hot topics in autism: cognitive deficits, cognitive...
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HOT TOPICS IN AUTISM: COGNITIVE DEFICITS, COGNITIVESTYLE, AND JOINT ATTENTION DYSFUNCTION
AUtism is characterized by severedeficits in a range of social skillsand behaviors. In many ways it is
possible to think of autism as a sociallearning disability. However, otherdisorders of childhood, especially otherdevelopmental disabilities, also affectsocial development. In addition, thereis a growing consensus that childrenwith autism represent a heterogeneousgroup. Thus, one can view aUtism asa collection of phenotypes, perhapsvarying along a continuum, perhapshaving multiple etiologies withconverging characteristics, or perhapshaving divergent phenotypes fromcommon etiologies. So it is a dauntingtask to identify a narrow range ofcharacteristics that can help physiciansscreen for the disorder.
With these caveats in mind,
several features of aUtism are uniqueto the disorder. They appear to begood indicators of aUtism in early life,and offer insight into both the severityand quality of the social deficits inautism. In this brief paper, I willfocus mainly on one aspect of socialfunctioning in aUtism; namely, deficitsin joint attention. However, I will alsobriefly review other "hot topics" inaUtism research, including deficits insocial cognition (including theory ofmind), executive functions, and central
coherence. Each of these concepts willbe considered in relation to the jointattention deficits seen in autism.
JOINT ATTENTIONThe Normal Case
Joint attention is a family of socialabilities ("social pragmatic abilities")that help individuals regulate, respondto, and engage in social interactionswith others. Of particular interest tothe study of autism are joint attentionbehaviors (JA) that regulate socialinteractions between a child, an
interactive partner, and other aspectsof the environment. These types ofjoint attention events are termed triadic
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STEPHEN J. SHEINKOPF, PHD
social interactions.'
ThroughoUt the first two yearsof life, infants develop increasinglycomplex nonverbal, vocal, and (soonerfor some than others) verbal skills that
can be deployed to meet the demandsof social interactions. There are a
number of different ways to view therepertoire of social pragmatic behaviorsin this early developmental period.Infants may initiate social interactions,or respond to social bids of others.Social-communication episodes mayalso vary with respect to communicativefunction. ( Figure 1) Children mayuse nonverbal behaviors to request anobject oUt of reach, or they may requesthelp with an object. The means to thissocial end may vary, with some actsinvolving pointing, others involvingeye contact, others simply a reach,and some combining a number ofbehaviors. Whatever the form, however,
these behaviors serve as requests, forthey have some instrumental valueand function to elicit aid from a social
partner.Other behaviors coordinate
attention between a child, a social
partner and the environment in orderto share social information. These actsdo not have the same instrumental
function as requests and instead serve asocial-affiliativeor commentingfunction.Indeed, these acts are sometimes termed
"protodeclarative."2 In this paper Icall these acts "joint attention" acts.More specifically, infant-initiated jointattention acts are termed initiatingjoint attention (I}A). The responsiveform of this class of social pragmaticbehavior is termed responding to jointattention (R}A) and reflects the ability
of infants to orient their gaze or focusof attention to that of a social partner,as when an infants looks to where an
adult is pointing.Joint Attention in Autism.
AUtism is characterized by severedeficits in both IJA and RJA.3-5Children with aUtism show deficits
in the frequency and complexity ofjoint attention behaviors, as well asdifferences in the qualitative patternsof strengths and weaknesses in jointattention as related to other social
pragmatic behaviors. Autism ischaracterized by generally poor socialand communication skills. But there is
a particular weakness in IJA and RJAskills. Thus, children with autism show
severe deficits in the frequency withwhich they initiate joint attentionbids (I}A) as well in their ability tomonitor and respond to joint attentionbids of others (RJA). These deficits
contrast with a relative sparing ofrequesting skills.
This is not say that the childrenwith aUtism show completely normaland age-appropriate abilities to requestand to make their needs known.
Indeed, children with autism mayshow deficits in the complexity ofrequests (e.g., failure to use pointingor poor coordination of eye contact,vocalizations, and other communicative
means when making requests). Instead,the pattern of social pragmatic skillsseen in aUtism, particularly in youngchildren with autism, reflects a greaterpropensity to regulate the behaviorof others for instrumental gain and a'diminished tendency and/or ability tocoordinate attention with others forsocial affiliative functions.6
Such patterns of social andcommunicative abilities can be seen
through behavior observation and areevident in parents' descriptions of theirchildren. How do we observe these
behaviors in the laboratory or clinic?In the laboratory, we stage a semi-structured play sessionwhere a clinicianpresents a series of toys and gamesdesigned to elicit requesting and jointattention behaviors.7 The clinician will
present a toy that creates a spectacle, likea wind-up toy. While this toy is active(e.g., moving about, hopping, makingnoises, etc), a typically developinginfant may point, alternate gaze with
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Figure 1: Functional uses of joint attention behaviors
the examiner, smile, and/or vocalize, all
in the service of coordinating attentionbetween themselves, the adult, and
the toy. When the infant touches theobject, s/he may even hold it up toshow it to the adult. These are all bids
of joint attention (specifically, IJA).When the toy stops, the infant may useeye contact to indicate that the adultshould activate the toy again. Morecomplex requests may involve points,eye contact, or even the child givingthe toy to the adult. At other times,the infant may point to an object outof reach to request a new toy. Typicallydeveloping infants display both IJAand requests with some frequency,even in interactions with an unknown
adult in a laboratOry. In contrast,IJA acts are rare for young childrenwith autism, whereas rudimentaryrequesting behaviors would be muchmore likely.
Joint attention deficits are
important to our understandingof autism and to the identification
and diagnosis of the disorder. Thediagnostic criteria for autism (i.e.,ICD-lO and DSM-IV) reveala number
of symptOms that are more or lessreflective of deficits in joint attention.These deficits are among the earliestappearing symptoms8 and are stronglyrepresented in the scoring algorithms ofscreening and diagnostic instruments.9-11Joint attention deficits are related tothe overall severity of symptoms inautisml2 and to cognitive and languagedevelopment in this population.13Clinical experience indicates that thisis a particularly difficult set of abilitiesto remediate through intervention,although recent efforts have targetedjoint attention skills in interventionsfor young children with autism. 14
SOCIAL COGNITIVE DEFICITSIN AUTISM
A large body of literature onTheory of Mind (ToM) probes theability of individuals to reason aboutthe intentions and beliefs of othersY
A seminal paper by Baron-Cohen andcolleaguesl6 reported that individualswith autism were unable to reason
about the false beliefs of protagonistsin a series of vignettes. This deficit hasbeen widely replicated in subsequentresearch. One influential theory arguesthat ToM abilities are rooted in a
discrete information-processing abilitythat allows children to represent thethoughts of others.17
Theoretical links betWeen social
cognition and joint attention includepropositions of JA as a precursor toToM abilitiesl8.19as well propositionsthat JA is an early form or behavioralindicator of ToM. 20.21There is a generalassumption that for children to engagein acts ofJA they must understand thatthe other has a unique point of view.JAand ToM have been argued to recruit acommon cognitive module that lets anindividual represent the thoughts andbeliefs of others,22with JA involving amore basic and rudimentary form ofunderstanding than later developingToM abilities.23Such a view postulatesthat autistic deficits in pretend play, anadditional marker of autism in earlychildhood, also share this requirementfor representational thought.
Despite these theoretical links,there is little empirical evidence for thelink betWeen JA and ToM, in spite ofsome longitudinal links that have beenreported.24
EXECUTIVE FUNCTION DEFI-CITS.
Executive functions (EF) are a
broad classof cognitive abilities involved
in the regulation of thought and action.This class of higher cognitive abilitiessupports such functions as strategicplanning, impulse control, workingmemory, organization of mean-endbehaviors, and flexibility in thoughtand action. The frontal lobes are heavilyinvolved in these processes.25
Deficits in EF are well replicatedin children with autistic disorder. 26-
28 However, research indicates that
autism is related to a specific patternof deficits in executive skills; i.e.,
deficits in planning efficiency andperseverative responses that indicatedifficulties in shifting response set.26.27These patterns have been found todifferentiate the executive performanceof autistic individuals from those with
ADHD and other neurodevelopmentaldisorders. Children with ADHD are
most likely to show deficits in responseinhibition, whereas autistic individualstend not to show evidence of such
dysfunction on EF batteries.26,29An important issue for the EF
deficits in this population is theirdevelopmental course. Ozonoff andcolleagues have reported that deficitsin planning efficiency and set shifting,purportedly related to prefrontalfunctioning, were of greater magnitudefor older than for younger individuals.27This is consistent with the view that
frontal lobes (and EF) are late to mature
and suggests that floor effects maymask the appearance of such deficitsat younger ages.
While EF deficits are most robustlyseen in older and higher functioningindividuals, at least one reportdocuments increased perseverativeresponses on an object search task inpreschool age children with autism.30Thus, it may be that early EF deficitsmay be seen with appropriately sensitivetasks. An interesting trend from the
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Joint Attention
n
SocialSharingI InstrumentalGain SocialGames InformationGatheringIntersubjectivity
Joint Attention Requests Socia/Interaction Socia/ Referencing
studies ofEF skills in younger childrenwith autism is that performancedifferences on EF tasks appear to berelated to earlyJA abilities.30-32In short,there may be a syndrome-specific setof EF deficits in autism, at least some
aspects of which may be related toJA.
CENTRAL COHERENCE
Frith and Happe33 proposedthe concept of central coherence asan addition to the ToM approachin understanding the cognitive styleof individuals with autism. Central
coherence (the tendency to integrateinformation to form a whole, coherent
meaning.) reflects a cognitive style thatallows one to "see the forest for the
trees." The central coherence theory
is intended to help explain aspects ofautistic functioning that are not wellexplained byToM deficits; namely, thetendency to focus on local features ofthe environment.34 In part, this theorywas also intended to help explainwhy individuals with autism performbetter on certain cognitive tasks; e.g.,the embedded figures task, where anindividual is required to identify afigure (e.g., a triangle) embedded in ameaningful picture. A local processingstyle is thought to favor this task and ispredicted to result in faster responses(i.e., shorter latencies to find the
target) .Empirical research on this concept
is limited. Nonetheless, studies have
found evidence for a preference for localversus global processing style in youngchildren with autism (i.e., under age 5years), and examined this construct inrelation to JA skills.34.35There is alsosome evidence that relatives of children
with autism (i.e., parents and siblings)may show a tendency towards thislocal processing style.36 One obviousquestion is whether this processingstyle is related to, or perhaps a differentlevel of explanation of, the executivedysfunctions described above. Verylittle data can be brought to bear onthis question. One study has indicatedthat EF deficits and weak central
coherence may be independent featuresof autism,37but this hypothesis remainsunresolved.
A second question is whetherweak central coherence is related to
the social deficits seen in autism, and
to deficits in JA. It has been suggestedthat weak central coherence limits an
individual's ability to integrate aspectsof the social world into a meaningfulwhole.34.35Some preliminary evidencesuggests a relationship between centralcoherence and ToM abilities in typicallydeveloping and autistic children.34 Inaddition, one report on JA and centralcoherence in children with autism and a
comparison sample with developmentaldelay did not find evidence for a linkbetween joint attention and centralcoherence.35 Although it was not clearthat the JA measure was an appropriatetest of the JA deficit in autism, theseresults raise the hypothesis that weakcentral coherence may be independentof other social and cognitive deficitsseen in autism.
SUMMARYThis review has touched on
selected hot topic issues in autismresearch. There are other excitingdevelopments in the field, includingadvances in neuroimaging and genetics.Such advances notwithstanding,an understanding of the social andcognitive features of autism reviewedhere has great importance. For example,research in our laboratory is focusedon identifying factors that mayunderlie the JA deficit in autism. Abetter understanding of these factorswould improve predictions aboutthe presentation of the disorder inearly infancy, as well as better targetinterventions on pivotal skills andbehaviors.38
In addition to implications forresearch, concepts such as JA, ToM,EF, and central coherence can helphealth care providers develop a fullerpicture of both the strengths andimpairments that characterize autismspectrum disorders. This can helpproviders better understand autism notas a collection of isolated symptoms,but as a description of a populationof children with syndrome-specific
strengths and weakness.
Preparation for this paper was supported
in part by grants from the NationalAlliance for Autism Research and theNational Institutes of Mental Health (JR03 MH072856-01).
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Stephen j. Sheinkopf, PhD, isAssistant Professor of Psychiatry &Human Behavior, Brown MedicalSchool
Correspondence:Stephen Scheinkopf, PhDE.P. Bradley HospitalInfant Development CenterDevelopmental Disabilities Program1011 Veterans Memorial ParkwayEast Providence, RI 02915
phone: (401) 453-7637fax: (401) 432-1500
E-mail: [email protected]