Current perspectives on physical activity and exercise recommendations for children and adolescents...

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doi: 10.2522/ptj.20100294 Originally published online May 5, 2011 2011; 91:1116-1129. PHYS THER. Galloway Anjana N. Bhat, Rebecca J. Landa and James C. (Cole) Disorders Infants, Children, and Adults With Autism Spectrum Current Perspectives on Motor Functioning in http://ptjournal.apta.org/content/91/7/1116 found online at: The online version of this article, along with updated information and services, can be Collections Perspectives Pediatrics: Other Other Diseases or Conditions Motor Development Motor Control and Motor Learning in the following collection(s): This article, along with others on similar topics, appears e-Letters "Responses" in the online version of this article. "Submit a response" in the right-hand menu under or click on here To submit an e-Letter on this article, click E-mail alerts to receive free e-mail alerts here Sign up by guest on August 7, 2014 http://ptjournal.apta.org/ Downloaded from by guest on August 7, 2014 http://ptjournal.apta.org/ Downloaded from

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doi: 10.2522/ptj.20100294Originally published online May 5, 2011

2011; 91:1116-1129.PHYS THER. GallowayAnjana N. Bhat, Rebecca J. Landa and James C. (Cole)DisordersInfants, Children, and Adults With Autism Spectrum Current Perspectives on Motor Functioning in

http://ptjournal.apta.org/content/91/7/1116found online at: The online version of this article, along with updated information and services, can be

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Perspectives     Pediatrics: Other    

Other Diseases or Conditions     Motor Development    

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Current Perspectives on MotorFunctioning in Infants, Children, andAdults With Autism SpectrumDisordersAnjana N. Bhat, Rebecca J. Landa, James C. (Cole) Galloway

Autism spectrum disorders (ASDs) are the most common pediatric diagnoses in theUnited States. In this perspective article, we propose that a diverse set of motorimpairments are present in children and adults with ASDs. Specifically, we willdiscuss evidence related to gross motor, fine motor, postural control, and imitation/praxis impairments. Moreover, we propose that early motor delays within the first 2years of life may contribute to the social impairments of children with ASDs; there-fore, it is important to address motor impairments through timely assessments andeffective interventions. Lastly, we acknowledge the limitations of the evidencecurrently available and suggest clinical implications for motor assessment and inter-ventions in children with ASDs. In terms of assessment, we believe that comprehen-sive motor evaluations are warranted for children with ASDs and infants at risk forASDs. In terms of interventions, there is an urgent need to develop novel embodiedinterventions grounded in movement and motor learning principles for children withautism.

A.N. Bhat, PT, PhD, Physical Ther-apy Program, Department of Kine-siology, Neag School of Educa-tion and Center for EcologicalStudy of Perception and Action,University of Connecticut, 358Mansfield Road, U2101, Storrs,CT 06269 (USA). Address allcorrespondence to Dr Bhat at:[email protected].

R.J. Landa, CCC-SLP, PhD, Ken-nedy Krieger Institute and Depart-ment of Psychiatry and BehavioralSciences, Johns Hopkins Univer-sity, School of Medicine, Balti-more, Maryland.

J.C. Galloway, PT, PhD, InfantBehavior Lab, Department of Phys-ical Therapy, University of Dela-ware, Newark, Delaware.

[Bhat AN, Landa RJ, Galloway JC.Current perspectives on motorfunctioning in infants, children,and adults with autism spectrumdisorders. Phys Ther. 2011;91:1116–1129.]

© 2011 American Physical TherapyAssociation

Perspective

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Autism spectrum disorders(ASDs) are characterized by arange of social and communi-

cation impairments, as well as repet-itive behaviors.1 These disorderscomprise 3 diagnostic subcategoriesbased on number and type of symp-toms: autism, pervasive developmen-tal disorder–not otherwise specified(PDD-NOS), and Asperger syndrome(see Figure and Appendix for detailedsymptomatology).1 Autism and PDD-NOS are distinguished by numberof symptoms as defined by the Diag-nostic and Statistical Manual ofMental Disorders–Text Revision(DSM-IV-TR).1 Asperger syndrome isdefined by the presence of socialimpairment accompanied by repeti-tive and stereotyped patterns ofbehaviors in the absence of cognitiveimpairment or history of languagedelay.1

Although social impairments are thedefining feature of ASDs, motor func-tioning often is abnormal in one ormore ways. This article aims to high-light and support our perspectivethat motor abnormalities seen inindividuals with ASDs, if morewidely recognized, may affect ASDinterventions and eventual outcomes.Specifically, this perspective articlewill focus on 5 major issues: (1)types of motor impairments; (2) acomparison between motor impair-ments in ASDs and other pediatricdiagnoses; (3) a theoretical view-point on how motor impairmentsmay contribute to the social commu-nication impairments of ASDs; (4)clinical and research implications ofthe current evidence, including ourperspective on current motor assess-ments used by clinicians and theliterature on motor interventionsfor individuals with ASDs, as well assuggestions for new interventiondirections based on the availabletheoretical and empirical work; and(5) limitations of the current evi-dence on motor findings and assess-

ments and embodied interventionsfor ASDs.

Autism spectrum disorders, with aprevalence of 1 in 110 children, arethe most common pediatric diagno-ses in the United States, with 36,500new cases per year and a total of730,000 cases.2 They are also one ofthe most costly disabilities, with upto $3.2 million in lifetime costs for anindividual and family and $34.8 bil-lion in societal costs for all familieshaving individuals with ASDs.3 As aresult, there is worldwide researchand clinical interest in understand-ing the progression of ASD-relatedsymptoms during the course ofdevelopment and in creating novelautism interventions to improve out-comes. Given the presence of motorimpairments, physical therapists areincreasingly becoming part of thetreatment team for children withASDs.

Motor Impairments inPeople With ASDsPerformance on StandardizedTests in School-Age Children andAdults With ASDsChildren, adolescents, and adults withASDs display a range of measurablemotor impairments on current stan-dardized motor assessments (Tab. 1).Specifically, children and adults withASDs ranging between 7 and 32years of age have shown poor upper-limb coordination during visuo-motor and manual dexterity tasksand poor lower-limb coordinationduring tasks requiring balance, agil-ity, and speed.4–7 These studies typ-ically quantified performance usingstandardized measures such as theBruininks-Oseretsky Test of MotorProficiency8 or the MovementAssessment Battery for Children.9

Earlier studies reported motor func-tioning in children with ASDs as afunction of their cognitive develop-ment, as assessed by IQ scores. Oneof the first studies demonstratedmore severe motor impairments in

children and adolescents with ASDswith IQ scores below 75 comparedwith those with IQ scores above 75.4

In contrast, some studies identifiedgreater motor impairment in chil-dren with Asperger syndrome thanin those with autism.5–9 Yet, a morerecent and comprehensive, large-sample study showed comparablemotor impairments in children withASDs without any cognitive delays(autism and Asperger syndrome),with both groups performing worsethan peers who were developingtypically on a standardized neuromo-tor examination involving activitiesof gait, balance, and coordination.10

Therefore, we propose a shift in howthe literature reports motor impair-ments in ASDs: prior research pri-marily emphasized motor impair-ments in children with ASDs andcognitive delays, whereas recentstudies have recognized motorimpairments in children withoutcognitive delays as well.

Functional Activities in Childrenand Adults With ASDsUsing motion analyses, individualswith ASDs have been found to dis-play atypical movement patternsduring locomotion, reaching, andaiming.11–15 Earlier reports suggesteda “parkinsonian gait,” characterizedby longer stance duration, shorterstride lengths, lack of a heel-toe pat-tern, and reduced upper-limb move-ment.11 In contrast, recent reportsidentified features of “ataxic gait,”characterized by instability, asobserved in reduced range of motionat the ankle and increased variability

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of stride lengths.12 One report iden-tified differences in reaching andaiming movements between individ-uals diagnosed with autism with IQscores below and above 75.13 Forexample, children with autism wereasked to reach and grasp objects of2 different sizes that were placed at2 different reaching distances. Bothgroups performed well; however,those children with IQs below 75performed slower reaches and begangrasping later in the reach than thosewith IQs above 75.13 A recent analy-sis of aiming coordination of adults

with autism with IQs ranging from65 to 119, however, did not find IQas a predictor of arm movement pat-terns.14 In addition, handwriting ofchildren with ASDs without any cog-nitive delays is worse than that ofage- and IQ-matched children whoare developing typically and signifi-cantly correlated with their overallmotor performance and not IQ lev-els.15 Together, these studies sup-port the notion that motor impair-ments are commonly observed inindividuals with ASDs and cannot

solely be attributed to cognitivedelays.

Early Motor Delays in Infants andToddlers at Risk for ASDsGiven the aforementioned evidencethat motor involvement is presentin older children with ASDs, there isgrowing interest in using measuresof motor development as markersfor early detection in infants (birth–1year of age) and toddlers (1–2 yearsof age) who are more likely todevelop ASDs than the general pop-ulation.16–19 In addition to young

Children and AdultsWith Autism

Prevalence: Fombonne andTidmarsh99 offer a

conservative prevalenceestimate of 10 per 10,000children with ASDs may

develop autism.

Diagnostic criteria:Marked impairment insocial interaction andcommunication and

restricted behaviors andinterests that emerge prior

to 3 years of age.

Children and AdultsWith PDD-NOS

Prevalence: Prevalenceestimates are unknown forPDD-NOS. This categoryis considered a catchall

when 2 other diagnoses are not suggested, so the rest of

the children may fall intothis subcategory.

Diagnostic criteria:Marked impairment insocial interaction andcommunication and

restricted behaviors andinterests. Fewer specificbehavioral features are

required for a diagnosis ofPDD-NOS.

Children and AdultsWith Asperger Syndrome

Prevalence: 2 per 10,000children with ASDs have

Asperger syndrome.99

Diagnostic criteria:Significant impairment in

social interaction andrestricted behaviors andinterests that is typically detected after 3 years of

age. In addition, there areno clinically significant

delays in expressivelanguage or cognitive

development.

Infants and Toddlers With ASDs

Prevalence: 20% of infant siblings ofchildren with ASDs and 0.9% of children

in the general population will develop ASDs.

Symptoms: Verbal and nonverbalcommunication delays and social delaysthat meet diagnostic criteria for ASDs as

early as 14 months of age. Motor delays orabnormalities may be present, but are not

diagnostic.

Broader Autism Phenotype (BAP)

Prevalence: 25%–50% of infant siblings of children with ASDs have BAP symptoms.

Symptoms: Verbal and nonverbal communicationdelays, social delays, motor delays, or unusualsensory interests. These symptoms are neither

severe enough nor present across enoughdevelopmental systems simultaneously

to meet diagnostic criteria for ASDs.

Figure.Prevalence and key diagnostic impairments for the various subcategories of individuals with autism spectrum disorders (ASDs) andearly symptoms in infants at risk for ASDs. PDD-NOS�pervasive developmental disorder–not otherwise specified.

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children formally diagnosed withASDs (termed “infants who laterdeveloped ASDs”), infant siblings ofchildren already diagnosed withASDs16,19,20 are a population of inter-est in studies of early ASD diagnosisand intervention because they are 20times more at risk to develop ASDsthan the general population.19,21 Therisk for siblings of children alreadydiagnosed with ASDs to developASDs was previously reported to be10%21; however, most recently pro-spective studies cite rates of 20%(Figure).16 There is an additional riskof 25% to 50% for developing milderimpairments such as language,social, and sensorimotor delays,which together define a broaderautism phenotype.16,19,20 In contrast,the risk for developing ASDs in thegeneral population is only 0.9%.19

Gross Motor Delays in Infantsand Toddlers at Risk for ASDsEarlier reports on motor impair-ments in infants at risk for ASDs werebased on retrospective data such ashome videos of first-year birthdays

or parent reports.17,18,22–25 Thesereports suggested that infants wholater developed ASDs showed arange of gross motor problems,including delays in motor mile-stones, abnormal muscle tone(velocity-dependent resistance tostretch), abnormal reflexes, and pos-tural asymmetries.17,18,22–25 Theseinfants also showed jitteriness andirritability or reduced motor activity,excessive stereotypical object play,and excessive time looking at nearbyobjects within the first year of life.These infants also had social impair-ments such as reduced eye contact,reduced smiling, and difficultyresponding to name prompts towardthe end of the first year.22–25 Threerecent retrospective studies haveidentified motor delays duringinfancy in children with ASDs.17,24,25

These studies included a comparisongroup of infants with developmentaldelays inclusive of children withglobal developmental delays ofunknown or heterogeneous etiolo-gies.17,24,25 Motor delays, includingthe acquisition of supine, prone, and

sitting skills, in children with ASDswere comparable to or greater thanmotor delays in infants with develop-mental delays.17,24,25 A more detailedretrospective video analysis of supinepostures revealed greater asymme-tries during both static positionsand movements in the infants wholater developed ASDs compared withinfants who were developmentallydelayed and infants who were devel-oping typically.24

Motor delays have also beenobserved in the second and thirdyears of life in young children withASDs. Toward the second year of life,motor delays may include delayedonset of walking.16,25 Observationalgait analysis of retrospective datafrom young children who later devel-oped ASDs identified a lack of heel-toe pattern, a lack of reciprocal armmovements, and a more waddlinggait compared with age-matchedinfants who were developing typi-cally.25 It is important to note thatretrospective video data and parentreports, such as those cited above,

Table 1.Motor Impairments in Children and Adults With Autism and Motor Delays in Infants and Toddlers at Risk for Autism SpectrumDisorders (ASDs)

Motor Impairmentsor Delays

Impairments in School-Aged Children andAdults With ASDs

Delays in Infants at Risk for ASD and inToddlers and Preschoolers With ASDs

Gross motorcoordination

Poor upper-limb and lower-limb coordination,including bilateral coordination and visuomotorcoordination

Gross motor delays in supine, prone, sitting skillsare present in the first year of life. Delayedonset of walking may be present in thesecond year of life. Gross motor delays arealso present in preschoolers recentlydiagnosed with ASDs.

Fine motorcoordination

Poor fine motor coordination such as in performanceon manual dexterity tasks (eg, Purdue PegboardTest)

Reaching and grasping appear to be delayed ininfants at risk for ASDs. Fine motor delayspersist in the second and third years of life.

Motor stereotypies Motor stereotypies are common in older children andadults with ASDs.

Motor stereotypies such as repetitive banging ofobjects or unusual sensory exploration mayappear in the first year of life, but most oftenemerge in the second year of life.

Postural Feedforward and feedback control of posture areaffected in children and adults with ASDs. Overall,deficient postural control persists in adults withASDs.

Delays are evident in postures such as rollingand sitting. There are suggestions of unusualpostures held for brief to long periods ininfants who later developed ASDs.

Imitation and praxis Imitation impairments are present during postural,gestural, and oral imitation. Performance of complexmovement sequences is poor during imitation, onverbal command, and during tool use, suggestinggeneralized dyspraxia not specific to imitation.

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have potential limitations such aslack of standardized methods andrecall bias.19 These limitations canbe overcome in prospective studiesinvolving siblings of children alreadydiagnosed with ASDs or by compar-ing and following the developmentof toddlers recently diagnosed withASDs. Although, few prospectivestudies have described the develop-mental trajectories of motor develop-ment in siblings of children alreadydiagnosed with ASDs, each of thesestudies found that these siblings wholater developed ASDs or languagedelays were likely to exhibit motordelays at 6, 12, 14, and 18 months.16,20

Fine Motor Delays in Infants andToddlers at Risk for ASDsFine motor delays have also beenreported in siblings of childrenalready diagnosed with ASDs and intoddlers diagnosed with ASDs.16,20

For example, a prospective studywith a small sample using the MullenScales of Early Learning26 identifiedfine motor delays as early as 6months of age in siblings of childrenalready diagnosed with ASDs wholater developed language delays.16

Infants who developed ASDs by theend of their second year showedgross and fine motor delays by 14months.16

A well-designed retrospective studywith a large sample also identifiedfine motor delays in infants laterdiagnosed with ASDs.27 These delayswere observed in a range of behav-iors over the first and second years oflife, including reaching, clapping,pointing, playing with blocks andpuzzles, and turning doorknobs.27

Importantly, it was found that thesemanual motor delays in infancy cor-related with speech delays.27 Simi-larly, a prospective study with asmaller sample showed differencesin the onset of rhythmic arm move-ments and babbling in siblings ofchildren already diagnosed withASDs (outcome diagnosis unknown)

compared with age-matched childrenwho were developing typically.28 Spe-cifically, at 9 to 10 months of age,infants who were developing typicallypeaked in both their babbling and thefrequency of rhythmic arm move-ments such as banging. However,such co-occurrence was notobserved in siblings of childrenalready diagnosed with ASDs at thissame age.28

Lastly, toddlers and preschoolersrecently diagnosed with ASDs dis-played significant fine motor delaysthat were comparable to their grossmotor delays, as reflected in the Pea-body Developmental Motor Scales.29

This finding suggests that both fineand gross motor skills are equallyaffected in many children with ASDs.29

Given the link between movementand communication,30 we proposethat these early motor impairmentscontribute to the later developmentof gestural and verbal communica-tion difficulties, a hallmark of ASDs.Therefore, we propose that upondetecting gross and fine motorimpairments during early childhood,language and social developmentshould be screened, and an autism-specific screening is warranted.

Motor Stereotypies in Infantsand Children With ASDsPediatric clinicians commonly assessgross and fine motor milestones. Yet,spontaneous movements, particu-larly those that can occur without aclear external stimulus, may not be astandard area of assessment. Theseinclude repetitive or stereotypicalspontaneous movements such asrocking, arm flapping, or finger flick-ing, which are common in older chil-dren with autism.31 However, chil-dren who are on the autismspectrum and display fewer symp-toms, as in PDD-NOS, show fewerrepetitive behaviors compared withthose with autism.32 Similarly, repet-itive behaviors are less obvious ininfant siblings of children already

diagnosed with ASDs because a widerange of these movements are dis-played by infants who are develop-ing typically.33

Using Thelen’s taxonomy of rhyth-mic leg, arm, and body move-ments,34 one study compared motorstereotypies at 12 and 18 monthsamong siblings of children alreadydiagnosed with ASDs who laterdeveloped ASDs, nondiagnosed sib-lings of children diagnosed withASDs, and toddlers who were devel-oping typically.33 Overall, there wereno differences in frequencies of var-ious limb and body movementsexcept for more arm waving and, insome cases, more “hands to ear” pos-tures in siblings of children diag-nosed with ASDs who later devel-oped ASDs.33 In contrast, toddlerswho later developed autism showedmore atypical hand and finger move-ments and more stereotypical objectplay, such as excessive banging orpreoccupation with spinning objectsor with part of an object, comparedwith toddlers with milder forms ofASDs such as PDD-NOS.35,36

Taken together, we propose thatmotor stereotypies in infants andtoddlers with ASDs are not as obvi-ous in the first year of life, exceptwhen they may be observed for pro-longed durations, and clearly differfrom those of their peers who aredeveloping typically. Consistent ste-reotypic behaviors are more likely toemerge in the second year of life andcould serve as “red flags” for ASDs.

Sensory Processing Deficits inInfants and Children With ASDsSensory modulation disorders (SMDs)are frequently reported in childrenand adults with ASDs and maydirectly affect their motor perfor-mance.37 Sensory modulation dis-orders are defined as difficultiesin regulating and organizing thenature and intensity of behaviors inresponse to specific domains of sen-

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sory input (tactile, olfactory, visual,auditory, proprioceptive, and vestib-ular).38 Three categories of SMDshave been described in young andolder children with ASDs: (1) “under-responsive” or slow to respond tosensory input (eg, failure to respondto name or react to pain), (2) “over-responsive” or exaggerated or pro-longed response to sensory input(eg, covers ears to loud sounds ortroubled by background noise), and(3) “sensation seeking” or cravingsensory input for extended periods(eg, performing stereotypical move-ments such as body rocking and armflapping).18,39,40 These behavioralresponses usually are reported byparents via questionnaires such asthe Short Sensory Profile.41 More-over, the severity of sensory modu-lation impairments appears to directlycorrelate with autism severity, level offunctioning, and severity of socialcommunication impairment.38,42

Recent studies suggest that sensorymodulation impairments of childrenwith ASDs may involve mixed pat-terns of sensory processing, withvarying levels of responsiveness indifferent sensory domains. Specifi-cally, 3 subgroups of sensory modu-lation have been reported in chil-dren with ASDs between 3 and 10years of age: (1) inattention/exces-sive attention, (2) atypical tactile/smell sensitivity, and (3) atypicalmovement sensitivity/low energyand weak motor responses.42 Thesesubgroups appear to include bothunderresponsive and overresponsivecategories of children with ASDswithin specific sensory domains.42

The third subgroup is particularlyimportant to physical therapists.Children with ASDs who have atypi-cal movement sensitivity usually areoverresponsive to proprioceptiveand vestibular input, whereas chil-dren with low energy and weakmotor responses have poor fine andgross motor skills.41,42 Therefore,children who perform poorly on the

movement sensitivity/low energysections of the sensory profile maybe at a greater risk for motor delaysand long-term motor impairments.We propose that both underrespon-siveness and overresponsiveness todifferent sensory inputs may coexistin children with ASDs. Moreover,specific sensory modulation impair-ments may directly affect motorcoordination and postural control ofchildren with ASDs.

Postural Control Impairments inSchool-Age Children and AdultsWith ASDsA few studies have examined pos-tural control of children and adultswith ASDs, and each identified somelevel of postural impairment. Impair-ments in adaptive postural responses(ie, postural muscle activity occur-ring in response to a sensory pertur-bation) to changing sensoryinput43,44 and in anticipatory pos-tural responses (ie, postural muscleactivity occurring prior to a volun-tary movement)45 have been identi-fied in individuals with ASDs. Themost comprehensive study com-pared postural responses of childrenand adults with autism with those ofage- and IQ-matched individuals,aged 5 to 42 years, who were healthyusing a somatosensory and visualperturbation paradigm.44 This cross-sectional study showed that individ-uals with autism who were 12 yearsor older displayed adaptive responsesin postural control, but even theoldest adults did not display levelscomparable to those of individualswho were healthy. In addition, indi-viduals with autism displayed poorpostural stability when somatosen-sory or visual input was removedor altered, which the authors inter-preted as impairments in multimo-dality sensory integration. A studythat quantified anticipatory posturalcontrol showed that older childrenwith autism were delayed in theirresponses and relied more on feed-back rather than feedforward con-

trol during a bimanual, load-liftingtask.45 Collectively, these studiessuggest that children and adultswith autism may have impairmentsof adaptive or feedback-dependentmechanisms as well as anticipatoryor feedforward-dependent mecha-nisms of postural control.

Postural Delays in Infants andToddlers at Risk for ASDsPostural delays are also evident inyoung infants who later developedASDs, as mentioned briefly in theprevious section.23 A recent pro-spective study showed that siblingsof children already diagnosed withASDs spent less time in advancedpostures used in sitting and crawlingand more time in less-advanced pos-tures such as prone play thanage-matched infants who were devel-oping typically.46 Our own data com-paring siblings of children alreadydiagnosed with ASDs and a controlgroup of infants who were develop-ing typically, using the Alberta InfantMotor Scale at 3 and 6 months, sug-gest that siblings of children alreadydiagnosed with ASDs have poorpostural control, as reflected in lackof head holding and rolling at 3months and lack of pivoting and side-prop postures at 6 months.47 Over-all, postural delays and impairmentshave been observed, yet are under-studied in older children and adultswith ASDs as well as infants at riskfor ASDs.

Imitation and Praxis Impairmentsin Children and Adults With ASDsIn the second year of life, motorskills are used in increasingly com-plex ways in socialization and com-munication. Children often learnskills by observing and imitatingadults during interactive games andplay.48 For example, during imita-tion, the child must attend toanother person’s movements andproduce a response that is timedappropriately and spatially correctfor the other person to consider

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the response to be truly reciprocal,coincident, and thus engaging tosustain the interaction. Not surpris-ingly, impairments in imitation dis-tinguish children with ASDs fromother children who are developmen-tally delayed and children who aredeveloping typically as early as 2years of age.49 Moreover, theseimpairments persist into adulthood50

and are connected to later impair-ments. For example, young childrenwith ASDs who had imitation impair-ments went on to have languagedelays in the preschool years.51

Some common imitation impair-ments are impaired orofacial, man-ual, and postural imitation; greaterreversal errors (eg, while copying apalm facing forward, a child withASD places the palm facing towardhis or her body); and body-part-for-tool errors when performing actionson objects.52 An example of a body-part-for-tool error would be where achild uses his or her hand as a tooth-brush versus demonstrating a graspof the toothbrush when asked toshow how he or she uses a tooth-brush. Some authors53 have pro-posed that imitation impairmentsare part of a larger deficit in perform-ing complex movement sequencestermed dyspraxia, which, in turn, isattributed to poor motor planningand sequencing. Taken together, imi-tation impairments in older childrenand adults are considered autism-specific, as they are significant enoughto distinguish individuals with ASDsfrom other groups with developmen-tal delays.

Comparing MotorImpairments Between ASDsand Other PediatricDiagnosesLimitations in daily activities such aslocomotion and reaching could bedue to common motor impairmentssuch as abnormal muscle tone, mus-cle weakness, incoordination during

fine and gross motor activities, poorbalance, and involuntary movementsor to secondary impairments such asmuscle contractures.54 The few stud-ies examining motor impairments inchildren with ASDs suggest the pres-ence of low muscle tone,22 signifi-cant motor incoordination,4–7 poorbalance,4–7,43–45 imitation and praxisimpairments,49–53 and the presenceof motor stereotypies such as armflapping or preoccupation withobjects.32,35,36 There are suggestionsof abnormal movement patternssuch as toe-walking in children withASDs; however, there are no system-atic studies on whether secondarymuscle laxity or contracturesdevelop in children with ASDs.55

Other diagnoses commonly encoun-tered by pediatric physical thera-pists, such as certain forms of cere-bral palsy,56 Down syndrome,57,58

developmental coordination disor-ders (DCDs),59,60 and spina bifida,61

also may be present with the afore-mentioned impairments such astonal abnormalities, incoordination,or balance impairments. In addition,motor stereotypies are observed inchildren with Down syndrome,62

and specific types of involuntarymovements such as choreoathetosisor tremors are observed in childrenwith athetoid and ataxic cerebralpalsy.54 However, some studies63,64

suggest that impaired imitation andpraxis appear to distinguish school-age children with ASDs from age-matched children with attention-deficit/hyperactivity disorder andDCDs.

The issue of motor impairments suchas comorbidity (ie, an impairment inaddition to the primary diagnosticimpairments) often is described invarious psychiatric disorders, includ-ing ASDs, attention-deficit/hyper-activity disorder, behavioral disor-ders such as oppositional defiantdisorder, and anxiety disorders.65–68

Several studies65–68 have demon-

strated significant motor impair-ments in balance and fine and grossmotor coordination, as well as lowlevels of physical fitness, in childrenwith psychopathologies indicativeof common mechanisms of neuro-logical dysfunction. Moreover, thesestudies emphasize the need forassessment and management ofmotor problems in children diag-nosed with psychopathologies.63–68

Although there is some evidencethat imitation and praxis impair-ments may be autism-specific, wepropose that the majority of themotor impairments observed in chil-dren with ASDs also may be seen inchildren with other movement disor-ders and psychiatric disorders. Thus,there is a need to compare motorimpairments among various pediat-ric diagnoses to better understandwhether there is a motor profile spe-cific to autism and to determinewhether novel motor assessmentsneed to be developed. Lastly, motorimpairments are highly prevalent inpediatric psychiatric disorders andmust be addressed in clinical assess-ment and intervention.

Theories and RecentEvidence for Motor-SocialLinks in ASDsTo fully engage in social interaction,an individual requires a full reper-toire of movement behaviors for usein communication and for under-standing the communicative natureof others’ movements. We proposethat understanding the limitationsin the planning and coordination ofmovement and posture is fundamen-tal to a comprehensive understand-ing of the qualitative social impair-ment of ASDs. More specifically,we propose that a developmentallyimportant linkage exists betweenmotor and social communicationimpairments in autism. There isemerging empirical support for sucha linkage. For example, motor delaysat 18 months of age are highly pre-

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dictive of ASDs at 3 years of age intoddlers at risk for ASDs.69 Similarly,better motor performance in 2-year-old children newly diagnosed withASDs significantly correlates withbetter future outcomes at 4 years ofage.70 Together, these empirical find-ings support the link between motorand social communication in autismand provide support for the hopefulhypothesis that enhancing the motorperformance of children with ASDsmay facilitate their future motor andsocial communication development.

How Might Motor ImpairmentsContribute to Social Impairmentsin ASDs?Our proposal that motor and socialimpairments in ASD are linked hasits grounding in an ecological,dynamical systems perspective. Thisperspective emphasizes the multi-factor, cyclic nature of the develop-ment of perception-action-cognitionand the critical role of daily explor-atory interactions of a child and hisor her world.71 A child requires a fullmovement repertoire of functionalactions to engage in social interac-tions. Yet, many children with ASDsexhibit qualitative or quantitativeabnormalities in one or more aspectsof movement detected as early asinfancy. Typical coordination andmobility are critical to begin and con-tinue social interactions throughoutthe day. A child’s poor coordinationand slowed movement are linkedto poor social participation andincreased anxiety during playtimein the preschool and kindergartenyears.72–74 Friendships and socialconnections are made throughshared experiences among childrenduring the several hours of playtime.Viewed this way, it is not surprisingthat motor clumsiness will result inmissed opportunities and reducedengagement with coordinated andagile peers, which, in turn, limitsthe initiation and maintenance offriendships and may contribute todelayed social skills and long-term

social impairments.75–77 Children withmotor disorders such as cerebralpalsy and DCDs have significant dif-ficulties developing social and peerrelationships.75,76 Moreover, difficul-ties with social adjustment in chil-dren are also linked to their emo-tional as well as behavioralproblems.72,75

A more specific example to autism ishow slowed or uncoordinated headand arm movements may limit effec-tive and timely head turning, reach-ing, pointing, giving, and showingthat are key components of initia-tion and response to the social over-tures of others, also known as jointattention.78 It is important to pointout that coordinated movement isrequired to fully perceive the world,so actions are not only enabling chil-dren to perform social communica-tive acts but also improve their abil-ity to receive perceptual informationfrom their surroundings.79 For exam-ple, the emergence of locomotionis a causal factor across a host ofdevelopmental areas, including depthand distance perception and objectperception such as size and shapeconstancy.79,80 Locomotor experi-ences are known to directly facilitatesocial communication behaviorssuch as gestural communication andobject sharing with caregivers.81 Insummary, we propose that basicperceptuo-motor impairments pres-ent in infancy and early childhoodsignificantly contribute to the motorand social communication impair-ments observed in older childrenand adults with autism. We are notproposing that social impairments inautism are solely anchored to motorimpairments. Rather, our proposal isthat early in life, when social engage-ment is first emerging, motor limita-tions may impede social develop-ment. Therefore, early motor delays,in particular, must be addressedthrough motor interventions notjust for enhancing motor develop-

ment, but also for enhancing socialdevelopment.

Implications for CliniciansAssessmentBased on the literature reviewedabove, we propose that comprehen-sive motor evaluations are warrantedfor children with autism, regardlessof age, and for infants at risk forASDs. Children with autism mayhave basic fine and gross motorimpairments or more complex imita-tion and planning impairments.These aspects of development are animportant focus of physical therapyassessments, and physical therapistsoften address such abnormalities intheir intervention practices. Infantsat risk for ASDs may not always havemotor delays within the first year.For example, delayed onset of walk-ing may be the first delayed motormilestone in some toddlers at risk forASDs. Thus, we propose that clini-cians continue to perform follow-upsof infants at risk for ASDs, particu-larly infant siblings of children withASDs, even if motor delays are notobserved within the first year.Infants who have a family history ofASDs and are being evaluated as aresult of parental or professionalconcerns must be closely monitoredto detect and address even minormotor delays, especially if they coex-ist with other minor communicationdelays such as delayed emergence ofbabbling or sensory-perceptualimpairments such as difficulty shift-ing attention or reduced attention tosocial cues. Finally, when a childwith ASD is recommended for earlyintervention, the multisystem natureof autism calls for an interdisciplin-ary team approach wherein educa-tors, psychologists, speech-languagetherapists, occupational therapists,and physical therapists worktogether with families to screen,assess, intervene, and prevent fur-ther progression of autism symp-toms early in life.

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Valid and reliable standardizedmotor assessments that have beenreported in the available literaturepertaining to ASDs include theBruininks-Oseretsky Test of MotorPerformance8 and the MovementAssessment Battery for Children9

(Tab. 2). Imitation and praxis can bemeasured using the Modified FloridaApraxia Battery52 and the SensoryIntegration and Praxis Test.82

Although motor impairments havebeen observed in children with ASDsof all cognitive levels, one clearlimitation of all motor assessmentsis that, in children with cognitiveand language impairments, we areunable to discern whether poormotor performance is reflective ofprimary motor impairment or com-promised by cognitive or languageissues leading to poor comprehen-sion of what was being asked. There-fore, there is a clear need to furtherdevelop observational motor mea-sures during functional activities that

address this limitation. The AutismObservation Schedule for Infants69,83

is the only autism-specific measureavailable to assess motor behaviorsin infants. The Autism ObservationSchedule for Infants is considered areliable measure of early identifica-tion of autism-related abnormalitiesduring the first 2 years of life.83 Over-all, physical therapists have a signif-icant role to play during assessmentof a child with ASD, and there is aneed to further develop comprehen-sive, reliable measures for evaluatingimitation and praxis performanceas well as overall functional perfor-mance of children with ASDs.

TreatmentEven though there is sufficient evi-dence that motor impairments arepresent in infants and children withASDs, we know of no major studiesthat have quantified the effects ofmotor interventions on motor andsocial communication outcomes of

children with autism. Most autisminterventions focus on enhancingthe social, communication, cogni-tive, and preacademic skills of chil-dren with ASDs using contemporaryand traditional applied behavioralanalysis approaches, which, in turn,are based on principles of operantconditioning and learning.84 More-over, these interventions tend to behighly individualized due to signifi-cant variations in impairment acrossthe autism spectrum.84 Our infancywork suggests that associative formsof learning are intact in infants at riskfor ASDs and could be used to facil-itate relevant social and motorbehaviors.85 For example, cause-and-effect play with toys often is usedwith preterm infants86 and has thepotential to facilitate visual, move-ment, verbal, and affective explora-tion in infants at risk for ASDs. Someother approaches, such as FLOOR-TIME87 and sensory integration train-ing, implement some aspects ofmotor intervention88; however,there is no clear evidence to supportthe efficacy of these approaches.84

We propose that motor learningprinciples could be applied to ASDinterventions.54 Intervention ideascan be broadly divided into ideas forpractice, feedback, and types ofmotor skills. In terms of practice, evi-dence suggests that older childrenwith ASDs have the ability to learnsimpler motor skills in a proceduralor implicit manner (ie, using alearning-by-doing approach).89,90 Incontrast, individuals with ASDs mayhave a difficult time learning com-plex, multistep motor skills.91 There-fore, if a child has difficulty improv-ing motor performance despitecontinued practice or repetitions,highly explicit forms of guidancesuch as visual modeling or physicalguidance (ie, hand-on-hand instruc-tion), along with brief verbal expla-nation of each step within the entireactivity, may be helpful. Evidencealso suggests that children with ASDs

Table 2.Reliability and Validity Data on Motor Assessments for Autism Spectrum Disorders(ASDs)

Motor Assessments

For Young and Older Children For Infants and Toddlers

Movement Assessment Battery for ChildrenConcurrent validity with Bruininks-Oseretsky

Test of Motor Proficiency�.76Interrater reliability�.96Test-retest reliability�.77100

Gross and fine motor subtests of MullenScales of Early Learning

Validity�.5 or higherReliability�.65 or higher26

Bruininks-Oseretsky Test of Motor ProficiencyConcurrent validity with Movement

Assessment Battery for Children�.88Reliability�.90100

Alberta Infant Motor ScaleConcurrent validity with Peabody Motor

Developmental Scales, second edition�.9Interrater reliability�.99Test-retest reliability�.99101

Peabody Motor Developmental Scales, second editionConcurrent validity with Bayley Scales of Infant Development: high to very highTest-retest reliability�.73–.89 across subtests102

Autism Observational Schedule for Infants hasa motor control component that predictsASDs at 3 years of age69,83

Interrater reliability�.7–.9Test-retest reliability�.7

Praxis and Imitation Batteries

Modified Florida Apraxia BatteryInterrater reliability�.85–.9552

Sensory Integration and Praxis TestingConcurrent validity�.46–.71 for some subtestsInterrater reliability�moderate to high82

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have difficulty understanding move-ment goals.92 Therefore, it is impor-tant to emphasize the end goalwithin any task (eg, one could pro-vide immediate visual or verbal feed-back when a goal is achieved). Addi-tionally, when goals are achieved,previously defined rewards such asstickers or small toys could beoffered to the child, based on theapplied behavioral analysis approach.

Children with ASDs may have diffi-culty with perceptual processing;therefore, the type of feedback pro-vided may be important when teach-ing motor skills. It is unclearwhether children with ASDs show astrong preference for using visual orproprioceptive feedback.93–95 Recentdata suggest that individuals withASDs have the ability to use bothproprioceptive and visual feedbackto improve their coordinated armmovements; however, they took lon-ger to process visual informationcompared with proprioceptive infor-mation.95 These results suggest thatproprioceptive feedback such asphysically guiding the child throughthe action sequence may better assistin improving motor skills comparedwith visual feedback. However, ifvisual feedback is used, clinicianscan choose to provide models usingclear 2-dimensional visual maps ofthe steps involved or input fromtechnologies such as computerizedvideo feedback.93

We propose that clinicians must cap-italize on the social interactions thatwill occur between themselves andthe children during therapy activitiesto create a rich context for stimulat-ing social engagement. These motoractivities must be developmentallyappropriate and tailored to the func-tional needs of the child and familyto facilitate generalization into dailylife. Based on the variety of motordelays present, motor activities uti-lized in intervention could target finemotor and gross motor skills, bal-

ance skills, imitation skills, posturalskills, and joint action during groupplay with other children, 2 or moreat a time, such as “follow the leader”games. Examples of autism interven-tions that implement principles ofjoint action are music-based inter-ventions such as creative music ther-apy. Although music-based inter-ventions look promising due to theembodied nature of the social inter-actions offered, there currently islimited evidence to support thisapproach.96

A group of researchers at the fore-front of early detection and manage-ment of ASDs comprise the InfantSibling Research Consortium.97 Therecommendations made by the con-sortium confirm the lack of evidencefor autism interventions duringinfancy.97 As clinical researchers,they recommend the use ofcaregiver-facilitated, reciprocal socialplay contexts, particularly infant-initiated social interactions thatrequire the child to actively engagewith the caregiver. They recom-mend facilitating not only the socialcommunication systems but alsothe motor systems.97 Moreover, theyadvocate individualized interventionsbased on the delays observed in theinfant. Toward the end of the firstyear, joint attention and pretend playusing appropriate objects could beencouraged.97

Given these recommendations, wepropose a multisystem approach toautism intervention during infancywherein caregiver handling andinteractions should be used to facili-tate both perceptuo-motor andsocial communication development.Infants at risk for ASDs could receivea variety of social, object-based, orpostural experiences that facilitategeneral and specific movement pat-terns, positive affect, and verbaliza-tions. In the first half year of life,social cues could be providedthrough verbal reinforcement as well

as physical handling of the infant.86

Similarly, object-based cues could beprovided by cause-and-effect toys.86,98

Specifically, parents could encour-age hands and feet reaching by offer-ing objects near the infant’s arms orlegs.

As stated earlier, infants at risk forASDs have intact associative learn-ing, which could be used to facilitateage-appropriate, perceptuo-motorand social communication develop-ment. As infants grow into the sec-ond half of the first year of life, it isimportant to encourage age-appropriate locomotor and objectexploration skills. During object-based interactions, caregivers shouldincorporate triadic contexts whereinrelevant social behaviors such asjoint attention (ie, sharing of objectplay with caregivers) are encour-aged. Postural experiences could beprovided by passively placing oractively moving the child within thepostures that appear to be delayed.Finally, we acknowledge that thevarious treatment ideas proposed inthis section are our perspectives onhow physical therapists could offerembodied, multisystem interventionsthat address both motor and socialcommunication development. Themajority of these ideas are basedeither on basic motor control studiesor treatment studies in other at-riskpopulations or on anecdotal evi-dence from clinicians on successfultreatment strategies for childrenwith ASDs.

Limitations and FutureDirections for ResearchBased on the above theoretical andempirical work, we believe that thecurrent literature has significant lim-itations. First, there is lack of sub-stantial evidence on how motorimpairments are associated withsocial communication impairmentsin children with autism. Althoughwe identified a few studies that linkmotor and social development in

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autism, there is a clear need to fur-ther examine this question. Second,there is limited information on thepattern of onset, progression,nature, and severity of motor impair-ments in ASDs within the first 3 yearsof life. Third, we know little aboutwhether and how motor impair-ments vary in nature and severityacross the different diagnostic sub-categories of ASDs and how they dif-fer from other pediatric diagnoses.Fourth, the lack of evidence on howmotor interventions affect the futuremotor and social communicationfunctions of children and adults withautism is a significant research gap.Together, these questions opennumerous avenues of inquiry forclinical researchers in the physicaltherapy profession.

ConclusionsIn this perspective article, we pro-vide evidence that motor behaviorsare qualitatively and quantitativelydifferent in infants, toddlers, andschool-aged children with ASDscompared with those withoutautism. Significant impairments inmotor coordination, postural con-trol, imitation, and praxis are presentin individuals with ASDs. We alsoprovide evidence that motor delaysare present in infants and toddlerswho later develop ASDs along withrecent findings in infant siblings ofchildren with ASDs. Finally, we pro-vide empirical support for a linkbetween motor and social impair-ments in individuals with ASDs andgeneral and specific implicationsfor physical therapy clinicians andresearchers. Although several studieshave confirmed the presence ofmotor impairments in people withASDs, substantial research focusedon motor functioning in people withASDs is needed. We are hopefulthat future clinical trials to improvemotor functioning may contribute toimproved overall outcomes for chil-dren with this chronic developmen-tal disability.

All authors provided concept/idea/projectdesign and writing. Dr Bhat provided clericalsupport.

This article was submitted September 1, 2010,and was accepted March 7, 2011.

DOI: 10.2522/ptj.20100294

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Appendix.Definitions and Symptoms of Various Categories Under Autism Spectrum Disorders Based on the American PsychiatricAssociation’s Diagnostic and Statistical Manual of Mental Disorders (DSM-IV-TR)1

1. Autism is characterized by the presence of markedly abnormal or impaired development in social interaction andcommunication and a markedly restricted repertoire of activities and interests. The manifestations of this disorderemerge prior to 3 years of age in the domains of social behaviors, communication, or pretend play. The numberand severity of symptom manifestation vary greatly from child to child. Qualitative social impairments mainlyinclude impairments in nonverbal behaviors such as gaze modulation, facial expressions, body postures, andgestures used during social interactions. Failure to develop peer relationships, lack of spontaneous sharing ofinterests and enjoyment, and lack of social or emotional reciprocity are also characteristics of autism. Commu-nication impairments include a delay in or lack of spoken language, impaired ability to initiate or sustain aconversation with others, use of repetitive or idiosyncratic language, and a lack of spontaneous pretend play orimitative play. Restricted repetitive and stereotyped behaviors and interests include atypical preoccupation withone or more stereotyped patterns of interest, inflexible adherence to routines and rituals, stereotypic andrepetitive motor mannerisms, and persistent preoccupation with parts of objects. The entire range of IQ isrepresented in children with autism; therefore, the level of functioning varies from one child to another.

2. Pervasive Developmental Disorder–Not Otherwise Specified (PDD-NOS) is defined by the same characteristicsas those listed above for autism, but is distinguished from autism by having fewer of these symptoms. The IQrange for children with PDD-NOS has not been specified in the Diagnostic and Statistical Manual of MentalDisorders–Text Revision (DSM-IV-TR), so all levels of IQ and functioning may be represented.

3. Asperger syndrome is characterized by a significant and sustained impairment in social interaction and thepresence of restricted, repetitive patterns of behaviors and interests. Although qualitative aspects of communi-cation may be impaired, individuals with Asperger syndrome exhibit no clinically significant delays in acquisitionof expressive language. In addition, there are no clinically significant delays in cognitive development or in thedevelopment of age-appropriate self-help skills or adaptive behaviors in childhood.

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doi: 10.2522/ptj.20100294Originally published online May 5, 2011

2011; 91:1116-1129.PHYS THER. GallowayAnjana N. Bhat, Rebecca J. Landa and James C. (Cole)DisordersInfants, Children, and Adults With Autism Spectrum Current Perspectives on Motor Functioning in

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