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Articletype:FocusArticle
Articletitle:Guidelinesforstudyingdevelopmentalprosopagnosiainadultsandchildren
Firstauthor:Fullnameandaffiliation;plusemailaddressifcorrespondingauthorKirstenA.Dalrymple*InstituteofChildDevelopment,UniversityofMinnesota,Minneapolis,[email protected]:Fullnameandaffiliation;plusemailaddressifcorrespondingauthorRominaPalermo*SchoolofPsychology,andARCCentreofExcellenceinCognitionanditsDisordersUniversityofWesternAustralia,Crawley,[email protected]
Pleasenotethatbothauthorswouldliketobelistedas“correspondingauthors”.
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Abstract
Developmental prosopagnosia (DP) is a neurodevelopmental condition characterized by severe face
identity recognition problems that results from a failure to develop the mechanisms necessary for
adequate face processing1. It occurs in children and adults with normal visual acuity, and without
intellectualimpairmentsorknownbraininjuries.Giventheimportanceoffacerecognitionindailylife,
and the detrimental effects of impaired face recognition, DP is an important area of study. Yet
conventionsforclassifyingindividualsasDPforresearchpurposesarepoorlydefined.Inthisfocuspaper
wediscuss:1)criteriaforanoperationaldefinitionofDP;2)testsoffacerecognition,andconventions
for classifying individuals asDP; and 3) important considerations regarding common associations and
dissociations, and cognitive heterogeneity in DP. We also highlight issues unique to studying DP in
children,arelativelynewendeavourthat isprovingtobean importantcomplementtotheworkwith
adults. Ultimately we hope to identify challenges researchers face when studying DP, and offer
guidelinesforotherstoconsiderwhenembarkingontheirownresearchpursuitsonthetopic.
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Developmental prosopagnosia (DP) is a neurodevelopmental condition characterized by severe face
identityrecognitiondifficultiesthatoccurwhenfaceprocessingmechanismsfailtoadequatelydevelop1.
DPoccursintheabsenceofbraininjury,inpeoplewithoutintellectualimpairmentandwithotherwise
typicalvision.Sometimesreferredtoascongenitalprosopagnosia[1]3,DPhasbeenestimatedtoaffect2-
2.9%ofthepopulation4,5.FacerecognitiondeficitsinDPcanbeassevereasthosereportedinacquired
prosopagnosia,which results frombraindamage1. Studieson thepsychosocial consequencesofDP in
adultsandchildrenindicatethatDPcanhaveaprofoundimpactonsocialandpsychologicalfunctioning,
creating difficulties making and maintaining relationships, participating in social activities, as well as
increasedlevelsofanxiety6-8.Giventheimportanceoffacerecognitionindailylifeandthedetrimental
effects of DP, it is particularly important to discover what underlies face recognition deficits and, in
doing so, inform potential treatment strategies. Studying DP also has the potential to provide
informationaboutthedevelopmentofhigh-levelvision,andotherdevelopmentaldisorders.
In recent years therehasbeen a surgeof interest in developmental prosopagnosia.A Scopus
search for articles or reviews that make reference to developmental (or congenital) prosopagnosia
reveals216publicationssincetheyear2000,aspecialissueinCognitiveNeuropsychologyin2012,anda
forthcomingspecialissueintheQuarterlyJournalofExperimentalPsychology.Thiscomparestoonly13
publicationsbetween1960and1999.Despitethisinterest,conventionsforclassifyingindividualsasDP
forresearchpurposesarestillpoorlydefined,potentially limitingprogressinunderstandingDP.Inthis
focus paperwewill discuss how to best define DP and how to determinewhether an adult or child
should be classified as DP in research studies. We examine commonly used tests that tap different
aspects of the face recognition process, and discuss which of these seem most suitable for the
measurementofabilitiesinadults,andalsoimportantly,inchildren(seeTable1).Wealsodiscusstests
and questionnaires that measure associated abilities and disabilities (e.g., object processing, autism)
which areuseful indeterminingwhether the childor adult is likely tohaveabroaderdevelopmental
conditionratherthanamore“pure”caseofDP(Table1).Wearguethatitisimportantfortheprogress
of the field to study those with relatively circumscribed face deficits, and also those with broader
deficits,buttobetransparentastowhichindividualsand/orgroupsareincludedinthesample.
[1] “Congenital” prosopagnosia implies that face recognition difficulties were present at birth, while“developmental” prosopagnosia is agnostic as to when in the developmental process the difficultiesemerge. As such, some caseswhere brain injury occurred early in development and resulted in facerecognitiondifficultieshavebeenreferredtoasdevelopmentalprosopagnosia(e.g.,2).However,theseareexcludedfromourdefinition,whichfocusesonthosewithnoknownbraininjury.
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OPERATIONALDEFINITIONOFDP
To develop a coherent body of research on DP, it would be useful to have relatively standard
diagnosticcriteriaacrossstudies.Onecriticalaspectofdefiningadisorderoffacerecognitionisdefining
face recognition itself.Face recognition involvesperceivinga face,encoding it intomemory,and then
subsequentlyretrievingthatmemorytodeterminewhetherthefaceisfamiliarandwhoitmightbe9.An
impairmentoffacerecognitioncouldresultfromafailureofanyoneoftheseprocesses.Therefore,like
other developmental disorders (e.g. autism10), there are likely to be subtypes of DP, rather than one
singleform.Inadults,someindividualswithDPhavenormalfaceperceptiondespitetheirfacememory
deficits11-15.Thismayalsobethecaseforchildren,althougharecentstudysuggeststhatdeficitsinboth
face perception and memory are more common in children than adults12. To accommodate this
heterogeneity,DPisbestdefinedasadeficitoffacememory,withnormalorabnormalfaceperception.
Thereverse,impairedfaceperceptionwithpreservedfacememory,hasbeenreportedintheliterature
onacquiredprosopagnosiaforfacesthatwereseenpriortobraindamage16.However, inDP, itseems
unlikelythatanindividualwhosefaceperceptionhasalwaysbeenimpairedwouldhavetheopportunity
toacquireaccuratefacememories,makingfacememoryandfaceperceptiondifficultdisentangleinDP.
Facememorydeficitscanbemeasuredusingtestsoffacerecognition(seebelow;Table1),but
DPshouldalsobecharacterisedbytheexperienceoffacerecognitiondifficultiesindailylife.Forsome
individualswith DP these experiences include failures identifying very familiar people, such as family
members,whereasotherindividualswithDPprimarilyreportfailuresrecognisingfamiliarbutlessoften
seenpeople,suchasneighbours,whenseenoutofcontext (e.g.,at themall). IndividualswithDPare
also less likely to report a sense of familiarity for unrecognised faces17. However, self-report is
subjective,both in termsof thereportandthe interpretationof thereport,and individualsmayhave
onlyminimalinsightintotheirfacerecognitionabilities18(butsee19).Forexample,failingtorecognizea
familiarpersonoutofcontextisarelativelyubiquitousexperienceandthereisnostandardforwhenan
anecdotalreportcrossesintoevidenceofpathologyinfacerecognition.Furthermore,someindividuals
withDPwereunawarethatthefacerecognitiondifficultiestheyexperiencedwerenotsharedbyothers
until theyparticipated in testing sessions or learnedaboutDP and realized that it explainedmanyof
their lifeexperiences4,20.Unlikeacquiredprosopagnosia, inwhichan individual is typicallyaware that
they have lost an ability they formerly possessed, individuals with DP do not have experience with
normalfacerecognitiontoprovideapointofcomparison1.Children,inparticular,maylackawarenessof
their difficulties hence it is often parents who provide the key anecdotal evidence of their child’s
everyday face difficulties based on observations they have made6. Thus in children, identifying DP
5
requireskeenobservationbyparentsorteachers,combinedwiththeknowledgeofthedisorder,and/or
thetime,resources,andskillsettoresearchthesignsandsymptoms.Recently,severalresearchershave
attempted to improve the assessment of everyday face difficulties by designing self-report
questionnaires.A15-itemquestionnaire19containsquestionsonfaceidentityrecognition,aswellothers
onotheraspectsof faces suchas attractivenessandemotions.Themore recentProsopagnosia Index
(PI20)consistsof20 itemsspecifictoface identityrecognition,andmayproveuseful inscreeningand
standardisingtheassessmentofeverydayfacerecognitionproblems21.Nosuchscalesareyetavailable
forchildren.
We recommend that adefinitionofDP includeobjectivelypoorperformanceon testsof face
memory (just ‘how poor’ is discussed below), along with a subjective feeling of repeated face
recognitionfailuresindailylife.Testsareneededbecauseevenifpeopleknowthattheyarepoorerthan
averageatfacerecognition,theymaynothaveinsightintothedegreeoftheirdeficit18(i.e.,whetherthe
classificationwouldbeasa“poorrecogniser”ratherthanthemoresevereDP).Alternatively,ifaperson
performs at DP levels onmultiples tests of face recognition but reports no everyday difficulties (via
interview and/or questionnaire) then they would seem qualitatively different to people who are
classifiedasDP.Assuch,peoplewhoareidentifiedvialarge-scalescreeningexercisesthatonlyinclude
face recognition tests and nomeasure of subjective difficulty should only be classified as “potential”
DPs.Thereisalsotheinterestingcaseofpeoplewhoreporteverydaydifficultiesbutperformattypical
levelsonmultipletestsoffacerecognition.TheseindividualsaretypicallyexcludedfromDPsamplesbut
itwouldbeinformativetodeterminewhythisoccurs.
An additional definitional factor that is often raised regarding DP is whether the recognition
deficitisspecifictofacesoralsoaffectstheprocessingofotherobjects.Weexpectthatindividualswith
DPwouldbeabletorecogniseobjectsatthe“basic”level(e.g.,bicycle,car,etc.)andthisistypicallythe
case22 when they are asked to name pictures of line drawn objects in the Birmingham Object
RecognitionBattery (BORB)23 (althoughnote that these typesof tests can suffer fromceilingeffects).
However, it is less clear whether they should be proficient at distinguishing similar non-face objects
(e.g., different bicycles). There are cases of “pure”DPwhere the individual does not appear to have
difficulty differentiating between non-face similar objects24-26, and the double dissociation of an
individualabletorecognisefacesbutnotobjects27.However,somepeoplehavedifficultywithfacesand
objects24,28,29.WearguethatthesepeopleshouldstillbeconsideredDP.However, inthesecases it is
importanttodemonstratethatthe individualcanperformnormallyonsomecognitivetaskstoensure
that poor scores cannot be explained by general deficits of cognitive functioning or a failure to
6
understandtaskinstructions,andthattheyhaveadequatevisualacuity(seeTable1forexampletasks).
Thisisparticularlyimportantwhenworkingwithchildren,withwhomattentionandeffortlevelsshould
alsobecarefullymonitored.Moreover,itwouldbeusefulforstudiestotryanddifferentiatethosewith
more face-specific problems from those with more general visual memory impairments, as the
aetiologiesofthesemayvary.
TESTSOFFACERECOGNITION
One difficultywith studying DP is the lack of well-designed clinical tests that can be used to
reliablyevaluatefacerecognition4,20.Togetacompletepictureoffacialidentityrecognitionabilities,it
is importanttousemultiplemeasuresoffacememory.Inaddition,faceperceptiontasksareusefulto
helpqualifythenatureoftheidentityrecognitiondeficits.
Facememory
Assessmentsoffamiliarfacememoryareanobviouschoiceoftaskbecauseoftheirecological
validity.Photosofpersonallyfamiliarindividualsprovidedbyafamilymemberortakenforthepurpose
of the task are ideal, particularlywhen controlled for extra facial cues like hair, jewelry, glasses, and
clothing.Drawbacksofthistypeoftestarethatitcanbedifficulttoacquirealargenumberofcarefully
controlledphotographs,theindividualcanoftendeducewhowillbeincludedinthetest,andthetime
andeffortrequiredtomakecustomizedtestsforeachindividual.Additionally,itisdifficulttocontrolthe
leveloffamiliarity;someimagesmaybeofclosefriendsandfamily,whileothersmaybeofco-workers,
teachers,or acquaintances. Familiar face tasksalso requirea special control groupof individualswho
are similarly familiar with the individuals featured in the test, making it difficult to get an adequate
controlsampletocomparetotheDP’sperformance.
Famousfacesprovideanalternativemethodthatcircumventsmanyoftheseissuesandcanbe
usedformultipleparticipantstoenablecomparisonacrossDPsandwithacontrolgroup.However,the
issueofdegreeoffamiliaritymuststillbetakenintoaccountandparticipantsshouldbetestedlaterwith
thenamesofthecelebritiesinthetasktodeterminewhethertheyhavehadexposuretothefaceofthe
individual and could reasonably be expected to recognize them. Many famous people (especially
politiciansandsportspeople)aretypicallyonlyfamousinoneortwocountries,whichmeansthatthese
facescannotbeusedacrosscountries(althoughthetestformatscanbethesame).Itisalsoimportant
tonote that someDPs report that theyhave little interest in celebritiesorwatchingTVbecause they
find it difficult to recognize faces. These issues are exacerbated when designing tasks for children:
7
finding famous individualswhoare familiar tochildrenofawiderangeofages ischallengingbecause
differentcohortsareoftenexposedtodifferentcelebrities.Anotherissuewithfamousfacetestsisthat
participantsmayperformwellbyusingcompensatorystrategies,suchasidentifyingdistinctivefeatures
(e.g.,abeautyspotonMarilynMonroe),whichmaybemorecommononveryfamousfaces.Asaresult,
apoorscoreisoftenmoreinformativethanahighscore:ifanindividualperformspoorlyatidentifying
thefacesinafamiliarfacetaskdespitedemonstratingfamiliaritywiththeidentitiesinthetestbasedon
names,thisallowsconfidencethatthepersonis impaired.However,ahighscoreonthetaskcouldbe
explainedbyalternativerecognitionstrategies(e.g.memoryfordistinctivetraitsoffamiliarfaces).
Unfamiliar face memory tests can supplement tests of familiar face memory, and provide a
common starting point for all participants because level of familiarity is controlled4. Some existing
clinical tasks for adults such as theWarrington RecognitionMemory for Faces Test (RMF)30 and the
BentonFacialRecognitionTest(BFRT)31havebeenformallyevaluatedanddeemedtobepoormeasures
of true face recognition32,33. Individualswith impaired face recognition candowell on these tasksby
usingextra-face cues (e.g. theRMF includeshair and clothing), or bymatching images (e.g. theBFRT
includesdistinctivehairlinesandusessimultaneouspresentationwithunlimitedresponsetimes).Newer
tasks,suchastheCambridgeFaceMemoryTest(CFMT)34werecarefullydesignedtoreduceextra-face
cuesaswellasother imagecuessuchas lightingandlow-levelvisualproperties. IntheoriginalCFMT,
participantslearnsixfacesofadultmalesandaretestedwithathree-alternativeforcedchoiceformat.
There are three parts that increase in difficulty as the test progresses: the introduction involves
immediaterecallofindividualfaceswhilelatersectionsinvolverecallofanyofthesixtargetfacesand
introduce changes in lighting and viewpoint and finally added visual noise (Figure 1a). Bowles and
colleagues4foundasignificantdeclineinperformanceontheCFMTaftertheageof50,soperformance
onthesetasksshouldbecomparedtoage-matchedcontrols.Alternatively,age-adjustedz-scorescanbe
calculatedfromtheformulascontainedinBowlesetal.4TheCFMTisfreelyavailabletoresearchersand
iscommonlyuseddueto itsvalidityandreliability,whichmakes ituseful inscreeningforDP14,34,35. In
addition,severalversionsexisttoallowfollow-uptestingandtestingofdifferentraces(CFMT-Chinese36)
and ethnicities (CFMT-Australian14). Another advantage of using the CFMT is that there arematched
tests for within-category object recognition – the Cambridge Car Memory Test (CCMT)37 and the
Cambridge Bicycle Memory Test (CBMT)38 (Figure 1b) although note that other tests of object
recognitionareavailablee.g.,TheVanderbiltExpertiseTest(VET)39.
Likealltests,theCFMTdoeshavelimitations.Somepeopleperformpoorlyontestsoffamous
face recognition, but not on the CFMT, perhaps because they have used effective compensatory
8
strategies, leading to an ambiguous classification14, 40. In these cases, administering two different
versionsoftheCFMTcanhelpreachaconsensus13.Somepeoplewillperformpoorlyononeofthetwo
versions,increasingthelikelihoodofacorrectdiagnosisofDP(e.g.,someAustraliansperformpoorlyon
theCFMT-AustralianbutnottheoriginalCFMT,possiblybecausethefacesintheformertestmatchthe
ethnicity of the faces most commonly experienced in Australia and make it more difficult to match
distinctive features)14. Alternatively, others will perform at “poor”, but not DP levels on either test,
excluding a diagnosis of DP14. For some of these cases, the short delays betweenmemorization and
recognition in theCFMTmaymaskdifficulties retaining faces over longdelays (i.e., they shouldhave
difficulty with famous faces but not other tasks)14, 41. The CFMT-Australian includes a 20 min delay
sectionthatmayproveusefulindisambiguatingthesecases13.Asnotedearlier,thefacesusedinCFMT
tasksarecarefullycontrolled,andithasbeenarguedthatthesekindsofexperimentalmanipulationsare
likelytoaltertheprocessingofunfamiliarfacesandthattestsshouldalsobedesignedwithmore“real”
faces (e.g., that includehair)42. It is of interest here to note thatwedesigned a versionof theCFMT
(CFMT-Films)where the study stage involveswatching short film clips of people interacting, and this
correlateshighlywiththeoriginalCFMT17.
Forchildren,somegeneralneuropsychologicalassessmentbatteriesdoincludefacerecognition
subtests43,44,however,liketheRMTandtheBFRT,theyincludesuperficialcuesforrecognition(e.g.,hair
andfacesofmultipleraces)allowingchildrentoinferthecorrectanswersusingextra-facialinformation
ratherthannormalfacerecognitionmechanisms.NewtasksoffacerecognitionsuchastheCambridge
Face Memory Test for Children (CFMT for Children)45 and the Cambridge Face Memory Test – Kids
(CFMT-Kids)20(Figure1c)havebeendesigned.Althoughtheybothfollowthesamegeneralprocedures
astheoriginalCFMTforadults,theCFMTforChildrenusesadultfaces,fivetargets,andtwo-alternative
forcedchoiceformat,whiletheCFMT-Kidsuseschildren’sfaces(meanage=9.3years),sixtargets,and
three-alternativeforcedchoiceformat.Theexistenceofown-agebiasesinrecognition46suggeststhatit
maybepreferabletousechildren’sfacesintestsforchildren.However,giventhatthesebiasesappear
tobedrivenby experience47, the facesof young adultswould alsobe suitable. The advantageof the
formeristhatitiseasierforchildren,buttheadvantageofthelatteristhatchancelevelperformanceis
33%,allowingalargerrangeofscoresabovefloor(i.e.scorestwostandarddeviationsbelowthecontrol
meanyetabovechancearepossible,seeFigure2).Othersimpletestsofunfamiliarfacememoryexist,
such asOld/NewFaces48. This task involvesmemorizing ten target faces and thendeterminingwhich
fromasetoftwoisatargetface(i.e.the“old”face).Thetaskiseasytocreateandquicktoadminister.
Itisalsoeasytocreatematchedtasksusingdifferentclassesofobjects26(e.g.,horses,cars,guns,tools,
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houses,glasses,etc.)thoughoneweaknessofthesetestsisthattheycurrentlyusethesameimagesfor
studyandtest.
Faceperception
TheCambridgeFacePerceptionTest(CFPT)49isausefultoolforassessingfaceperceptionability
inadultparticipants(Figure1d).Itinvolvessortingadultmorphfacesonacontinuumfrommostliketo
leastlikeatarget.Themorphfaceshelpavoiddirectcomparisonormatchingoffeaturesfromthetarget
facetothesortingfaces.Additionally,thetargetfaceispresentedat3/4-profileviewwhilethesorting
facesarepresentedinfrontalviews.AlimitationoftheCFPTisthat itrequiresusingthemousetore-
order thecontinuum,sopoor scorescould reflectpoormotivation to shift the faces ina time-limited
(oneminutepertrial)task.PerformanceontheCFPTdeclinesbymiddleage,andpastyoungadulthood
femalesperformbetter thanmales4.Therefore,both sexandage shouldbe taken intoaccountwhen
administering the CFPT (age- and sex-adjusted z-score calculations for the CFPT are available4). Even
whenusingage-matchedcontrols,standardtaskssuchastheCFPTshouldnotbeusedtoevaluateface
perceptioninindividualsover80becauseofflooreffects4.Forchildren,theDartmouthFacePerception
Test(DFPT)12involvesdecidingwhichofthreechildfaceslooksthemostlikeatargetfacethatremains
at thetopof thescreen(Figure1e).LooselybasedontheCFPT, thetarget face ispresentedata3/4-
profileviewandthechoicefacesarefrontalviewstakenfromamorphcontinuumbetweenthetarget
faceandadistractorface.Themorphstrengthsofthechoicefacesweretitratedtosystematicallyvary
taskdifficulty.
Oneconcernwithfaceperceptionteststhatusemorphsisthatthefacesareunnaturallysimilar
andcontainelementsofthetargetface,reducingtheecologicalvalidityofthetask. Incontrasttothe
CFPT andDFPT, theGlasgowFaceMatching Test (GFMT)50 doesnot usemorphs and thus avoids this
issue. In this task, participants are asked to determine whether face pairs are the same individual
(match), or different individuals (mismatch), with no time limit. Faces are frontal views with neutral
expressions. Matched faces are images of the same individual, taken with different cameras several
minutes apart.Mismatched face pairs were chosen based on similaritymeasures generated through
pilotwork.Inadditiontoretainingecologicalvaliditythatmaybeabsentintasksthatusemorphs,one
advantageoftheGFMTisthatitprovidesaformatthatcouldbeeasilymatchedtoanobject-matching
task(tasksinvolvingmorphsaremoredifficulttoconstructusingobjects,thoughithasbeendone51).
Specialconsiderationsforthedesignoftasksforchildren
10
One major challenge for designing face recognition tasks for children is achieving a level of
difficulty thatwill be suitable for all ages: above floor for young children, but below ceiling for older
children.These issuesaremorepronouncedfor testsof facememorybecauseunlike faceperception,
whichdevelopsatthesamerateasperceptionforotherobjects,facememoryappearstodevelopmore
slowlythanmemoryforotherobjects51.Thisdifferencemakesitdifficulttodesignmatchedtestsofface
andobjectmemory thatwill helpevaluate face-specificity: anobjectmemory task that ismatched in
difficultytoafacememorytaskforolderchildrenmaybepoorlymatchedforyoungerchildrenandvice
versa.However,creatingmultipleversionsofatask,forexampleaneasierversionofthefacememory
taskforyoungerchildren,leadstootherdifficulties:1)determiningwhichtaskshouldbeadministered
toanindividualwhoisatanintermediateage,ordeterminingafixedagerangeforeachtest;2)trying
toestablishadevelopmental trajectory for the task (i.e. comparingkidsacrossawide rangeofages);
and3)comparinganindividualchild’sscoreovertime:iftheindividualwasoriginallyevaluatedonatest
foryoungerchildren,whichtestshouldbeadministeredwhenthechildhasagedoutsidethecut-offfor
the original test? Amove to amore difficult test couldmask improvement, yet re-administering the
originaltestforyoungchildrencouldleadtoinflatedscores.
We have been confronted with the above difficulties when designing our tests of face and
objectprocessingforchildren.Wehavedesignedmultipletestsoffacememory(CFMT-Kids20,Old/New
Faces),matchedobjectmemorytasks(CBMT38,Old/NewFlowers12),andatestoffaceperception12(see
Table1).TheCFMT-Kids20seemstobeausefultoolforassessingfacememoryinchildren10andabove,
butsuffers fromflooreffects inyoungerchildren.Wedesignedanewversionof thetask foryounger
childrenbyreducingthenumberoftargetsfromsixtofour,but it isstillclosetofloor inyoungerage
groups. To address this difficulty,we designed a CFMT-style test that involves immediate recall only.
Althoughthisnewtestimprovesscoresacrosstheboard,itleadstoceilingeffectsinolderchildrenand
doesnotevaluatetheabilitytomaintainmultipleidentitiesinmemoryatonetime(Figure2).
Incontrasttothefacememorytasks,ourothertasks,suchastheDartmouthFacePerception
Test (DFPT)12,havebeenuseful fortestingchildrenbetweentheagesof7to12years.Controlmeans
areareasonabledistancefromfloorandceiling,andstandarddeviationsaresmallenoughthatthetask
maybeusefulforalargeragerange.Asaresult,wehavebeenplacingparticularemphasisonimpaired
face perception, combined with poor face memory scores and evidence of difficulties with face
recognitionindailylife,whenidentifyingprosopagnosiainyoungchildren6.
STATISTICALGUIDELINES
11
One popular criterion for neuropsychological impairment is a score that fallsmore than two
standarddeviationsbelowthemeanforage-matchedcontrols34.Intermsoffacerecognition,scoreson
the CFMT and CFPT that are greater than two standard deviations below the control mean tend to
correspondwithclinicallysignificantcomplaintsof facerecognitiondifficulties4,52.While twostandard
deviationsbelowthemeanisausefulguideline,statisticaltechniqueshavebeendevelopedtoformally
testtheprobabilitythatasingle individual’sscore istakenfromthecontrolgroup53. If the individual’s
scoreisstatisticallyunlikelytocomefromthegroup(i.e.p<0.05),theindividualisconsideredimpaired
for the ability that is being measured. Software to perform these calculations using the group size,
mean, standard deviation, and individual’s test score can be downloaded for free (SINGLIMS)54,55. To
corroborate case-by-case diagnoses of DP, we suggest reporting whether scores fall more than two
standard deviations below themean andwhether theymeet statistical significance12,56. Similarly,we
suggestusingbothstatisticalmethodswhenreportingperformanceonother tasks (e.g.objects, facial
expression,gender).
As discussed above, identifying cases of DP in children can be particularly challenging due to
floor effects. Children produce variable results both between subjects, and even trial-to-trial within
subjects57,58. If thecontrolmeanonagiventask is lowandthestandarddeviation ishigh, itbecomes
difficult to detect a score that ismore than two standard deviations below themean (see Figure 2).
These factors similarly affect the outcome of statistical tests. It is difficult to advise how to classify
children who are on the cusp or who have ambiguous results, but it is recommended that case
descriptionsprovideasmuchinformationaspossibletojustifyinclusionorexclusionofaparticularcase
from theDP group.A combinationof anecdotal reports of failures of face recognition in daily life, in
addition to multiple test scores of face memory and face perception compared to a two standard
deviationfromthemeancut-offandformalstatisticalanalysessuchastheCrawford,Garthwaite,and
Howell53modifiedstatisticsisappropriate.Thesestatisticaltestscanbeusedtotestforadeficitonone
test relative to a control group (SINGLIMS)54 55 or for dissociations in performance on two tests
(DiffBayes_ES_CP.EXE software)59-61. Ideally, when drawing conclusions with regards to a given
hypothesis,somecaseswillprovideclearresults.However,casesthataremoreambiguousshouldalso
beincludedtopresentamorecompletepictureofthebehaviorsbeingstudied.
ASSOCIATIONSANDDISSOCIATIONS
Formostresearchstudies,theidealparticipantswouldhavepureprosopagnosia(i.e.difficulties
withfacialidentityrecognitionalone).However,researchersdonotappeartoroutinelyreportwhether
12
the people in their DP sample show impairments with other aspects of face processing, such as
expressionorgenderrecognition.Wesuggestthatthismightbeduetothetime-consumingnatureof
administering a battery of tests to examine various aspects of face processing (e.g., expressions, eye
gaze, gender, sex etc.), coupled with a paucity of brief, widely accepted, reliable tests to diagnose
deficitsintheseprocesses.
Similarly,therearecurrentlynoformallyestablishedexclusioncriteriaforindividualswhoshow
impairmentsdistinguishingbetweennon-faceobjects.Moreover,somehavesuggestedthatpurelyface-
specificdeficitscannotoccurandthatallprosopagnosicsmusthavecorresponding,thoughoftenmilder,
recognitiondeficits, suchasobject agnosiaorwordagnosia, that canbe revealed through theuseof
carefullydesigned tasks62,63.Althoughcomorbidobjectprocessingdeficits are common24,28, thereare
individualswhoonlyhavedifficultywithfaces24,26.Navigationaldifficultiesmayalsobeassociatedwith
DP, with approximately 15% of adults in the faceblind.org database reporting severe navigational
difficulties64,althoughitisnotyetknownwhetherthisratewouldbehigherthanthatreportedbythe
general population. These comorbiditiesmaybeexplainedby theproximitybetween face,place, and
object processing areas in the brain64. At least for objects, tests are available to enable comparisons
between face and object processing abilities (see Table 1) andwe recommend that researchers note
whetherthosetheyclassifyasDPappeartohaveface-selectiveormorewidespreaddeficits.
Faceidentityrecognitiondeficitsalsoexistinotherdevelopmentaldisorders,suchasautism65-68
andTurner syndrome69,but face recognitiondeficits cananddoexist in individualswhohavenormal
socialfunctioning67.Itisunclearatthispointwhetherthefacerecognitiondeficitsthataccompanyother
developmental disorders should be classified as DP, but given themuch broader cognitive effects in
disorders like autism spectrumdisorders (ASD), it is possible that face recognitiondeficits outsideDP
maybequalitativelydifferent(see70forexample).Thusitisadvisabletoexcludeindividualswithsocial
developmentaldisordersfromstudiesofDP,unlesstheyareaparticularpopulationofinterest.
When working with children with no formal diagnosis of autism, we recommend including
measuresofautistictendenciestoconfirmthatthechilddoesnothaveautism.TheAutismDiagnostic
ObservationSchedule(ADOS)71isonecomponentofthegoldstandardassessmentbatteryforASD,but
trained personnel must administer it, and research reliability is difficult to achieve. It is also time
consuming to administer (30minutes to > 1 hour, plus scoring), and additional assessments are still
required for diagnosis. Alternative, more practical, measures for researchers are parent report
questionnairessuchastheSocialResponsivenessScale–2(SRS-2)72andtheRepetitiveBehaviorScale–
Revised73. While these questionnaires are not sufficient for diagnosing ASD, they can be used as
13
guidelinessuchthatindividualswithhighscores(indicatingautistictendencies)canbefurthertestedor
excluded from the study as a precaution. The Autism Quotient (AQ)74, 75 is commonly used among
researchers as a quick assessment of autistic tendencies, but parents complain that the items are
antiquated (e.g. “S/he isnotverygoodat rememberingphonenumbers.”)andmay thereforebe less
current than the SRS-2 and the RBS-R. For adults, some previous studies15 have tended to exclude
individualswhoscored32oraboveon theAQ,whichwasa range indicativeofapossibleASD74.One
drawbackofusingtheAQwithDPs is that it includesquestionsrelatedto facerecognitionabilityand
relatedsocialinteractionandcouldthereforeresultininflatedscores(e.g.,“WhenI’mreadingastory,I
caneasilyimaginewhatthecharactersmightlooklike”,“Ifindsocialsituationseasy”,“Ienjoymeeting
newpeople”).Additionally,wenotethattheAQisdesignedtobedescriptiveratherthandiagnosticand
thatthereareupdatedmeanAQscoresfortypicalandASDpopulations76.Otherquestionnairesarealso
availabletomeasureautistictraitsinadults(see77foracomparison).
In terms of strictly visual comorbidities, we have noticed a recent increase in the number of
children requesting assessment for face recognition deficits who already have a diagnosis of Cortical
Visual Impairment(CVI).CVI isdefinedasvisual impairmentaffectingbothvisualfieldsdespitenormal
oculomotor systems. It can be related to abnormal development of the visual cortex78, 79 due to
congenitalbrainmalformation78,withthelocationandextentofthecorticalabnormalitiesdetermining
thefunctionaloutcomes80.SomeindividualswithCVIhaveprosopagnosia80makingitanopenquestion
whether a diagnosis of CVI, in some cases,would be better classified as DP, orwhether some or all
individualswithDPmayhaveadditionalsymptomsthatwouldqualifyforadiagnosisofCVI.
Another consideration when identifying DP is whether the individual had early visual
disturbancessuchascongenitalcataracts,amblyopiaorstrabismus.Thereisevidencethatnormalvisual
experiencewithfacesfromanearlyage iscritical forthedevelopmentofnormalfacerecognition81-85.
Forexample,some individualswhohadcongenitalcataractshave long-lasting faceprocessingdeficits,
evenifthecataractswereremovedatanearlyage(e.g.withinthefirst8monthsof life)andacuity is
restored to normal81-83, 86. This is especially true for individuals with bilateral or left eye cataracts84,
possibly because in infancy information from the left eye projects almost exclusively to the right
hemisphere87, which is thought to be particularly important for face processing88-91. Thus one issue
concernswhether an individualwith face recognitiondeficitswhohad congenital cataracts shouldbe
excludedfromresearchonDP.
Onemight predict that early amblyopia, a conditionwhere the vision in one eye is reduced,
could similarly affect face processing and could therefore raise similar flags for participant inclusion.
14
However,atpresentthere isnoempiricalevidencethatfacerecognitiondeficitsaremorecommonin
individuals with amblyopia than the general public. While some researchers might advocate for
excludingthesecases,iflow-levelvisionisnormalorcorrected-to-normal,andtheintricaciesofthecase
are described in detail, cases with suspected aetiologies may help elucidate the developmental
processesleadingtoDP.ThesecasesmayalsorepresentaninterestingsampletocomparetoDPswith
nohistoryofissueswithlow-levelvision.
COGNITIVEHETEROGENEITY
Different phenotypes ofDPhavebeen identified in adults: some individualswithDP are only
impairedwithfacialidentityrecognition15,56,92-94,whileothersmayhaveproblemswithfacedetection56,
94, expression recognition26, or gender discrimination26. These dissociations can provide information
about which abilities are mediated by distinct neural mechanisms. Addressing heterogeneity,
associations, and dissociations in children with DP is particularly important: dissociations between
different types of face processing abilities in children with DP can provide clues as to when in
development theseabilitiesbegin to relyon separatemechanisms. Identifyingandunderstanding the
different subtypes of DP in childhood and adulthood will help inform choices for therapeutic
interventions.
While individual differences canprovideunique information aboutDP, distinct phenotypesof
DPsuggesttheneedforcautionwhenplanninggroupstudies(c.f.95).Therearenoclearguidelinesfor
whichindividualscanbegroupedtogether,andhowonedeterminesinclusioncriteriamaydependon
theprimaryresearchquestion.Thus,werecommendthatwhenpresentinggroupdataonDP,individual
databeincludedtoprovideamorecompletepictureofthedistributionofscores.Onedifficultyhereis
thatmanyof themeasuressuitable forassessinggroupdifferences in faceprocessingmechanismsdo
nothavetherequiredpsychometricpropertiestoreliablydeterminewhetheranindividual is impaired
or not. As an example, faces are represented as an integratedwholemore thanmost other types of
objects,aprocesstermedconfiguralorholisticprocessing96,97.Holisticcodingcanbemeasuredwiththe
composite effect96 and part-whole effect98, and recent studies have typically shown impairments in
groups of DPs15, 99, 100. However, current versions of holistic processing tasks are not appropriate for
evaluating holistic processing at an individual level. One way that researchers have attempted to
compensateforthelowtomoderatereliabilityofeachtaskhasbeenthecognitiveneuropsychological
approachofusingmore thanoneversionofaholisticcoding task to try toobtainconsensus foreach
individual101. Interestingly, individuals with DP can show typical holistic coding101, 102, indicating that
15
whilemeasuringholistic codingmaybeuseful for thedifferentiationofpotential subtypes, it isnota
definingfeatureofDP.
With sucha complex,heterogeneousdisorder, it is likely thataportionof thepopulationwill
produceborderlineorambiguousresults.Especiallywithchildren,itispossibleforanindividualtoscore
inthe impairedrangeforonetestof facememory,butthenscore inthenormalrangeforadifferent
testof thesameability.While it isperhapssimplest todisregard these individualsasuninterpretable,
thesevariableprofilesmayprovideamorecompleteaccountofthedisorderanditsrelationshiptothe
hypothesis. It isthereforerecommendedtoincludetheseambiguouscases inreports,buttointerpret
them with caution, or to only draw firm conclusions from the clear cases. This again speaks to the
drawbacksofgroupstudies,whereborderlineorinconsistentcasesmaydilutegroupeffects.
SUMMARYOFGUIDELINESANDFUTUREDIRECTIONS
Table1providesexamplesoftasksthatareavailablefortheassessmentofDPinchildrenand
adults.Itwouldbeidealtohavevalid,reliable,andbriefteststomeasureeachoftheprocessesinvolved
infacerecognitiontodeterminethelocusoftheimpairment(e.g., intactfaceperceptionbutimpaired
facememory).Inaddition,itwouldbepreferabletohavemorethanonetestavailabletomeasureeach
oftheseprocesses,thoughatpresent,onlyCFMTtasksareavailableinmorethanoneversion.Itisalso
desirabletouseagreatermixtureofhighlycontrolledandecologicallyvalidtasks.Thetestsneedtobe
sensitive to diet of faces experienced by individuals and so will need to vary by race, and perhaps
ethnicity14. Finally, each of the tests needs to be age-appropriate – easy enough for children and
sensitivetodeclinesinperformancethatbeginfrommiddle-age.Thedesignandvalidationofadditional
testscouldbeguidedbytheprocessoftestdesignforotherconditions,suchasdevelopmentaldyslexia,
where a number of appropriate tests are available to distinguish between different subtypes of the
disorder103. We note that most recently devised tests of face recognition are freely available to
researchersviacontactingtheauthorsofthetest.However,thefieldmaywishtoconsiderestablishing
a central website for tests. We know of one that hosts numerous tests of language processing
(http://www.motif.org.au),fromwhichtestscanbeaccessedbythosewithappropriatecredentialsand
whichprovidesupdatestoresearchers.
Giventheavailable tests,weproposethe followingcertainminimumguidelines forevaluating
face recognition in adults. First, the person should report repeated instances of difficulty recognizing
faces(notnames)ineverydaylife,eitherviaquestionnaireorinterview,andnotreportanybraininjury
16
or disorder that would be expected to result in face recognition impairments (e.g. temporal lobe
epilepsy). Second, theperson shoulddemonstrate impaired face recognitionmemory (orperception),
ideally on more than one test (e.g., famous faces and CFMT; CFMT and CFMT-Australian; CFPT and
CFMT). To differentiate poor recognisers from DPs, we suggest examining z-scores and significance
levels on statistical tests such as Crawford, Garthwaite, & Howell’s (2009) modified t-tests. While a
stringent criteria would advocate that performance should be significantly impaired and below two
standarddeviationsonall testsof facememory, inpractice it is typicallymore instructive toexamine
performanceontherangeoftests includedandbeclearaboutwhichcasesmaybeambiguous.These
criteriawouldenableadiagnosisofDP,butwouldnotbe informativeas towhether the impairments
extendedtootherobjectsandifso,whetherthisisindicativeofageneralcognitiveimpairment.Forthe
former,weadvocate includingatestofobjectmemory;forthelatterweadvocateassessingcognitive
functioning with brief measures. We also recommend asking whether the individual knows of any
currentorpreviousvisual impairment,andtomeasurevisualacuity,whichif impairedcouldsuggesta
low-leveloriginforDP.Finally,ameasureofsocialfunctioningand/orpresenceofautistictraitscanhelp
todifferentiateadiagnosisofDPfromabroaderdevelopmentaldisorderofsocialfunction.
Similarguidelinesshouldbefollowedforchildren,butspecialconsiderationsmustbemade.For
instance, reportsof realworld facerecognitionproblemsarestill important,butwill likelycomefrom
parentsratherthanthechild.DiagnosisofDPinchildrencanbehinderedbyflooreffectsintestsofface
memory, particularly in younger children. As such, it is recommended to evaluate face perception in
childrenwithsuspectedDPasawayofprovidingconvergentevidenceforfaceprocessingdeficits.Given
thevariability in test taking inchildhood (bothwithin,andbetween individuals),ambiguouscasesare
likely to arise. These cases may be informative, and should be included in scientific reports, but
appropriatecautionshouldbeusedwhenofferinginterpretationsofthedata.
CONCLUSIONS
IndividualswithDPhave severe face recognitiondeficits in the absenceof brain damage and
despite normal low-level vision and intellect. The heterogeneity of the disorder, and the variety of
comorbidities that can accompany it, lead to challenges for researchers.We provided guidelines for
studyingDPbasedonourexperiences.AlthoughfacememoryimpairmentiscriticalforidentifyingDPin
adults, faceperceptionmightbethemost reliablewayto identifyDP inkids.Real lifedifficultieswith
facerecognitionalsoneedtobeconsidered.Theuseofsinglecasemodifiedt-testscansupplementthe
17
traditional approach of using two standard deviations below the mean as a cut-off for impairment.
Overallitisessentialtobetransparentandincludeasmuchinformationaspossibleforallcases.
18
Notes
ThewritingofthisarticlewassupportedbytheAustralianResearchCouncil(ARC)CentreofExcellence
in Cognition and its Disorders (CCD) [grant number CE110001021] http://www.ccd.edu.au. KAD was
supportedbyaBantingPostdoctoralFellowshipawardedbytheCanadianInstitutesofHealthResearch.
RPwas supportedby theCCDandARCDiscoveryProjectgrants (DP110100850andDP1401743).KAD
andRPwouldliketothankthemanychildrenandadultswhosegenerousparticipationinourresearch
projectshashelpedustoestablishtheseguidelines.SpecialthankstoBradDuchaineandLindaJeffery
fortheirinsightfulcommentsonpreviousdrafts.
Therearenoconflictsofinterest.
19
Table1.Someavailablemeasuresthatcanbeuseddeterminewhetherchildrenandadultshavesignificantfacerecognitiondifficultiescommensuratewithdevelopmentalprosopagnosia(DP),andwhethertheyalsopresentwithotherassociateddifficulties.
Abilities Children(ages6+)
Adults(ages18+)
Facerecognitiontests
Faceperception DartmouthFacePerceptionTest(DFPT)12
CambridgeFacePerceptionTest(CFPT)49
GlasgowFaceMatchingTest(GFMT)50
Facememory–unfamiliarfaces
CambridgeFaceMemoryTest–Kids(CFMT-Kids)20
CambridgeFaceMemoryTest–Children(CFMT-Children)45
CambridgeFaceMemoryTest(CFMT)34
Old-NewFaceRecognitiontest48
Facememory–familiarfaces
Familiarfacesprovidedbyfamilies Familiarfacesprovidedbyfamilies
FamousfaceTests17
Subjectivereportsofeverydayfacerecognitiondifficulties
Parentandchildreportsoffacerecognitiondifficulties
Anecdotalreportsoffacerecognitiondifficulties
ProsopagnosiaIndex(PI-20)21
Othertestsandmeasures
Within-categoryobjectmemory(usedtodeterminewhetherfaceandobjectmemoryimpaired)
CambridgeBicycleMemoryTest(CBMT)38
Old-NewFlowers12
CambridgeCarMemoryTest37
VanderbiltExpertiseTest39
Old-NewTests26
Selectivesocialdeficits(usedtodeterminewhethersocialdeficitsevident)
SocialResponsivenessScale-272
RepetitiveBehaviorScale-Revised73
AutismQuotient74
20
VisualAcuity(usedtodetermineadequatevisualacuity)
Parentalreportofvisualimpairments
HOTVDistancePediatricEyeChart
Self-reportofvisualimpairments
VisualacuitytestusingSloanfont
Generalfunctioning
Parentreportofanybraininjury
BirminghamObjectRecognitionBattery23
WechslerAbbreviatedScaleofIntelligence-II104
Self-reportofanybraininjury,disorder,educationallevelandoccupation.
BirminghamObjectRecognitionBattery23
DigitSpan(backwards)fromtheWechslerAdultIntelligenceScale-IV105
Raven’sProgressiveMatrices106
21
Figures
Figure1.a)FormatofCambridgeFaceMemoryTest(CFMT,Duchaine&Nakayama,2006a)foradults.
Thetargetfaceisforillustrativepurposesandisnotusedintheactualtest.b)Sampletrialfrom
CambridgeBicycleMemoryTest(CBMT,Dalrymple&Duchaine,2013)c)SampletrialfromCambridge
FaceMemoryTest–Kids(CFMT-Kids,Dalrymple,etal,2012)d)CambridgeFacePerceptionTest(CFPT,
Duchaine,Yovel,&Nakayama,2007)e)DartmouthFacePerceptionTest(forchildren)(DFPT,Dalrymple,
Garrido,&Duchaine,2014).
22
Figure2.MeanscoresbyagefordifferentversionsofCambridgeFaceMemoryTest–Kids(CFMT-Kids,
Dalrympleetal.,2012).Six-targetversionfollowstheformatoftheCFMTforadults,with72trialsin
total.Four-targetversionfollowsthesameformatastheCFMTforadults,butuses4targetsinsteadof
6,with48trialsintotal.TheImmediaterecallversionpresentstheIntroductorysectionoftheCFMT-
Kidssix-targetversiontwice,foratotalof12targets,with36trialsintotal.Specifically,childrenlearna
targetandthenpickitoutfromachoiceofthree,butareneverrequiredtoholdmultipletargetsin
memory.Errorbarsrepresentstandarddeviation.Twostandarddeviationsbelowthemeanisone
conventionforcalculatingacut-offforimpairment.Dottedlinerepresentschancelevelperformance.
23
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