Reaching and Grasping in Autism Spectrum Disorder: A Review of Recent Literature.

0.63 MB·English

by  Sacrey, Lori-Ann R.

REVIEWARTICLE
published:23January2014
doi:10.3389/fneur.2014.00006
Reaching and grasping in autism spectrum disorder: a

review of recent literature

Lori-AnnR.Sacrey1*,TamaraGermani1,SusanE.Bryson2,3 andLonnieZwaigenbaum1,4

1DepartmentofPediatrics,UniversityofAlberta,Edmonton,AB,Canada
2DepartmentsofPediatricsandPsychology,DalhousieUniversity,Halifax,NS,Canada

3IWKHealthCentre,Halifax,NS,Canada

4GlenroseRehabilitationHospital,Edmonton,AB,Canada

Editedby: Impairmentsinmotorfunctioning,which,untilrecently,haverarelybeenaprimaryfocusin
RenéeMorris,UniversityofNew autismspectrumdisorder(ASD)research,mayplayakeyroleintheearlyexpressionofbio-
SouthWales,Australia
logicalvulnerabilityandbeassociatedwithkeysocial-communicationdeficits.Thisreview
Reviewedby:
summarizescurrentknowledgeofmotorbehaviorinASD,focusingspecificallyonreaching
RenéeMorris,UniversityofNew
SouthWales,Australia and grasping. Convergent data across the lifespan indicate that impairments to reaching
KatyaKotschet,St.Vincent’sHospital, and grasping emerge early in life, affect the planning and execution of motor programs,
Australia andmaybeimpactedbyadditionalimpairmentstosensorycontrolofmotorbehavior.The
*Correspondence: relationshipbetweenmotorimpairmentsanddiagnosticoutcomeswillbediscussed.
Lori-AnnR.Sacrey,Departmentof
Pediatrics,AutismResearch Keywords: reaching, reach-to-grasp, motor planning, motor execution, movement, autism spectrum disorder,

Centre–E209,Glenrose review

RehabilitationHospital,Universityof
Alberta,10230-111Avenue,
Edmonton,ABT5G0B7,Canada
e-mail:[email protected]

INTRODUCTION as they learn about the physical world (24). The ability to plan,
Autism spectrum disorder (ASD) is a developmental disorder execute,andmonitorongoingmovementisanimportantaspect
characterized by impairments in social communication and the of completing an action toward a goal that is integrated in the
presence of repetitive or restricted behaviors (1).ASD is one of environment(25).Assuch,disturbancesingraspingpatternsmay
themostprevalentformsofdevelopmentaldisabilityinternation- impacthowchildrenplay,explore,usetools,andengagesocially.
ally,with current estimates at 1 in 88 (2,3). In his original case Thisreviewisaimedatprovidingadetailedsummaryofcurrent
series,Kanner (4) describedASD primarily in relation to severe knowledgeofskilleduseofthehandsinASD,focusingspecifically
impairmentinsocial–emotionalandcommunicationabilitybut onreachingandgrasping.
alsocommentedonseveralaspectsofmotordevelopment:motor Systematicsearcheswereperformedinfourcomputerizedbib-
milestones were generally within normal limits and fine motor liographicdatabases(PUBMED,ISIWEBof Science,PsycINFO,
coordinationwas“veryskillful,”althoughsomepatientshadgross ScienceDirect) to identify existing literature on reaching and
motor deficits. However,more recent reports suggest that gross grasping in ASD. The search terms included “reaching” and/or
andfinemotordeficitsareprevalentinASD(5–10)andinclude “grasping” with “autism.” Additional articles of interest were
impairmentsinbasicmotorcontrol(11–13),difficultyperform- locatedinthereferencesectionsofthearticlesfromthesystematic
ing skilled motor gestures (14,15),abnormal patterns of motor search.Tobeincludedinthereview,apaperhadto:(1)examine
learning (16,17),and disturbances in the reach-to-grasp move- handmovementsduringreachingand/orgraspingtasksinchil-
ment(18,19).Todate,thesemotorabnormalitiesarecategorized drenwithASD,(2)includeacomparisongroupoftypicallydevel-
as“associated(asopposedtocore)symptoms”(8)andarethought oping(TD)children(withoutafamilyhistoryofASD),butitcould
tointerferewiththedevelopmentof adaptiveskills(15,20–22). alsoincludeothergroupsforcomparison,suchaschildrenwith
Motorimpairmentsmayhaveprimaryeffectsonachievinginde- other forms of developmental disability (DD), and (3) confirm
pendence in activities of daily living (such as holding a spoon), the ASD diagnosis using a multidisciplinary approach. Twenty-
but also secondary effects on social functioning, by interfering fivearticlesmetinclusioncriteriaandwereincludedinthebody
withchildren’sabilitytoparticipateinage-appropriateactivities ofthereview.Theresultsofthesearcharepresentedbelow;begin-
withpeers(suchasteamsports). ningwithadescriptionofhowmanual-motorbehaviordevelops
Theembodiedtheoryofcognitionpositsthatweshouldcon- inthefirstyearsoflifeininfantsat-riskfor,ordiagnosedwith,ASD.
sidercognitionintermsofitsfunctioninservingadaptivebehavior Theremainderofthereviewisorganizedaroundtheframework
(23).Itfollowsthereforethatcomplexadaptivebehaviors,suchas of amotorepisode;describinghowASDaffectsmotorplanning
those of the hands, should be more closely related to cognitive andmotorexecution,aswellashowASDaffectsongoingmotor
functionsthansimpleadaptivebehaviors,suchasthoseofwalk- adjustment and knowledge across the lifespan (Figure 1). The
ing.Reachingandgraspingisacomplexandfundamentalmotor reviewendswithadiscussionoftheimplicationsofimpairments
activity that serves as a vital mode of exploration for children tomotorbehavior,andhowtheyrelatetodiagnosingASD.
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Sacreyetal. Reviewofreachinginautism
at3and6monthsof age,butmoreimportantly,allHRsiblings
whometcriteriaforacommunicationdelayat18monthsofage
exhibitedamotordelayat3monthsof age.MulliganandWhite
(34)prospectivelyexaminedtherelationshipbetweensensoryand
motorbehaviorsinHRinfants(n=13;meanage12.6months;5
males;4ofthe13werediagnosedwithASDat30monthfollow-
FIGURE1|Frameworkofreview.Amovementisplannedandthen up)andtheirTDpeers(n=12;meanage12.1months;5males)by
executed.Theexecutedmovementismonitored,asonlinecorrectionsaide
ongoingmovementsandofflinecorrectionsaidetheplanningof askinginfantsandcaregiverstoparticipateina10-minplaysession
subsequentmovements. anda5-mineatingsession.Theirbehaviorswerevideo-recorded
andcodedforthepresenceorabsenceofmouthingobjects,object
manipulation,hand to mouth with spoon,and plays with food.
REVIEWFINDINGS HRandTDinfantsshowedasimilarperformanceacrossthetwo
EARLYMOTORDEVELOPMENT sessions,althoughtheHRinfantsmovedaroundlessandmanip-
Theanalysisofearlyobjectmanipulationmayyieldinformation ulatedobjectsintheirhandslessfrequentlythantheTDcontrols.
onatypicaldevelopmentevenbeforetheonsetofmorecoresymp- The relationship between poor motor ability and ASD con-
tomsof ASD.Duringtypicaldevelopment,infantsgraspobjects tinues into childhood. Using Part I (oral-motor assessment) of
andmanipulatethemusingtheiroral,tactile,andvisualsensesto the Kaufman Speech Praxis Test for Children (35),Adams (36)
exploreobjectcharacteristics(26).Thesesensorimotorskillsare compared oral-motor abilities and simple and complex phone-
strongly associated with hand and finger sophistication in later micproductioninchildrenwithASD(n=4;meanage8.5years)
development(27,28).Forexample,aftergraspingablock,infants against a TD control group (n=4; mean age 9.0years). Chil-
willbringittotheirfacetolookatit,willrubtheirfingersalong dren were asked to execute non-speech motor movements (e.g.,
it to feel its texture,and will place it in their mouth to taste it. pucker lips), produce simple phonemes (e.g., vowel-to-vowel
Atypicalobjectexplorationhasbeenreportedforinfantsasyoung movements),and produce complex phonemes (complex conso-
as 12months of age, who are later diagnosed with ASD. Com- nantproduction,polysyllabicsynthesis).ChildrenwithASDwere
pared with TD peers, infants who later received a diagnosis of impairedonperformanceof oralmovements,particularlythose
ASDdemonstratedmorespinningandrotatingofobjects,aswell involvinginthetongueandlips,andtheseimpairmentsimpacted
asunusualvisualexplorationofobjects(29).Retrospectiveparent theirabilitytoperformcomplexphonemicproductionandsound
reportsoforal-andmanual-motorskillsfromprimarycaregivers blending.Inaccordancewiththeseresults,Gernsbacheretal.(30)
ofchildrenwithASD(n=172)andTDchildren(n=44)suggest foundthatperformanceoforal-andmanual-motorbehaviorsin
thatimpairedoral-motorabilities(e.g.,blowingaraspberry,stick- ASDdiffereddependingonlevelofverbalfluency.Minimallyflu-
ingouttongue,andmakinganimalsounds)andmanual-motor ent(n=20;meanage7.4years)andhighlyfluentchildrenwith
abilities(e.g.,grabbingdanglingtoys,blockplay)wereabletodis- ASD(n=20;meanage8.3years)completedPartIoftheKaufman
tinguishASDfromTDchildrenduringinfancyandtoddlerhood SpeechPraxisTestforChildren(35)andwerecodedas“able”or
(withsensitivityat83%andspecificityat93%fororal-motorabili- “unable”tocompletetasksof“controlsaliva,”“protrudetongue,”
tiesandsensitivityat89%andspecificityat86%formanual-motor “producevocalizations,”and“puckerlips,”etc.Overall,themini-
skillsinchildrenlaterdiagnosedwithASD).Surprisingly,correla- mallyfluentchildrenwerelessabletocompleteoral–manualskills
tionalanalysesrevealedthatoral-andmanual-motorabilitiesof thanthehighlyverbalchildren,showingimpairmentontaskssuch
infantswithASDwerebetterabletodistinguishchildrenwithASD as“openmouth,”“spreadlips,”andanytasksinvolvingwiththe
from their TD peers than delays in the prototypical milestones tongue.Resultssuchasthesehighlighttheimportantrelationship
of crawling or responding to name (30).A comparison of ASD betweennon-vocaloralabilitiesandvocalproduction.Anunder-
and DD is necessary to separate the ASD-specific impairments standingoftheseimpairmentsisimportantwhenassessingsocial
from general delay when examining the associations between andcommunicationabilityinHRinfants,aswellasolderchildren
oral-andmanual-motorabilitiesandsocial-communicationout- withASD,asimpairmentsinoral-andmanual-motorabilitycan
comes.Nevertheless,oral-andmanual-motorskillsarenotpurely confoundtheassessmentofbothverbalandnon-verballanguage,
a“motorproblem”andchildrenwithhighverbalskillslikelyhave extendingintotheabilitytoengagesociallywithpeers.Thatsaid,it
bettercomprehensionaswellasexpression,althoughsuchtasks isimportanttoacknowledgethatmanyfactorscontributetocom-
donotrequiremuchverbalinstruction. municationfunctioningotherthanoral–motorskills.Moreover,
Accordingly,severalgroupshaveexaminedwhetheroral,man- difficultiescomprehendinginstructionsmayconfoundassessment
ual,andmotorskillsarerelatedtodiagnosticoutcomesininfantsat ofmotorskillsinchildrenwithASDwhohavereceptivelanguage
high-risk(HR)forASD(forexample,youngersiblingsofachild delays,whichmayneedtobetakenintoaccountininterpreting
with ASD). Bhat et al. (31) examined the relationship between otherfindingssummarizedinthisreview.
early gross motor behavior, as measured by the Alberta Infant
Motor Scale [AIMS; (32)] at 3 and 6months of age, and com- MOTORPLANNING
municationoutcomes,asmeasuredbytheMullenScaleof Early Theanalysisofmotorplanningmayyieldearlyinformationcon-
Learning[MSEL;(33)]at18monthsofageinHR(n=24;12male) cerningimpairmentsincognitiveprocessinginASD(37).Before
andTDinfants(n=24;9male).ComparedtoTDcontrols,HR completing a motor act,such as reaching for a block to build a
siblings displayed the delayed motor performance on the AIMS tower,amotorplanfirstneedstobedeveloped.Motorplanning
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Sacreyetal. Reviewofreachinginautism
involvesthesequenceof motorcommandsthatconvertthecur- ordistanceof thetargettograsp(near/far).Followingillumina-
rentstateofone’sbodyintothedesiredstate.Thus,whenbuilding tion of the target, the ASD participants took longer to respond
a tower, a person must formulate a plan that consists of lifting and complete the movement, and again were more variable in
his/herhand,extendingittowardablock,shapinghis/herdigits responding than the TD controls. When performing the same
tograsptheblock,andthentransportingtheblocktothetableto task, but receiving an invalid precue, Nazarali et al. (40) found
beginconstruction. thatadultswithASD(n=12;meanage26.2years;12male)take
longertoreprogramandcompletetheirmovement(asindicated
Reactiontimetasks by increased reaction and execution times) than their TD peers
Recording reaction time is the simplest way to measure motor (n=12;meanage22.8years;10male).Theeffectwasevenmore
planning,asitprovidesabasicmeasureofthetimetakentoformu- pronouncedforinvalid“hand”cuesthaninvalid“direction”cues.
lateamotorplan.Themajorityofstudiesreportthatparticipants Theseresultsareofparticularimportanceforplanningdeficitsin
withASDtypicallyshowlongerreactiontimesthantheirTDpeers ASD.Thatis,whenpresentedwithaninvalid“hand”precue,addi-
(18,38–41).However,whenpresentedwithsimpletasks,suchas tionalsequencesofmovementsmustbeincludedinthenewplan
drawingalinebetweenthetwotargets,childrenwithASDandTD (i.e.,putdownlefthand,liftrighthand,reachtoleftspace),than
performsimilarly.Dowdetal.(42)investigatedmotorplanning ifpresentedwithaninvalid“direction”cue(i.e.,movelefthandto
andmotorexecutioninyoungchildrenwithASD(N=11;mean leftspaceinsteadofrightspace).ItfollowsthereforethatifASD
age=6.2years)andTDchildren(N=12;meanage=6.6years) isindeedassociatedwithaplanningdeficit,itwouldnotbesur-
usingapoint-to-pointmovementtask,inwhichparticipantswere prisingthattheASDgroupwouldbemoreaffectedthantheirTD
requiredtouseastylustomovebetweentwopointsonadigital peers.Inaccordance,thecomplextaskspresentedaboverequire
screen.Overall,ASDandTDgroupsdidnotdifferonanymeasures multi-levelprocessing;seeingacue,formulatingaplan,andini-
examined, but the ASD group did have more variable reaction tiating a motor response. As such, it is possible that observed
times.Inasimilarexperiment,Papadopoulosetal.(43)presented impairments on such tasks may not be purely related to motor
adolescentswithAsperger’sdisorder(N=20;meanage9.6years), skillsperse,butratherfromanincoordinationbetweencognitive
high-functioningASD(N=19;meanage9.8years),andTDchil- processingandmotoroutput.
dren(N=18;meanage9.8years)withvisualstimulionatablet;
twosmallorlargeyellowcircleswerepositionedonahorizontal Reachandgrasptasks
planefromlefttorightandwereseparatedbyaspaceof12–25cm. ThatindividualswithASDtakelongertorespondtoaninvalidcue
Theparticipantswereaskedtodrawalinebetweenthetwotar- maylendfurtherweighttofindingsfromsequentialmotortasks,
getsasfastandaccuratelyaspossible.Kinematicanalysisshowed whichindicatethatchildrenwithASDmaybelessresponsiveto
that time to complete the movement did not differ between the visualinformationwhenplanningasequentialtask.Usingareach,
threegroups;however,thehigh-functioningASDgrouphadmore grasp,andplaceparadigm,Fabbri-Destroetal.(47)examinedhow
variableend-pointswhencomparedtotheTDgroup,suggesting childrenwithhigh-functioningASD(n=12;meanage=10years)
the lack of a well-formed movement plan following a series of andsexandage-matchedcontrolsexecutemotorplansbymanip-
repetitions.Itisinterestingthatmorevariablereactiontimesare ulatingthesizeofthecontainerintowhichagraspedobjectisto
typicalofchildrenwithAttentionDeficitHyperactivityDisorder beplaced.WhileTDparticipantsadjustthetemporalcharacter-
[ADHD;(44)],andgiventhatasubstantialproportionofchildren istics of the reach and grasp components of the sequence based
withASDalsoshowsignsofADHD(45),itmaybeimportantto on the size of the final placement container,children withASD
determinethespecificityofthefindingofhighvariabilitytoASD didnotalterhowthemovementswereexecuted.Theauthorssug-
(i.e.,examinechildrenwithASDwhodoanddonotshowsigns gested that children with ASD program sequential movements
ofADHD). in independent steps, rather than as a cohesive pattern and do
Whenpresentedwithamorecomplextask,groupdifferences notutilizethevisualfeedbackofend-pointtargetwhenplanning
begintoemergeinrelationtoplanningamovement.Glazebrook theiroverallmovement.Thus,itcouldbearguedthatthedelayed
et al. (46) asked the participants with ASD (n=9; mean age response following the presentation of an invalid cue may not
26.9years) and their TD peers (n=9; mean age 25.1years) to be due to planning deficits per se, but rather an impairment in
move their index finger as quickly as possible to an illuminated registering and responding to visual feedback. Indeed, evidence
circular target after a starting cue. During the trials, the size of from functional imaging of connective networking in the brain
the targets as well as the distance between the targets varied.As suggeststhatindividualswithASDhaveimpairedcommunication
reportedwithsimplertasks,adultswithASDhadmorevariable betweenbrainnetworks,andthusmayhavetroublecoordinating
performance than the TD controls,but they also required more amovementinresponsetoavisualcue(48).
timetoprepareandexecutetheirmovements,andreachedlower Hughes(17)examinedmotorplanninginchildrenwithASD
peak acceleration and velocity than TD controls. In a follow-up byemployingareach-to-grasptaskthatencouragedaparticular
experiment,Glazebrook et al. (38) used a more complex exper- handposture.HughesalsoincludedagroupofchildrenwithDD
imental set-up consisting of a black box with 10 switches, 2 of asacomparisongrouptohelpidentifyASD-specificimpairments
whichservedasastartpositionfortheindexfingerofeachhand. toplanningability.ChildrenwithASD(n=36;12–14years),DD
AdultswithASD(n=18;meanage23.7years;17male)andTD (n=24; 10–12years),and TD (n=28; 3–5years) were asked to
controls (n=18; mean age 20.6years; 12 male) were presented pickuparodthathadoneendpaintedblackandtheotherend
with a valid precue to indicate either hand required (left/right) paintedwhiteandplaceoneofthecoloredendsintooneoftwo
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Sacreyetal. Reviewofreachinginautism
diskssothattherodstoodupright.Byvaryingthestartingposition
ofthebar,itispossibletoencouragetheparticipantstoproduce
anoverhandorunderhandgrip,leadingtoeithercomfortableor
awkwardfinalposturedependingontheirplanningabilities(see
Figure2).Thecriterionforacorrectresponse,andthusappro-
priate motor planning, was an appropriate hand action on the
underhand trials, in which the person begins with an uncom-
fortable grasp to end with a comfortable grasp. There were no
groupdifferencesontheoverhandtrials,whichrequirednospe-
cial planning (grasp horizontal bar and supinate wrist to place
endclosesttopinkyfingerintoring).Fortheunderhand(uncom-
fortable)condition,however,theASDgroupmadefewercorrect
initialposturesthantheDDgroup,andbothgroupstogetherper-
formedmorepoorlythantheTDgroup.Hughes(17)suggested
that performance of theASD group resulted from a fundamen-
taldeficitinmotorplanningleadingtoinabilitytoplanaseries
ofmovementsthatwouldresultinacomfortableend-grasppos-
ture. However,a similar experiment using an end-state comfort
FIGURE2|Experimentaldesignoftheunderhandgraspsusedin
task by van Swieten et al. (49) failed to detect motor planning Hughes(17).(A)Therodandringset-up;(B)exampleofacomfortable
differences between ASD and TD groups. Children with ASD end-stateunderhandgrasp;(C)exampleofanuncomfortableend-state
(n=20;agerange9–14years),developmentalcoordinationdisor- underhandgrasp.Notethattherodispositionedthesameforeachtrial,
der(DCD;n=11;agerange9–13years),andTDpeers(n=44;age onlythecoloroftheendoftherodtobeplacedintheringdiffersbetween
range9–14years)werepresentedwithawoodendowelattached trials[adaptedfromRef.(17)].
to a rotating platform. One end of the dowel was painted red
and the participants were told to place their thumb on the red
end of the dowel as the start position, and rotate their wrist to MOTOREXECUTION
move the dowel 180° to the end position. The children had to Analysesofmotorexecution(thatis,actsofcarryingoutplanned
choosebetweenperformingeithertheminimumamountofrota- movements) provide the opportunity to understand the neuro-
tionorend-statecomfort(on50%ofthetrials,thesecoincided). logical underpinnings of cognitive processing that precede such
Interestingly,theASDandTDgroupsperformedsimilarlyonthe movements. Commands from the motor cortex are sent to the
task,choosingend-statecomfortonapproximately75%oftrials; correspondingnervesandmusclestocarryoutthemotoract.For
however,both groups differed from the DCD group,who more example,after planning to grasp a block with the right hand,a
often chose minimal rotation over end-state comfort (approxi- person must then specify the particular muscle contractions to
mately60%oftrials).Thediscrepancybetweenthefindingsfrom movethelimbinthecorrectdirectionandshapethedigitsappro-
Hughes(17)andvanSwietenetal.(49)maybeduetothecom- priatelyforgrasping.Duetothereciprocalinteractionsbetween
plexity of the plan required to complete the tasks. The Hughes motorcortex,sensoryinput,andmotoroutput,thereareample
(17)taskparametersrequiredtheprocessingof threesequential opportunities for errors to occur when executing a motor plan.
aspects of the reaching motion; that is, participants needed to Here,wereviewmotorexecutioninchildrenwithASD.
choosebetweenanoverhandandunderhandgrasp,lifttheobject,
andeithersupinateorpronatetheirwristtoplacetheobjectina Graspingtasks
hole.Incontrast,thetaskofvanSwietenetal.(49)onlyrequired Using a grasp and place task, Forti et al. (50) found that the
the child to process one aspect of the motion (either supinate movement duration of participants withASD is nearly twice as
orrotatetheirwrist),beggingthequestionofwhetherthemotor long as those of controls. Participants with ASD (n=12; mean
impairmentsseenontheHughes(17)taskmaybeduetoproblems age3.5years;ninemales)andageandsex-matchedTDcontrols
processingmultiplepiecesofinformationtoformulateasuccinct were instructed to transport a rubber ball from a start loca-
motorplan. tion and drop it into a hole,located 30cm away,while wearing
To summarize, analysis of motor planning in ASD has sug- kinematic markers (markers placed on the body that allow the
gestedincreasedvariabilityinmovementonsetandoffset(42,43), online/offline tracking of body segments). In addition to taking
increasedreactiontimetovalidcueing(38,39),delaysinreiniti- longertocompletethemovement,childrenwithASDhadhigher
ating and completing a movement following invalid cueing (38, velocities at movement terminus. Although the ASD group was
40), and impairments when planning a comfortable end-grasp able to accurately transport the ball and drop it into the hole,
posture,depending on the complexity of the plan required (17, every member of theASD group made corrections at least once
49).Whentakentogether,theresultsofmotorplanningliterature after entering the area of the hole, whereas fewer than half the
suggestthatindividualswithASDhavetroubleinformulatinga TD controls made corrections. Interestingly, there were no dif-
motor plan when asked to process multiple pieces of informa- ferencesobservedfortheinitialmovementphases,whichshould
tion(i.e.,complextask),whichmaybecognitivelytaxingandthus reflect motor planning processes. In a related study, Stoit et al.
interfereswithmotoroutput. (51)examinedfeed-forwardmotorcontrolinchildrenwithASD
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Sacreyetal. Reviewofreachinginautism
(n=31; mean age 11.6years) and TD children (n=29; mean age-matched TD controls (n=8; mean age=6.5years for both
age 10.5years) using a precision versus power grasp task. Feed- groups)showed thatEMG activitystarted beforethehand even
forwardmovementsrelyoninternalmodelsforaccuracyanddo grasped the object for the TD group. In contrast,EMG activity
notrequiretheonlineuseofsensoryfeedbackevolvingduringthe inthechildrenwithASDstartedmuchlater,whenthehandwas
action(52).Participantswereseatedbehindatableandpresented bringingthefoodtothemouth.ArecentreportbyPascoloand
with two cylinders, a small cylinder affording precision grasp- Cattarinussi(54)criticallyevaluatedtheresultsofCattaneoetal.
ingandalargecylinderaffordingpowergrasping.Foreachtrial, (53) and failed to replicate their finding of impaired synchro-
participants received a cue, administered by a human hand, to nization between grasping and eating. Pascolo et al. employed
indicate the location (left/right) or grip-type (precision/power) the same methodology as Cattaneo et al. but applied increased
of the target to be grasped (see Figure 3). As in the previous control over the experimental set-up. For example, the supple-
study,movementtimesweresignificantlylongerintheASDgroup, mentary information that accompanied the original article by
although there were no differences in initiation errors or time Cattaneoetal.acknowledgedthatthedistancebetweenthechild
to respond following start cue between the two groups. Using and the food varied across trials and there were extra person-
a similar reach-to-grasp task,Mari et al. (18) report that reach- nel in the room when the experiment was conducted (which
ingandgraspingkinematicsarelargelyuncoupledandexecuted could be distracting). To examine the effect of these limitations
in a successive non-overlapping manner in children with ASD. on mouth activation, Pascolo et al. varied the distance of tar-
Children with ASD and their TD peers (n=20 per group; 7– get (near, far, and comfortable distance) and had the children
13years) grasped wooden blocks of varying sizes and distances reach for food in a quiet room without extra personnel. Pas-
and specific kinematic measures were recorded, including time colo et al. (54) did not find any differences between the per-
to reach peak velocity, deceleration time, as well as the coordi- formance of the ASD group (n=7; mean age=7.3years) and
nation of the reach and grasp components. Because the reach their TD peers (n=12; mean age=7.7years), as both groups
component is controlled by the proximal musculature of the opened their mouth after the food had been grasped. Interest-
shoulder and elbow and the grasp component is controlled by ingly,whenlookingattheeffectof distanceonmouthopening,
distalmusculatureoftheforearmandhand,itispossiblethatthe Pascoloetal.foundthatthefurtherthetargetwasawayfromthe
ASD group might show an impairment of coordination. Over- body, the later the onset of mouth opening. The lack of repli-
all,the children withASD performed the movement quite well, cation between Cattaneo et al. and Pascolo et al. likely relates
anddidnotdifferfromtheirTDpeers.Exploringtheresultsfur- to differences in experimental methodology employed. Pascolo
ther, the performance of the ASD group was contrasted by IQ. et al. carefully controlled for two extraneous influences on the
Anidentified“lowerfunctioning”group(IQrange70–79)showed performanceofchildrenwithandwithoutASD,byhavingthem
evidenceofdesynchronizationbetweenthereachandgraspcom- repeat the same movement numerous times in a quiet setting.
ponents, whereas the identified“higher functioning”group (IQ Cattaneo et al. had children with and without ASD perform a
range80–109)demonstratedacloselyintegratedandoverlapping graspingandeatingmovementinamorenaturalisticsetting,with
movement.TheseresultshighlighttheimportanceofincludingIQ variance in food location and extraneous persons present. The
and/ordevelopmentalmatchedcontrolstodeterminespecificity difference in set-up between these two experiments emphasizes
offindingstoASD. theimportanceoftaskboundarieswhenconsideringexperimen-
Theresultsof Cattaneoetal.(53)alsosupporttheincoordi- tal results. When presented with a quiet environment in which
nationofmotorcomponentsofareaching-to-graspmovementin one movement is repeated, ASD children perform similarly to
ASD.Electromyography(EMG)recordedmuscleactivityrelated TD children. When they are presented with a more naturalistic
tomouthopeningduringaneatingtaskinchildrenwithASDand environment,inwhichvarianceoccursbetweentrials,andextra-
neouspersonnelarepresent,thecognitivesystemofchildrenwith
ASD becomes taxed, resulting in impaired motor performance.
This is in accordance with results from motor planning, which
suggest that motor performance of individuals with ASD simi-
larlybecomeimpairedwhenaskedtoprocessmultiplepiecesof
information(17,38,47).

MOTORCORRECTION
Theanalysisofmotorcorrectionscanprovideinformationonan
individuals’ability to understand and respond to ongoing stim-
uli in the environment. Ongoing adjustment during movement
execution is termed online control. The internal representation
of the movement is compared to the executed movement, and
adjustments to the movement are made based on visual and
proprioceptive feedback (55). For example,when lifting a block
FIGURE3|ExampleofthecueingusedbyStoitetal.(51).(A)Pointing tobuildatower,somatosensoryfeedbackguidestheapplication
cuetoindicatecylindertobegrasped(leftorright);(B)handshapecueto
indicatecylindertobegrasped(precisionorpower). of differential force to blocks made of foam versus those made
ofwood.
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Sacreyetal. Reviewofreachinginautism
Load-liftingtasks and intellectual disability (ID; n=11; mean age 11.6years), as
In a unique experiment, Schmitz et al. (25) investigated motor wellasyounger(n=11;meanage9.1years)andolderTDchil-
adjustment during a bimanual load-lifting task in children with dren(n=11;meanage14.1years)toplaceawoodenblockonto
ASD (n=8; mean age 7.9years, six males) and their TD peers atargetwhileviewingthetargetapparatusthroughaprismlens
(n=16; mean age 6.0years; seven males). Participants wore a thatdisplacedvisionoftheirenvironment.Overall,theASDand
bracelet on their right hand equipped with a strain gage that IDgroupstooklongertoadjusttheirmovementsundertheadap-
supported a platform on which a load could be placed. Motor tationtask,requiringalmostdoubletheamountoftimetoadapt
adjustmentwasmeasuredfromtheangulardisplacementof the to reaching with the prism glasses than both TD groups. Inter-
forearm along the elbow joint, and activity of bicep and tricep estingly,transferofmotoradaptationofthereachinghandtothe
muscleswererecordedusingsurfaceelectrodes.Theresponseof non-adapted (non-reaching) hand was found only for the ASD
thearmwasmeasuredwhentheloadwasremovedbytheexperi- group.Theauthorssuggestthatthetransferofadaptationtothe
menterorbytheparticipants’lefthand.Theresultsindicatedthat non-reaching hand is a clear indication that ASD children rely
themaximalangularamplitudeoftheelbowdidnotdifferbetween onproprioceptive,ratherthanvisualinformationtocompletethe
ASDandTDchildrenineithertheexperimenter-orself-unload target-reachingtask.Itispossiblethatdifficultywithprocessing
conditions,althoughthelatencyforbicepinhibitiontooklonger sequential visual information may account for the ASD partici-
intheASDgroup.ThedelayinbicepresponseoftheASDgroup pants’motorexecutionimpairmentsandconsequentrelianceon
suggestsalackofanticipationoftheunloadingforce,andassuch, proprioceptiveinput.
theyrespondonlyafterreceivingsensoryfeedbackthattheload Other experiments examining motor adaptation have not
hadbeenliftedfromtheplatform. reported differences in adaptation rates between ASD and TD
A recent experiment by David et al. (24) examining motor groups. Gidley Larson et al. (60) had high-functioning ASD
adjustment included a comparison group of children diagnosed (n=20; mean age 10.9years; 17 males) and TD (n=16; mean
withDDtohelpdistinguishbetweenimpairmentsduetogeneral age 10.8years; 11 males) participants complete a ball-throwing
delay versus those that were ASD specific. Grip and load force task at baseline without prisms (pre-adaptation), while wear-
weremeasuredinchildrenwithASD,DD,andTDpeers(n=21 ingprismgoggles(adaptation),andagainwithoutprismglasses
per group; 2–6years) during a grasp and place task. Grip force (post-adaptation). In contrast to the findings of Masterton and
wasmeasuredfromthedigitsonthegraspinghandandloadforce Biederman(59),theASDandTDgroupsshowedsimilaradapta-
wasmeasuredfromtheproximalmusculatureofthereachingarm tionratesandadaptationeffectsonmovementperformance.With
andshoulder.WithintheTDgroup,agewasinverselyrelatedto asub-setof thesameparticipants,GidleyLarsonetal.(60)fur-
grip-to-loadforceonsetlatencyandtimetopeakgripforce;how- therexploredadaptioninASDbyaskingparticipantstograspthe
ever,therewerenosimilarage-relateddecreasesbetweengripand handleofarobottooltomoveacursorontoatarget,whichwas
loadforceforeithertheASDorDDgroups,suggestingthatthe presentedonascreen.Theviewofthehandcontrollingtherobot
impairmentstomotoradjustmentonthistaskreflectamatura- tool was blocked throughout the task. On some of the trials, a
tionaldelay,ratherthananASD-specificdelay.Inanearlierreport, perturbation(forceorvisual)wasgiventoassessforparticipants
Davidetal.(56)examinedgripandloadforceadjustmentsina abilitytoplanalternatestrategies.Allchildrenexhibitedclearindi-
groupofolder,high-functioningchildrenwithASD(n=13;mean cationsof adaptationandreachedsimilarratesof adaptationto
age 11.2years). The adolescents were instructed to lift a target theforceandvisualperturbations,withnosignificantgroupdif-
fromastartpositiononloadcellandplaceitonatargetplatform, ferencesonanyofthemeasures.Thediscrepancyinfindingsmay
approximately6(cid:48)(cid:48) away.Onthistask,theASDgrouphadlonger resultfromthesimpleradaptationtasksinGidleyLarsonetal.(60)
grip-to-loadforceonsetlatencies,greatergripforceatmovement (i.e.,throwingaballandmovingarobottool),comparedtothose
onset,andmorevariableperformancethanTDcontrols.However, of Masterton and Biederman (59),which required the grasping
peakgripforceandtimetopeakgripforcedidnotdifferbetween andplacementofsmallblocks,amorecognitivelytaxingtask.
theASDandTDgroups.ThechildrenwithASDconsistentlydid
not respond until the load was removed, suggesting they were Motorknowledge
unabletouseongoingexperiencetoanticipateupcomingunload The ability to calibrate our body to perform motor actions is
force. referred to as affordance perceptions. When shaping our digits
tograsp,weuseasmallerapertureforablocktobeobtainedwith
Adaptationtasks a pincer grasp and a larger aperture for a block to be obtained
Motor adaptation is the modification of a voluntary movement withapowergraspwhenbuildingourtower.Affordancepercep-
basedonerrorfeedbackbetweenrepeatedtrials(57).Tobeconsid- tion contributes to successful performance of many motor and
ered“adaptation,”themovementmustchangeinrespecttooneor non-verbal social capabilities. For example, when participating
moreparameters(e.g.,forceordirection),thechangemustoccur in team sports,such as badminton,one needs to be able to cal-
gradually(i.e.,overminutestohours),andoncethesechangeshave ibrate his/her body to hit the shuttlecock lightly, compared to
occurred,thepersonmustshow“after-effects”and“de-adapt”the tennis,in which the ball needs to be hit with more force. Being
movementinasimilarmannertoreturnbacktotheoriginalstate abletoadjustone’sbodyallowsforsuccessfulmotorperformance
(58).Tounderstandtheroleofvisualandproprioceptivefeedback onbothtasks.Linkenaugeretal.(61)determinedthatadolescents
inmotoradaptationinchildrenwithASD,MastertonandBieder- withASDpoorlyestimatetheirmotoraffordanceswhenpresented
man(59)trainedchildrenwithASD(n=11;meanage10.4years) with a perceptual-motor integration task. Youth (n=12; mean
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Sacreyetal. Reviewofreachinginautism
age 11.1years; all male) and adults with ASD (n=8; mean age abnormalplaywithtoys(e.g.,spinning,flicking),lesstoyplay,and
22.4years;allmale),andage-andsex-matchedTDcontrolswere atypicallyvisuallyexploreobjects(29,30).Astheygetolder,chil-
askedtoestimatethemaximumextensionof theirreachingarm drenwithASDshowimpairmentsinmotorplanning,including
(i.e.,how far they could reach),as well as maximum digit aper- delays in movement initiation and impairments when planning
ture(i.e.,thelargestfoamblocktheirdigitswereabletograsp). complexsequencesofmovementsresultinginacomfortableend-
Followingtheirestimates,participantscompletedareachdistance graspposture(17,38,42,43),andimpairmentsinmotorexecu-
taskandgraspingtasktodeterminetheirmaximalactualvalues. tion,suchasincreasedmovementduration,end-pointcorrections
TheASDgroupsmadedrasticallylargererrors(17–20%foryouth; atmovementterminus,anddesynchronizationbetweencompo-
14–26%foradults)thantheTDgroups(3–5%foryouth;5–7% nents of a reaching movement (38–40, 50, 53). Impairments to
foradults),suggestingtheyoverestimatedtheirmotoraffordance. onlineandofflinecorrectionsarealsoevident,astheyareunable
These findings raise the possibility that motor deficits in ASD tousebothongoingvisualfeedback,aswellasinformationfrom
couldoriginateintheinabilitytousethemotorsystemtodeter- apreviousmovementtoplansubsequentmovementsmoreeffec-
mineactioncapabilitiesandutilizepriorknowledgeof ourown tively (24,25,56). One might postulate that abnormal toy play,
capabilitiestoaidinplanningandexecutingthetaskathand. includingabnormalsensorycontrol,inveryyounginfantscould
Toexaminetherelationshipbetweenactionunderstandingand interfere with subsequent opportunities for motor learning and
ASD,Cossuetal.(62)presentedhigh-functioningASDchildren mayalsoimpactsocialcommunication.Forexample,ifachildhas
(n=15;meanage8.1years;13males)andtwoTDsamples,one trouble in grasping an object,and continues to stare at it as he
matchedforchronologicalage(meanagewas8.7years)andasec- orshespinstheobjectinhisorherhands[asperRef.(29)],the
ond,foryoungerchronologicalage(meanage4.9years),withthree childinturnmayspendlesstimeshowingtheobjecttoaparent
tasks.Thechildrenwatchedavideoclipandwereaskedtoimitate orfriendandengaginginotherjointattentionbehaviors.
actions (conventional or non-conventional actions on objects), Are motor impairments and cognitive outcomes in ASD
producepantomimesofactions(e.g.,shownatoolandrequired related? Findings linking motor ability to outcomes in individ-
topantomimethecorrectactionofthetool),orunderstandapan- ualswithASDhavebeenreplicatednumerouslyintheliterature
tomimedaction(e.g.,watchanactormimeanactionwithoutan (66–68).Forexample,thetransitiontoindependentsittingisasso-
objectandpointtotheobject“used”inthepantomimedaction). ciated with greater variations in babbling (69), motor delays at
TheauthorsfoundthatthechildrenwithASDweresignificantly 18months of age are highly predictive of a diagnosis of ASD at
worseatimitatingconventionalactionsonobjects,imitatingfin- 3yearsofageinHRtoddlers(70),andbettermotorperformance
ger posturing, and imitating oral–facial gestures than both the innewlydiagnosed2-year-oldswithASDisassociatedwithbetter
youngerandage-matchedcontrols.ThechildrenwithASDper- futureoutcomesat4yearsofage(71).Althoughdelaysinmotor
formedsimilarlytotheyoungercontrolgroupwhenidentifying andcommunicationdevelopmentmayrepresentco-existingbut
tools used in pantomimed actions, but both groups performed relativelyindependentaspectsof theASDphenotype,theremay
worsethantheolderTDgroup.Thesimultaneousimpairmentof be consequences of motor delays that impact on opportunities
actionimitation,production,andcomprehensionofpantomime for developing and practicing social-communication skills. For
actionsuggeststhattheprocessof constructinganactionmotor example,if a child is delayed in sitting,and spends most of his
representationisimpairedinchildrenwithASD.Criticallyhow- or her time on the tummy,then he or she would have less time
ever,isthatlanguageabilitywasnotcontrolledforinthesestudies. withthehandsfreetoengageinreachingandgraspingforobjects,
It has been reported that the ability to imitate familiar gestures showing objects,and requesting objects than an infant who has
(suchasconventionalactionsonobjects)iscorrelatedwithlan- maturedtoasittingposition.Assuch,theonsetofthese“social”
guagecomprehension(63).Withoutcontrollingforlanguageabil- behaviorsmayalsobedelayed.Thisisconsistentwiththefindings
ity,onecannotruleoutthatthelackofimitationmaybetheresult of LibertusandNeedham(72),whofoundthatTDinfantswho
ofreducedcomprehensionofthetaskrequirements(64). engageinactive,self-producedreachingmovementsalsoengage
In summary,individuals withASD appear to be impaired in in spontaneous orienting to faces, whereas infants who engage
boththeonline[i.e.,useofongoingsensoryfeedback;(25)]and in passive toy play (watching others play with objects) showed
offline control of movement [i.e.,using memory from previous less spontaneous orienting to faces. Clearly,there are other fac-
trials;(24,56)],aswellasinestimatingtheirmotorabilities(61). torsthatinfluencesocial-communicationdevelopment,aswellas
That is,they are unable to use both ongoing visual feedback,as examplesofneurologicalconditionsassociatedwithseveremotor
wellasinformationfromapreviousmovement,toplansubsequent impairmentsyetrelativelypreservedsocialskills[e.g.,earlyonset
movementsmoreeffectively[alsonotedbyKhanetal.(65)].These neuromuscular disorders;(73)]. However,there is evidence that
impairmentsmayresultfromdeficitsinthevisualcontrolofmove- motor- and social-communication skills are correlated in ASD,
mentinASD,resultinginanincreasedrelianceonproprioceptive both in the school age years (74) and in infancy (31). More-
feedback to complete movements [as supported by adaptation over, gross and fine motor delays may be among the earliest
transferringtothenon-adaptedhandforASDonly;(59)]. identifiablesignsdistinguishinginfantswithASDfromtheirTD
peers(75–77).
DISCUSSION Impairmentinobjectmanipulationmayalsoimpacthowoth-
There is now robust evidence from early motor development, ers’actionsareunderstood(51,78–81).Evidenceforthiscomes
motor planning and execution,as well as motor correction that fromfindingsthat,duringactionobservation,murhythmdesyn-
movement is impaired in ASD. Very young children display chronization is less evident in ASD. Mu rhythm is a pattern of
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Sacreyetal. Reviewofreachinginautism
electricalactivitythatcomesfromtheareaofthebrainthatcon- Howdomotorimpairmentsrelatetosocialimpairments?Typ-
trolsvoluntarymovement(primarymotorcortex)whenatrest. ically,achildhasafullrepertoireofmovementthatheorshecan
Whenlargenumberofneuronssynchronizeinpreparationfora use to engage in social interactions.With respect to the current
movement, or when viewing an actor making a movement, the review,theabilitytoproperlymanipulateobjectsisimportantfor
mu rhythm is described as“desynchronized”(82). Bernier et al. activitiesofdailyliving(suchasbrushingteeth),engaginginsolo
(83)foundreducedmurhythmdesynchronizationduringmove- playactivities(suchasassemblingapuzzle),andparticipatingin
ment observation in ASD, and reduced desynchronization was teamsports(suchasbaseball).Yet,manychildrenwithASDhave
associatedwithpoorerimitationskills.Similarly,Obermanetal. impairedmotorbehavior,detectableasearlyas3monthsof age
(84) report that, although individuals with ASD exhibit desyn- (31).Beingabletoparticipateinpeerplaywouldrequireachildto
chronization of mu rhythm during voluntary movements, mu respondinatimelymanner(catchaballbeforeithitsyouorthe
desynchronizationisabsentwhenobservinganactorperformthe ground),performskilledmotortasks(hittingaballwithabase-
samemovement.Interestingly,thedegreeof mudesynchroniza- ballbat),engageineyecontact(tounderstandandshowaction
tioninASDissensitivetoleveloffamiliarity,onlyrespondingwhen intention),andrespondtosocialcues(understandingwhenitis
individualscanidentifywiththestimuliinapersonalway(85).The appropriatetostealabase).Manyofthesebehaviorsarethosethat
lackofamudesynchronizationresponsewhenobservinganactor areimpairedbyASD.Notsurprisingly,LearyandHill(20)propose
mayresultfromanimpairedmirrorneuronmechanism(MNM) thatmotorabilitymighthaveasignificantimpactonthecorechar-
inASD(62).Mirrorneuronsareinvolvedinimitationofsimple acteristicsofASD.Theideais,whenapersonisunabletorespond
movements(86),learningofcomplexskills(87),intheperception toanother’sactioninatimelyfashion,he/shewillmissthepositive
ofcommunicativeactions(88),andinthedetectionofbasicaction reinforcementassociatedwithinterpersonalinteractions.Achild’s
intentions(89).Parietalmirrorneuronscodethegoalofbothan experiences throughout development may be drastically altered
executedandobservedmotoract,suchasgraspinganobject,and if,at an early age,he/she is unable to remain involved in social
also code the overall intention of the action, whether the actor interaction,andasaresult,maywithdrawalfromsocialactivities
intendstobringthegraspedobjecttothemouthorplaceitina [reportedinRef.(20)].This“motorcognition”perspectivedoes
container(90–93).DeficitsintheMNMhavebeenreportedduring not imply that social impairments are a direct result of motor
movementexecutionandobservationforchildrenwithASD[Ref. impairments,butratherthatimpairedmovementsmayinterfere
(94,95);seereviewbyRizzolattiandFabbri-Destro(96)].Asmen- withopportunitiesforpositivesocialexperiencesandthus,social
tionedpreviously,Cattaneoetal.(53)employedEMGtorecord learning.Conversely,reducedsocialinteractionopportunitiesmay
muscleactivityrelatedtomouthopeningduringaneatingtaskin alsocontributetopooractionunderstanding.Thus,therelation-
ASD.Whenobservinganactorpickupafooditemandtransportit ship between social and motor competencies/impairments may
tothemouth,EMGincreasesinmouthmuscleswerefoundforthe bereciprocalinASD,ahypothesisthatremainstobeexploredin
TDcontrols,butnotfortheASDgroup.Theseresultssuggestthat futurelongitudinalresearch.
childrenwithASDhaveimpairedmudesynchronizationthatmay Therearecommonmethodologicallimitationspresentinthe
translatetoadysfunctionalMNM.Suchimpairmentsmayimpact literaturereviewedhere.First,manyofthearticleshaverelatively
motorlearningandactionunderstanding,whichmayultimately smallsamplesizes;Adams(36)sampleconsistedofonly4children
leadtomisinterpretationofothers’actions. withASD,Glazebrook et al. (46) recruited only 9 children with
Althoughmirrorneuronsplayanimportantroleinactionexe- ASD,andsamplesizesofindividualswithASDintheotherstudies
cutionandobservation(97,98),theyareunlikelytofullyaccount rangedfromasfewas8(53)toasmanyas36(17).Withthesmall
for the myriad of motor impairments displayed by individuals samplesizesinseveralof thestudies,thereisariskof participa-
withASD.Pathologicalstudiesconsistentlyreportabnormalities tionbiasinoversamplingindividualswithASDwhopresentwith
inbrainregionsknowntomediatemotorfunction,includingthe motor difficulties. Second,there is quite an age range in several
cerebellumandsubcorticalwhitematter(99–106).Thecerebellum oftheexperiments.Thedevelopmentalcourseofmotordevelop-
isoneofthekeystructuresrequiredtoformaccurateinternalmod- mentinindividualswithASDisnotwellunderstood,particularly
elsofmotoracts,makingreciprocalconnectionswithmotorareas whenconsideringthetimespanfromtoddlerhoodtoadulthood.
ofthecortextocarryoutplannedcorrectionsduringmovement Becauseofthis,itisdifficulttocomparetheresultsfromoneage
execution(107,108).Assuch,itislikelythatcerebellarabnormal- group(i.e.,youngchildhood)toanother(i.e.,adulthood).Third,
itiesplayaroleinmovementcorrectionimpairmentsseeninASD, thereisagenerallackinappropriatecontrols.Whendetermining
aswellasimpairmentstoeyemovements[suchasprolongedstar- the ASD-specific deficits in movement,many studies report the
ing;forarecentreviewoftheroleofthecerebelluminASD,see useofTDcontrolonly.However,theresultsofHughes(17)and
Ref.(109)].Inaddition,abnormalconnectivitybetweenadjacent Davidetal.(24)highlighttheimportanceofincludingacontrolfor
primarysensoryandmotorareashasbeenreportedinASD(48, intellectualordevelopmentallevel.Similarly,theresultsof Mari
51),andmayaccountforimpairmentsseenduringtheonlinecon- etal.(18)demonstratetheimportanceofstratifyingintelligence
trolofmovement(110).Moreover,reducedconnectivitybetween wheninterpretingexperimentalresults.Fourth,importantly,the
moredistalareasofthemotorsystem,suchasbetweenvisualand severityofASDsymptomologyvariesacrossthestudiesreviewed
motorregionssub-servingaction,mayberesponsibleforimpair- here,andassuch,thecomparabilityof studyconclusionsmight
mentsinmotorplanningandmotorexecutioninindividualswith be constrained by the methodological limitations present in the
ASD(48,51). literature.

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ThisresearchissupportedbyCIHRandAutismSpeaksCanada. 19.NoterdaemeM,MildenbergerK,MinowF,AmorosaH.Evaluationofneuro-

Lonnie Zwaigenbaum is supported by the Stollery Children’s motordeficitsinchildrenwithautismandchildrenwithaspecificspeechand

languagedisorder.EurChildAdolescPsychiatry(2002)11:219–25.doi:10.1007/
Hospital Foundation Chair in Autism Research and an Alberta
s00787-002-0285-z
Innovates-HealthSolutionsScholarAward.SusanE.Brysonissup-
20.LearyMR,HillDA.Movingon:autismandmovementdisturbance.Ment
portedbytheCraigChairinAutismResearchandtheDalhousie Retard(1996)34:39–53.
Medical Research Foundation. Lori-Ann R. Sacrey and Tamara 21.BaranekGT,ParhamLD,BodfishJT.Sensoryandmotorfeaturesinautism:

Germani are supported by a CIHR Autism Research Training assessmentandintervention.3rded.In:VolkmarF,KlinA,PaulR,editors.

HandbookofAutismandPervasiveDevelopmentalDisorders:Assessment,Inter-
Programaward.
ventions and Policy. (Vol. 2), Hoboken, NJ: John Wiley and Sons (2005).
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