

FIGURE 2. Chronologic progression of gross motor development. Adapted with permission from Piper MC, Darrah J. MotorAssessment of the Developing Infant. Philadelphia, Penn: WB Saunders Co; 1994. Illustrations by Marcia Smith.

CHILD DEVELOPMENTInfancy

Example: Motor Quotient

A 12-month-old boy is seen for health supervision. He is not walkingalone, but he pulls up to stand (9 months), cruises around furniture (10 months), and walks fairly well when his mother holds both hands (10 months). This child has a gross motor age of 10 months at a chronologic age of 12 months. Should this 2-month discrepancy be aconcern? To decide, one should calculate the DQ by using these grossmotor milestones:

motor age 10 monthsDQ =

chronologic age × 100 =

12 months = 83

The motor age and the developmental quotient are good summarydescriptors of the child and have more meaning than plotting each milestone. Because the lower limit is 70, this boy’s DQ falls within the “suspect” or gray zone. In reality, infants falling into the gray zoneof motor domains usually do quite well and rarely require referral to anearly intervention program. This is in contrast to those falling in thegray zones of the cognitive domains.

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inconsistently and transiently; thosewho have central neurologic (ie,cerebral) injuries show stronger and more sustained primitive reflexposturing. Primitive reflexes aresomewhat difficult to gauge, even in expert hands. The appearance of postural reactions in sequencebeginning after 2 or 3 months of ageis easier to elicit clinically and canprovide great insight into the neuro-motor integrity of young infants.Postural reactions are sought in each of the three major categories:righting, protection, and equilibrium.These movements are much lessstereotyped than the primitive reflexes, and they require a complexinterplay of cerebral and cerebellarcortical adjustments to a barrage of sensory inputs (proprioceptive,visual, vestibular) (Figs. 5 and 6).They are easy to elicit in the normal infant but are markedly slow in appearance in the infant who has central nervous systemdamage.

FINE MOTOR DEVELOPMENT

In the first year of life, fine motordevelopment is highlighted by theevolution of a pincer grasp. Duringthe second year of life, the infantlearns to use objects as tools duringfunctional play. There are manystages in accomplishing these twoskills; selected ones are illustrated in Table 2. In the early months, theupper extremities assist with balanceand mobility. As balance in the sit-ting position improves and the infantassumes biped mobility, the handsbecome more available for manipula-tion of objects—their ultimate func-tion. Primitive reflexes are inte-grated, and the upper extremitiescome under cortical control. Reach-

ing becomes more accurate, andobjects are brought to the mouth fororal exploration. As developmentprogresses from proximal to distal,reaching and manipulative skills areenhanced further, and precise manualexploration replaces oral exploration.During the second year, fine motorskills are assessed by observing themanner in which the hands useobjects as tools (eg, blocks to buildand crayons to draw). The closeassociation between gross and finemotor skills in the first year of lifeevolves into a similar relationshipbetween problem-solving and finemotor skills during the second year.One skill enables or promotes thedevelopment of the other. If progressin manual dexterity is slow, this mayimpede cognitive development viamanipulation of objects.

RED FLAGS IN MOTOR DEVELOPMENT

It is important to begin the motorevaluation by observing the infant.Pay particular attention to the hands;persistent fisting at 3 months of ageoften is the earliest indication ofneuromotor dysfunction. Sponta-neous postures (eg, froglegs andscissoring) provide visual clues tohypotonia/weakness and spastichypertonus, respectively. Delays inthe appearance of postural reactionsherald future delays in voluntarymotor development. An infant willbe unable to sit or walk indepen-dently without intact protective andequilibrium mechanisms. Abnormalmovement patterns may indicatepathology. For example, earlyrolling (1 to 2 months), pullingdirectly to a stand at 4 months(instead of to a sit), W-sitting,

bunny hopping, and persistent toewalking may indicate spasticity.Hand dominance prior to 18 monthsof age should prompt the clinician to examine the contralateral upperextremity for weakness associatedwith a hemiparesis.

Analysis of the information gathered in these areas makes it relatively easy for the practitioner to reassure him- or herself (and theparents) about a child’s motor com-petence or to identify motor impair-ment at an early age. Once a motorabnormality has been identified, further assessment of its exactnature and etiology is essential. Thisalmost always warrants referral toan appropriate subspecialist or sub-specialty team. Based on clinicalexamination and history, the astuteclinician usually can decide intowhich category the motor disorderfalls: 1) static central nervous systemdisorders, 2) progressive diseases,3) spinal cord and peripheral nerveinjuries, or 4) structural defects.

Cognitive DevelopmentCognitive processing skills are thesubstrate for intelligence and includea wide range of abilities (Table 3).Intellectual development depends on learning that contains three components: attention, informationprocessing, and memory (whichincludes both encoding and retrievalof information). Intellectual develop-ment is reflected in advancing abili-ties to comprehend, reason, andmake judgments. Standardized intel-ligence tests generally measure twoforms of intelligence in the school-age child: verbal and performance(or nonverbal). Such standardized

Pediatrics in Review Vol. 18 No. 7 July 1997 231

CHILD DEVELOPMENTInfancy

12111097 86

FIGURE 2. Continued

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232 Pediatrics in Review Vol. 18 No. 7 July 1997

CHILD DEVELOPMENTInfancy

tests are not available to measureinfant intelligence. How then, doesone recognize the attributes of ver-bal and nonverbal intelligence ininfants? In the past two decades, the discovery of visual habituationtechniques to assess infants’ atten-tion was considered a breakthroughin the study of infant cognition. It is exemplified by one study thatdescribes 4-day-old infants listeningto a long series of “bee-see-lee”sounds. When a novel “da” soundwas heard, the infants respondedwith a change in heart rate andfaster, stronger sucking on a pacifier,thereby indicating that very younginfants can perceive differences invowel sounds.

More complex studies usingsimultaneous auditory and visualstimuli indicate that infants also arecapable of organizing perceptionsacross sensory modalities (cross-modal matching) without the lan-guage skills to describe them. Forexample, 11-month-old infants were presented a sequence of con-tinuous and interrupted pure tones.Two pictures were in the infants’view throughout the experiment: one contained a continuous line, the other a dashed line. The infantsconsistently matched the correctvisual stimulus to the auditory one,inferring cross-modal matching andsome rudimentary understanding of the concept of interruptedness.Using these techniques, it has beendemonstrated that infants youngerthan 1 year old can form a widerange of fairly complex categoricalrepresentations, including those forfaces, color, geometric shapes, andorientation of lines.

The attempts to measure infantresponses precisely, such as thosedescribed previously, depend onsophisticated technology, includinginfra-red photography for trackinginfant eye gaze and pupillary dilata-tion, videotaping of facial reactions,and electrophysiologic monitoring of heart rate and evoked potentials.The primary pediatrician can bestestimate infant intelligence by evalu-ating problem-solving and languagemilestones. Language is the singlebest indicator of intellectual poten-tial; problem-solving skills are thenext best measure. Gross motorskills correlate least with cognitive

FIGURE 4. Clinically useful reflexes. A. Tonic labyrinthine reflex. In the supine posi-tion, the baby’s head is extended gently to about 45 degrees below horizontal. Thisproduces relative shoulder retraction and leg extension, resulting in the “surrenderposture.” With head flexion to about +45 degrees, the arms come forward (shoulderprotraction) and the legs flex. B. Asymmetric tonic neck reflex (ATNR). The sensorylimb of the ATNR involves proprioceptors in the cervical vertebrae. With active orpassive head rotation, the baby extends the arm and leg on the face side and flexesthe extremities on the occiput side (the “fencer posture”). There also is some mildparaspinous muscle contraction on the occiput side that produces subtle trunk curvature. C. Positive support reflex. With support around the trunk, the infant issuspended and then lowered to pat the feet gently on a flat surface. This stimulusproduces reflex extension at the hips, knees, and ankles so the infant stands up, completely or partially bearing weight. Children may go up on their toes initially but should come down onto flat feet within 20 to 30 seconds before sagging backdown toward a sitting position. From Blasco PA. Pediatric Rounds. 1992;1(2):1– 6.Reprinted with permission.

FIGURE 3. The declining intensity of primitive reflexes and the increasing role ofpostural reactions represent at least permissive, and possibly necessary, conditionsfor the development of definitive motor actions. From Capute AJ, Accardo PJ, Vining EPG, Rubenstein JE, Harryman S. Primitive Reflex Profile. Baltimore, Md:University Park Press; 1978. Reprinted with permission.

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potential; most infants who are diag-nosed later with mental retardationwalk on time.

PROBLEM-SOLVING

Problem-solving skills consist ofmanipulating objects to solve aproblem (eg, choosing the correctopening for a circular shape in athree-piece form board). The infant’sability to solve a problem dependson intact vision, fine motor coordi-nation, and cognitive processing.During the early weeks of life, theinfant explores the environmentvisually. Later, these visual experi-ences reinforce movement. As theupper extremities come under visualguidance, reaching and grasping areenhanced. At first, the infant bringsobjects to the mouth for oral explo-ration. Later, the infant visuallyexamines an object held in one handwhile manipulating it with the other.Isolation of the index finger pro-motes more refined manipulation ofthe various parts of objects, and theinfant becomes successful in discov-ering how they work (eg, fingeringthe clapper of the bell). Mouthing ofobjects becomes less appealing. Thisprecise manual-visual manipulation,triggered by a heightened curiosityand facilitated by a longer attentionspan, heralds true “inspection” ofobjects. The infant is progressingfrom “learning to manipulate” to

“manipulating to learn.” Improvedmacular vision (via myelination ofthe fovea) and refinement of the pincer grasp promote inspection of progressively smaller objects. As cognitive abilities continue toadvance, the infant learns to shiftattention between two objects (onein each hand), compare, makechoices, and discard or combineobjects. This sensory-motor phase of learning is the foundation forongoing nonverbal intellectualdevelopment.

The 1-year-old child recognizesobjects and associates them withtheir functions. Thus, he or shebegins to use them functionally as“tools” instead of mouthing, bang-ing, and throwing them. This childhas left the period of sensory-motorplay and entered the stage of func-tional play. Play serves as a windowinto the infant’s thoughts andbecomes particularly important dur-ing the next stage of symbolic play.At this point, the infant uses toysthat represent real objects in actions toward him- or herself (putting a toytelephone to the ear and vocalizing) and later in actions toward dolls or teddy bears (putting a toy tea cup tothe doll’s mouth). The use of sym-bols lays the foundation for imagi-nary play. This next stage of playusually does not appear until 24 to30 months of age.

The interdependence of languageand problem-solving developmentbecomes stronger as the child beginsto label objects and actions. Midwaythrough the second year, this abilityto label and categorize allows thechild to match objects that are thesame (car to a car and spoon to aspoon) and later to match an objectto its picture. Nonverbal intelligenceis assessed by observing the infantinteract with test objects. In theolder child, it is assessed throughstandardized pencil and paper tasksor computerized tests.

One aspect of nonverbal cogni-tive development deserves extraattention: object permanence, a con-cept studied extensively by Piaget.Prior to the infant’s mastery ofobject permanence, a person orobject that moves “out of sight” is“out of mind”; its disappearancedoes not evoke a reaction. The abil-ity to maintain an image of a persondevelops before that of an object.The child will show interest in peek-a-boo play, and separation anxietywill occur when a loved one leavesthe room. Shortly thereafter, thechild will begin to look for an objectthat has been dropped. At first, anauditory cue when it hits the floor is necessary to locate it. Later, thechild will experience success infinding an object that was droppedfrom sight and landed silently. Next,the child will progress to finding anobject that has been hidden under acloth or cup. A more complex taskis locating an object that has beenwrapped inside a cloth. Successrequires persistence and memory ofthe object long enough to completethe three-part unwrapping process.The next skill in this sequence is the ability to locate an object underdouble layers (eg, a cube is placedunder a cup and then the cup is cov-ered with a cloth). This is followedby the ability to locate an objectafter serial displacements. In thistask, an object is hidden under one cover and then changed to anotherone. The younger infant always will look for it under the first cover,even though the position change wasseen. Later, he or she will becomesuccessful with this task, as long aseach successive displacement still iswitnessed. Not until the end of thesecond year is the child able to

Pediatrics in Review Vol. 18 No. 7 July 1997 233

FIGURE 5. Normal parachute reaction.The examiner has suspended the childhorizontally by the waist and loweredhim face down toward a flat surface. Thearms extend in front, slightly abducted at the shoulders, and the fingers spreadas if to break a fall. From Blasco PA.Pediatric Rounds. 1992;1(2):1–6.Reprinted with permission.

FIGURE 6. The infant is seated comfort-ably, supported about the waist if neces-sary. The examiner gently tilts the childto one side, noting righting of the headback toward the midline, protectiveextension of the arm toward the side, andequilibrium countermovements of the armand leg on the opposite side. FromBlasco PA. Pediatric Rounds. 1992;1(2):1–6. Reprinted with permission.

CHILD DEVELOPMENTInfancy

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234 Pediatrics in Review Vol. 18 No. 7 July 1997

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CHILD DEVELOPMENTInfancy

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236 Pediatrics in Review Vol. 18 No. 7 July 1997

deduce the location of an object that is hidden without observing the displacement.

Another important concept domi-nating this period of development iscausality. Initially, the infant acci-dentally discovers that his or heractions produce a certain effect (eg, kicking the side of the crib activates a mobile overhead). Theinfant learns to repeat these actionsto obtain the same effects. Later, he or she will vary actions to cause a novel effect (pulling a string toobtain the ring). The concept ofcausality parallels social develop-ment in which the infant learns tomanipulate the environment by cry-ing or smiling to obtain the desiredreaction from caregivers. As theinfant approaches 2 years of age, he or she will learn that apparentunrelated actions can be combinedto produce an effect (eg, winding a key to make a toy move).

LANGUAGE DEVELOPMENT

Delays in language development aremore common than delays in otherdevelopmental domains. Parents andpediatricians generally are lessfamiliar with language milestones.Language is the most difficultdomain to assess by observationbecause infants rarely vocalize spontaneously in the clinician’soffice. For this reason, it is essentialfor the clinician to obtain a thoroughand accurate language history. Thepediatrician should become familiarwith milestone terminology andlearn to give examples (eg, “razz-

ing”). Between 10 and 18 months of age, word counts help in assess-ing a child’s expressive skills; after18 months of age, vocabulariesincrease exponentially, and it is difficult to keep up with counts.

Language includes receptive and expressive skills. Receptiveskills reflect the ability to under-stand language; expressive skillsreflect the ability to make thoughts,ideas, and desires known to others.Expression of language can takeseveral forms: speech, gestures, sign language, writing, typing, and“body language.” Thus, languageand speech are not synonymous.Speech is simply the vocal expres-sion of language. A child can havenormal language and yet be unableto speak. Examples include childrenwho are deaf and children who havesevere cerebral palsy. The child who has a hearing impairment may use manual sign language to communicate. A child who hasnormal intelligence but cannot speak because of oral-motor dys-function related to cerebral palsymay use a computer that is activatedwith a head stick. Conversely, a few children talk but fail to usespeech to communicate (eg, childrenwho have autism). Their vocaliza-tions consist of “parrot talk” orecholalia that has no communicativeintent and, thus, does not representlanguage.

Language development duringinfancy can be divided into threeperiods: prespeech, naming, andword combination periods.

1. Prespeech Period (0 to 10 months):Receptive language is character-ized by an increasing ability tolocalize sounds. Sound localizationis assessed by using a noisemakersuch as a bell (Fig. 7). Expressivelanguage consists of musical-likevowel sounds (cooing) that are interrupted by crying whenthe baby has a need. At about 3 months, the infant will beginvocalizing immediately uponhearing an adult speak. One ortwo months later the infant issilent and assumes a posture thatimplies he or she truly is “listen-ing” to the speaker. These infantsmake no vocalizations until thespeaker is quiet, mimic thespeaker, and then quiet againwhen the adult speaks. Theyappear to enjoy the “vocal tennis”and repeat this for several cycles.At approximately 6 months ofage, the infant adds consonants tothe vowel sounds in a repetitivefashion (babbling). Soon theinfant appears to initiate conver-sations. When a random vocaliza-tion (eg, “dada”) is interpreted bythe parents as a real word, theyshow pleasure and joy. In sodoing, adults give meaning tothese first “words” and reinforcetheir repeated use.

2. Naming Period (10 to 18 months):This period is characterized bythe infant’s realization that peoplehave names and objects havelabels. It is an important turningpoint in language development.The “dada” and “mama” that

FIGURE 7. Orienting to sound of bell. In the first stage (5 months), when a bell is rung at one side of the infant’s head (A), theinfant turns horizontally to the correct side (B). In the second stage (7 months), when a bell is rung at one side of the head (A),the infant localizes the sound by a compound visual maneuver consisting of a horizontal followed by a vertical component (C).In the third stage (91⁄2 months), when a bell is rung to one side of the head (A), the infant localizes the sound by a single visualmovement (D). From Capute AJ, Accardo PJ. Clin Pediatr. 1978;17:850. Reprinted with permission.

CHILD DEVELOPMENTInfancy

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were vocalized randomly havebeen reinforced, so the infantnow begins to use them appropri-ately. Infants next recognize andunderstand their own names andthe meaning of “no.” This marksthe beginning of exponentialgrowth in receptive language. By 12 months of age, someinfants understand as many as100 words. They also can followa simple command as long as thespeaker uses a gesture. Early inthe second year, a gesture nolonger is needed to aid in com-prehension of the command.Expressive language progresses at a somewhat slower rate. Theinfant will say at least one “real”word (ie, other than mama, dada,or a proper name) before his orher first birthday. At this time,the infant also will begin to verbalize with sentence-like intonation and rhythm (immaturejargoning). As the expressivevocabulary increases, real wordsare added (mature jargoning). By the end of the naming period,the infant will use approximately25 words spontaneously.

During this period, pointingbecomes important to both receptive and expressive languageskills. Pointing already hasbecome a method of explorationwithin the problem-solvingdomain. The infant beginning tolook in the general vicinity wherethe adult is pointing is a receptivelanguage skill. This ability isfacilitated by the infant’s newrealization that objects havelabels. Later, the infant begins totake part in pointing games. Heor she will point first to familymembers, then objects, bodyparts, articles of clothing, andpictures upon request. These allreflect receptive language skills.

Pointing also is used for language expression. First, theinfant points at an object anduses the adult as a tool to retrievethe object, referred to by linguistsas protoimperative pointing. Theinfant first points to the object(eg, a cookie) and then looksback and forth between the adultand the object expectantly. At alater stage, he or she directsattention to the adult and alter-

nately points at the adult and thedesired object while vocalizing(eg, “uh...uh”). Next, the infantuses the object as a tool to obtainthe parent’s attention (protode-clarative pointing). Protodeclara-tive pointing is a social act; the parent is an active and importantpartner in a shared world. Ratherthan acquisition of the object, theinfant’s goal becomes the parent’sacknowledgment of the interest-ing object. For example, when aninfant hears an airplane overhead,he or she points to it and vocal-izes to get the parent to look at it. If the parent does not complywith these initial efforts, theinfant may approach the parentand turn his or her face toward

the plane in a more determinedeffort to obtain what is some-times called “joint attention.”Finally, the infant will point at anobject and vocalize (“uh?”) in aneffort to obtain the proper labelor name for that object from thelistener. This is called “pointingfor naming.”

3. Word Combination Period (18 to24 months): Typically, childrenbegin to combine words approxi-mately 6 to 8 months after theysay their first word. If word com-binations appear much earlier,they are likely “giant words.”Giant words are two- or three-word combinations that the infanthears frequently, such as “Thankyou,” “Stop it,” or “Let’s go.”When the infant says one ofthese, he or she really is treatingthe phrase as a polysyllabic sin-gle word. At this stage of devel-opment the infant does not useeither word separately or in novelcombinations with other words.“Holophrases” also are beginningto appear at this time. For exam-ple, an infant may point to amother’s keys and say “mommy”instead of saying “keys.” In this context, the single word,“mommy,” has a sentence-likemeaning, such as “These keys

belong to mommy.” Single wordstake on multiple meanings and nolonger simply label an object.The infant usually does not com-bine words into true phrases orsentences until he or she has acquired an expressive vocabu-lary of approximately 50 words.Early word combinations are“telegraphic” in that they do notcontain function words (preposi-tions, pronouns, and articles).They do, however, convey thesame meaning as the moremature sentence. For example,“Go out,” in the context of thesituation, conveys the samemeaning as “I want to go out-side.” Telegraphic speech is thefirst stage in the child’s ability to

“grammaticize” speech, that is, to form sentences with propermorphology and syntax. At thispoint in development, a strangershould be able to understand atleast 50% of the infant’s speech(intelligibility). Language blos-soms after 2 years of age.

RED FLAGS IN COGNITIVEDEVELOPMENT

Language development provides theclinician with an estimate of verbalintelligence; skill development in theproblem-solving domain provides anestimate of nonverbal intelligence. Ifdeficiencies are global (ie, skills aredelayed in both domains) and signif-icant (ie, >2 standard deviationsbelow the mean), there is a possibil-ity of mental retardation. Mentalretardation refers to significant sub-average general intellectual function-ing as measured by standardizedtests. By current definition, thesedeficits must be associated with sig-nificant deficits in adaptive function-ing. About 3% of the population ismentally retarded. If the deficienciesare very mild (ie, in the low rangeof normal), the child is consideredto be of borderline intelligence or a “slow learner.”

When a discrepancy existsbetween problem-solving and lan-

Pediatrics in Review Vol. 18 No. 7 July 1997 237

CHILD DEVELOPMENTInfancy

Word combination begins approximately 6 to 8 months after an infant says his or her first words.

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guage abilities, with only languagebeing deficient, one must considerthe possibility of a hearing impair-ment or a communication disorder. If either language or problem-solv-ing skills is deficient, the child is athigh risk for manifesting a learningdisability later. A learning disability refers to academic achievement thatis substantially below what wouldbe expected from a person’s generalintellectual potential. Approximately5% to 7% of school-aged childrenhave learning disabilities. A learningdisability cannot be diagnosed for-mally until the child reaches school

age and demonstrates an inability tokeep up in one or more academicareas. Thus, a reading disability can-not be diagnosed until at least age 6 or 7 years when children normallyare expected to read. A delay in lan-guage development is a “red flag”and should prompt careful monitor-ing and further evaluation if thechild later demonstrates reading difficulties in school. The neurologicsubstrate for specific learning dis-abilities involves patchy dysfunctionin cortical information processingthat results in specific difficultieswith academic tasks.

Unless the deficiencies are severe during infancy, a child rarelypresents with a parental concern of“cognitive delay.” Concerns usuallypresent as speech delays, but suchcomplaints are infrequent before 24 months of age. The average ageat which mental retardation is diag-nosed is 3 to 4 years. Usually, themore severe the degree of impair-ment, the earlier the diagnosis ismade. Because the majority of chil-dren who are mentally retarded arein the mild category, most childrenare diagnosed well after infancy.Some are not diagnosed until theyenter school. The child who is bornwith dysmorphic features and has arecognizable syndrome known to beassociated with mental retardationwill be diagnosed earlier regardlessof the degree of impairment. Addi-tionally, abnormal findings on mag-

netic resonance imaging (performedbecause of atypical head growth orbecause of a known cerebral insult)indicate that the child is at risk forintellectual deficits.

Although a cognitive deficit isthe most common reason for lan-guage delay, all children who havedelayed language developmentshould receive audiologic testing to rule out hearing loss. The child who has a hearing loss will demon-strate normal expressive languageskills through the babbling stage (6 months). He or she will begin tobabble on time, but lack of auditory

reinforcement for these vocalizationsresults in their disappearance and ageneral decline in verbal expression.Receptive language abilities con-tinue to progress normally for a fewmore months. A 1-year-old who isdeaf will follow a command with a gesture (relying solely on the gestural cue) and may seem to hear.This ability to use environmentalcues can fool parents and profes-sionals and is one of the chief reasons that the average age of diagnosis of a severe hearing loss is2 years. Children who have a mildhearing loss will present even laterwith articulation errors, inability tolocalize sounds, or “attentional prob-lems.” An infant who is deaf willattempt to communicate by usinggestures. If a child has delayedspeech and fails to demonstrate adesire to communicate, a more pervasive problem, such as autism,should be considered. Although chil-dren who have autism may demon-strate protoimperative pointing (eg, pointing to obtain food or drink),they rarely point to the object for thepurpose of having the adult join inthe pleasure of admiring an interest-ing object (protodeclarative point-ing) or point to obtain the name of an object. Prodeclarative pointing isa social action, and one of the cardi-nal features of autism is the lack ofsocial relatedness. Another red flagis the finding that a child’s expres-sive skills are advanced compared

with his or her receptive skills. Achild who speaks in five-word sen-tences but does not understand sim-ple commands is at risk of having apervasive developmental disorder.The advanced speech may not befunctional or have communicativeintent. Finally, some parents willexcuse their child’s lack of speechbecause of an “Uncle Albert” whodidn’t speak until he was 4 years old but grew up to be a rocket scientist. In reality, this is very rare. Normal receptive languageskills in a child who has speechdelay would be reassuring and typically are easy to demonstrate.

Other problems may masqueradeas cognitive delay or impair theassessment of cognitive abilities.Problem-solving tasks require intactfine motor skills. Having poor fine motor skills puts the child at a dis-advantage with certain manipulativetasks used to assess nonverbal cog-nition. Due to cerebral palsy, a childmay not be able to place a squareform in a form board; however, heor she might be able to indicate thecorrect position by pointing or byeye gaze. Thus, the child actuallycould “pass” the form board item inthe problem-solving assessment.Similarly, visual impairment caninterfere with a child’s ability to perform many problem-solving tasks successfully.

Psychosocial DevelopmentEmotional, social, and adaptivemilestones have been assimilatedfrom multiple sources (Table 4).These milestones are more variablethan those in motor and cognitivedomains because of the greaterinfluence of environmental factors(nurture). An infant inherits a set ofemotional-social characteristics anda style of interacting, but these aremodified by parenting style, “good-ness of fit,” and the social environ-ment. Emotions include the infant’sfeelings as well as the expression ofthese feelings. Social milestonesinclude the steps necessary to forminterpersonal relationships. Tempera-ment influences social relationshipsand generally reflects a consistentpattern (or style) in “how” a childreacts. It is different from the

238 Pediatrics in Review Vol. 18 No. 7 July 1997

CHILD DEVELOPMENTInfancy

. . . all children whose language development is delayedshould receive audiologic testing.

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Pediatrics in Review Vol. 18 No. 7 July 1997 239

CHILD DEVELOPMENTInfancy

TABLE 4. Psychosocial Development

AGE IN MONTHS EMOTIONAL SOCIAL ADAPTIVE RED FLAGS

1–3 Interest Understands relationships State regulation IrritabilityDisgust between voices and faces Requires only one Sleep/eating disturbancesDistress (pain, hunger) Bonding (parent → infant) night feedingEnjoyment (social smile) Smiles reciprocally

Follows moving person with eyes

3–6 Anger Recognizes mother Absent smile may Happiness Attachment (infant → parent) indicate visual loss, Joy Anticipates food on sight attachment problems, Pleasure Smiles spontaneously or maternal depressionSadnessDispleasure

6–9 Personality unfolds Discriminates emotional Gums/swallows cracker Absent stranger anxietyFear facial expressions and Places hands on bottle may be due to multiple

reacts differently Takes solids well care providers Preference for a given Finger feeds dry cereal (eg, NICU care)

personStranger anxietyUnderstands means-to-an-end

relationship in social interactions (act→clap →repeat act)

9–12 Assertiveness Differential fear response Holds bottleCautiousness based on gender and age Holds, bites, chews

Concept of self cracker/cookieSocial interactions become Drinks from cup held

intentional and goal-directed for him or herSeparation anxiety

12–15 Shyness Solitary play Cooperates with dressingEmpathy Begins formation of Drinks from cup; Sharing relationships some spillageSelf-comfort • Love Removes socks/hat

(eg, attachment • Friendshipto blanket) • Acquaintance

• StrangersOffers ball to mirror imageKisses by simply touching

lips to skin or licks

15–18 Shame/guilt Self-conscious period; Uses spoon; some Lack of social Contempt “coy” stage spillage relatedness may

Hugs parents indicate autism

18–21 Associates feelings First application of attributes Drinks from cup with verbal symbols to self (eg, good, little, without spilling

Begins to have thoughts naughty) Moves about houseabout feelings Initiates interaction by calling without adult

to adult Emerging independenceKisses with a pucker Removes a garment

21–24 Beginning “socialization” Imitates others to please them Replaces some objects Persistent poor transitionsof emotional expression Recursive nature of social where they belong may indicate a pervasiveby social/cultural thought (ie, thinking about Uses spoon well developmental disorderinfluences “How I behave to you Opens door by turning • modulation of emotion and you to me”) knob• masking of emotion Parallel play Removes clothes without

Infant’s reaction to Tolerates separation; buttonsambiguous events is will continue activity Unzips zippersshaped by emotional Puts shoes on part wayreactions of others

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“why” (motivation) and the “what”(content) of social interactions. The inclusion of adaptive skills (ie, skills required for independencein feeding, dressing, toileting, andother activities of daily living) isunique to the discussion of psycho-social development and reflects the concept that these skills influ-ence, and are influenced by, socialfactors.

EMOTIONAL DEVELOPMENT

Emotions are present in infancy andmotivate expression (pain elicits crying). Emotion has three elements:neural processes, mental processes(feelings), and motor expression(facial, verbal) and actions. Emo-tions are mediated through the lim-bic system, which is responsible forreceiving, interpreting, and process-ing emotion-producing stimuli andthen initiating and modulating emo-tional responses. There is evidencethat an infant can express emotionwithout direct cognitive mediation.An infant who has anencephaly orhydranencephaly may show disgust

at sour flavors and interest in sweetflavors in ways very similar to anormal infant. Later, in the normalinfant, these instinct-like reactionsare modified by cognition. Althoughemotional feelings are constant overthe life span, their causes changeand become more abstract. Theinfant may show disgust for a bittertaste; the older child may show disgust for a revolting idea. Otheremotions have a definite cognitivefoundation. To experience fear, the 7- to 9-month-old child must be able to shift attention, compare,and recognize “familiar” from“unfamiliar” in the development of stranger anxiety. As the childdevelops, the interrelationshipbetween emotion and cognitionbecomes increasingly complex.When the child begins to associatelanguage symbols with emotions and memory, he or she can remem-ber prior emotional experiences. A verbal reminder of the event

then can evoke feelings identical to those experienced previously.Thus, language and cognition addflexibility and complexity to emotional behavior.

The expression of emotions alsoevolves with age and developmentaladvancement. Consider this exampleof an emotional reaction (fear) to astranger, based on skill level:

9 months

Cries and turns head away (mass body reaction)

and (avoidance reaction)

24 months

Runs away (motor development)

48 months

Says “Go away” or “Help” (language development);or tries to alter the threat (cognitive development)

In addition to developmentalprogress, the feedback loop betweencare providers and child modifiesemotional expression. Social forces

and cultural factors also modulateemotional expression to producemore restrictive and controlled facialsignals. An older child may learn to modulate the expression of pain (a facial grimace only) and appearquite stoic. Furthermore, childrencan learn to mask emotions such as smiling at a disappointing gift. At early stages, however, the trueemotion typically leaks out from under the mask.

SOCIAL DEVELOPMENT

The infant is surrounded by a socialnetwork. Sensory processing isinfluenced by the infant’s socialneeds. The infant has greater dis-crimination ability for social voices)than for nonsocial (environmentalnoise) stimuli. There are two pri-mary theories: the Epigenetic Modeland the Social Network Model. Inthe Epigenetic Model, the mother-child relationship is considered to be all important. If this relationship

is negative, then other relationshipswill be poor. If it is positive, thenfuture relationships will be good.The Social Network Model recog-nizes the relative importance of the mother-child relationship, but also recognizes the ability of otherrelationships to compensate forabsent or poor mother-child interac-tions. The devastating effect of apoor relationship can be overcomeby adequate substitutes and a sup-portive environment. The latterreflects the popular concept of childhood resiliency.

Social milestones begin withbonding, which reflects the feeling of the caregiver for the child. Attachment takes place within a few months and represents the feeling of the infant for the care-giver. These social relationships are manifested by the evolution of the smile, in which the level ofstimulus required to elicit reciprocitydecreases. At first, high-pitchedvocalizations and a smile from theadult are needed; later, a smile aloneis successful. When recognition ofand attachment to a familiar care-giver develops, the simple sight ofthis person (smiling or nonsmiling)will elicit a smile. The infant alsobecomes more discriminating in producing a smile as he or shebegins to differentiate betweenfamiliar and unfamiliar faces. As the infant acquires the concept ofcausality, he or she begins to usesmiling to manipulate the environ-ment and satisfy personal needs.

Later in infancy, other social relationships are established. Severalbehaviors are necessary for thedevelopment of these relationships.First, the infant must have a conceptof self versus others. Next, he or she must be able to put self in theplace of another, that is, to showempathy. The infant must perceive a separate identity with a differentset of needs. He or she must realizethe consequences of his or her inter-actions on others. Empathy is criti-cal to forming a relationship. Nextthe child must be able to share,which is critical to maintaining arelationship. There are four basictypes of relationships: with acquain-tances, strangers, friends, and loves.Whereas relationships with acquain-tances and strangers simply require

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CHILD DEVELOPMENTInfancy

Socioemotional milestones at 52 weeks include offering a ball to a mirror image and cooperating in dressing.

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a concept of self, friendship andlove require all three (a concept ofself, empathy, and sharing). Aboutthe same time that the child canlabel emotions (via language), he or she begins to think about socialinteractions. A child will demon-strate recursive social thoughts, thatis, show early signs of thinkingabout how others behave towardhim or her and how he or shebehaves toward others.

Temperament, or the infant’soverall style of reacting, can affectsocial relationships. The precise definition of temperament is contro-versial, but it generally is believedto represent the characteristic styleof a child’s emotional and behav-ioral response in a variety of situ-ations. It is determined by geneticfactors but is modified by environ-mental forces. Temperament showsconsiderable stability over time.Thomas and Chess describe ninetraits that determine whether a child will have an “easy,” “difficult,” or “slow-to-warm-up”temperament:

1. Activity level—proportions ofperiods of activity to inactivity

2. Adaptability to change3. Positive or negative mood4. Intensity of emotional responses5. Rhythmicity of biologic functions6. Persistence in the face of

environmental counterforces7. Distractibility or ease of soothing8. Approach versus withdrawal

tendencies in new situations9. Threshold of stimulation neces-

sary to produce a response

The Carey Infant TemperamentQuestionnaire often is used to evalu-ate these traits formally. Approxi-mately one third of infants will becharacterized as difficult or slow-to-warm up. The other two thirds willbe classified as easy infants. Theeasy infants fall into three subcate-gories: 1) gentle, tender, sensitive,affectionate; 2) changeable, variable,adaptable; and 3) social, playful,happy, attention-seeking. A child’stemperament can influence develop-mental testing. The child who is difficult or slow to warm up mayrefuse to cooperate with test items,thereby receiving lower scores

that do not reflect his or her trueabilities.

ADAPTIVE SKILL DEVELOPMENT

Adaptive skill development is influ-enced by the infant’s social environ-ment, as well as by motor and cog-nitive skill attainment. A child whohas quadriparesis may not be able tofeed him- or herself, even with nor-mal intelligence and a supportivesocial environment.

In contrast, acquisition of self-help skills by an able-bodied infantmay be delayed in the face of men-tal retardation and the lack of moti-vation to become independent. Inspite of normal motor and cognitiveskills, an infant may demonstratedelays in adaptive skills when socialsupport and encouragement are lack-ing. This is exemplified by delays in self-feeding skills when the care-giver is overly concerned aboutmessy spillage or feels the need torush mealtime. Additionally, parentsmay persist in dressing the olderchild in an effort to rush to childcare. The decision to initiate toilettraining often is influenced by bothfamily and culture.

RED FLAGS IN PSYCHOSOCIALDEVELOPMENT

Decreased rhythmicity (eg, colic)may be an early indication of a “difficult child.” Delay in theappearance of a reciprocal smilemay indicate an attachment problem,which may be associated withmaternal depression. In severe cases, child neglect or abuse may be suspected. However, a delay in smiling also may be associatedwith visual or cognitive impairment.The lack of social relationshipsplays a key role in the diagnosis of autism when it is accompanied by delayed or deviant languagedevelopment and stereotypic behav-iors. History and observation of aninfant’s behavior at play may alertthe clinician to abnormal social relationships. The emotional statusof the parents and parenting stylesmay affect the infant’s developmentof adaptive skills. A controlling,rejecting parenting style may berevealed in an oppositional childwho refuses to cooperate with self-care. Delays in adaptive skillsalso may indicate overprotective

parents or an excessive emphasis on cleanliness.

ConclusionThe journey through infancy truly isfascinating—a time of incomparablyrapid changes in physical growthand motor development. By the endof this period, the child is mobileand explores his or her environmentindependently. The child’s pincergrasp and release rival that of theadult. Cognitive and social changesare equally prodigious. The baby hasprogressed from simple methods ofexpression (crying and grimacing) toa “little person” who has a complexarray of emotional expressions thatare becoming “socialized.” He orshe has learned to use these emo-tions to manipulate the environmentand obtain the attention and theobjects that he or she desires. Addi-tionally, the child can think aboutemotions and feel empathy for theemotions of others. He or she hasstrong love and friendship relation-ships with family members and afew significant others. The next fewyears are characterized by exponen-tial language development, whichwill reveal the complex thoughts,feelings, and humor owned by thisamazing creature destined to becomean adult.

SUGGESTED READINGBooks:Ames LB, Ilg F, Haber CC. Your One-Year

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Brazelton TB, Nugent JK. Neonatal Behav-ioral Assessment Scale. 3rd ed. London,UK: Mac Keith Press; 1995

Capute AJ, Accardo PJ, Vining EPG, Ruben-stien JE, Harryman S. Primitive ReflexProfile. Baltimore, Md: University ParkPress; 1978

Fraiberg SH. The Magic Years. New York,NY: Charles Scribner Sons; 1959

Gesell A, Amatruda CS. Developmental Diagnosis. New York, NY: Paul B. Hoeber,Inc; 1951

Levine MD, Carey WB, Crocker AC. Developmental-Behavioral Pediatrics.2nd ed. Philadelphia, Penn: WB Saunders;1992

Osofsky JD. Handbook of Infant Develop-ment. 2nd ed. New York, NY: John Wiley& Sons, Inc; 1987

Piper MC, Darrah J. Motor Assessment of the Developing Infant. Philadelphia, Penn:WB Saunders Company; 1994

Saint-Anne Dargassies S. The Neuro-Motorand Psycho-Affective Development of theInfant. New York, NY:Elsevier SciencePublishing Co, Inc; 1986

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Blasco PA. Normal and abnormal motordevelopment. Pediatric Rounds. 1992;1:1–6

Blasco PA. Pitfalls in developmental diagnosis.Pediatr Clin North Am. 1991;38:1425–1437

Blizzard RM. The practitioner’s dilemmasabout growth and short stature. PediatricRounds. 1992;1:2–5

Capute AJ. Identifying cerebral palsy ininfancy through study of primitive reflexprofiles. Pediatr Ann. 1979;8:589–595

Capute AJ. Marking the milestones of language development. Contemp Pediatr.1987;4:24

Coplan J. Normal speech and language devel-opment: an overview. Pediatrics in Review.1995;16:91

Coplan J, Gleason JR. Quantifying languagedevelopment from birth to 3 years usingthe Early Language Milestone Scale. Pediatrics. 1990;86:963

Dobos AE, Dworkin PH, Bernstein BA. Pediatricians’ approaches to developmentalproblems: has the gap been narrowed? J Dev Behav Pediatr. 1994;15:34–38

Dorman C. Microcephaly and intelligence.Dev Med Child Neurol. 1991;33:267–269

Finney JW, Weist MD. Behavioral assessmentof children and adolescents. Pediatr ClinNorth Am. 1992;39:369–379

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242 Pediatrics in Review Vol. 18 No. 7 July 1997

CHILD DEVELOPMENTInfancy

PIR QUIZ1. An infant lies supine on an exami-

nation table with his head in themidline, hands clasped together. Hegrasps an offered throat stick andbrings it to the mouth. There is notransfer from hand to hand. In theprone position the infant lifts hishead to a vertical axis, with thearms extended to raise the trunk.He rolls over from prone to supineand smiles and coos on social con-tact. When the contact is broken,the smile disappears. The develop-mental level of this infant appearsto be closest to:A. 2 months.B. 4 months.C. 6 months.D. 8 months.

2. An infant sits without support onthe examination table, with herback straight. When offered athroat stick, she grasps it and trans-fers it from one hand to the other.When asked to return the throatstick to the examiner’s outstretchedhand, she touches the stick to thehand, but does not release it. A toyis placed before her, and as shereaches for it, a cloth is thrownover the toy. Without hesitation sheremoves the cloth to retrieve thetoy. When a raisin is placed beforeher, she reaches for it, puts herhand on the surface of the tablenext to the raisin, and traps itbetween the thumb and forefinger.Given a little bell, she uses theforefinger to explore the inside ofit. Pulled with both hands to astanding position, she takes a fewhesitant steps as her hands areheld. The developmental level ofthis child appears to be closest to:A. 6 months.B. 9 months.C. 12 months.D. 15 months.

3. An infant sits in a highchair with a tray before him. He is offeredpaper and a crayon and is asked toimitate a scribbling motion, whichhe does. When asked to imitate ahorizontal stroke, he produces avertical stroke. Given a circularblock and a three-place form board(circle, square, triangle), he suc-cessfully inserts the circular blockinto the form board. Shown how to make a tower of three 1-inchcubes, he clumsily makes a towerof two cubes. He ignores the thirdcube. He dumps a raisin out of alittle bottle and reinserts it with dif-ficulty. His mother reports that hewalks alone, that he responds to asimple request to find an object inanother room, and that he has twowords other than “mama,” althoughhe vocalizes with a rich jargon thathas some of the intonations ofspeech. He makes his wants orneeds known by pointing andvocalizing. He points to his nose or eyes on request. The develop-mental level of this child appearsto be closest to:A. 12 months.B. 15 months.C. 18 months.D. 21 months.

4. A child is sitting in a highchair,with a tray in front of her. Givenpaper and crayon and asked toscribble, she does so with gusto.Asked to copy a circle following ademonstration, she produces a cir-cular scribble rather than a closedcircle. She draws a vertical lineupon demonstration. She builds atower of six cubes and completesthe three-piece form board. Hermother reports that she has becomesomewhat self-assertive, with afirm “no,” and a wish to do thingsfor herself. The developmentallevel of this child appears to beclosest to:A. 18 months.B. 21 months.C. 24 months.D. 30 months.

5. In a 2-year-old child, the best indi-cator of future intellectual achieve-ment will be the child’s status in:A. Adaptive behavior.B. Fine motor activity.C. Gross motor activity.D. Language development.