Neu oscience and Biobeha io al Re iews 161 (2024) 105689
A ailable online 22 Ap il 2024
0149-7634/© 2024 The Au ho (s). Published by Else ie L d. This is an open access a icle unde he CC BY license (h p://c ea i ecommons.o g/licenses/by/4.0/).
Mini- e iew
The b eakdown o social looking
Te je Falck-Y e
a
,
b
,
*
a
De elopmen and Neu odi e si y Lab, Depa men o Psychology, Uppsala Uni e si y, Uppsala, Sweden
b
Cen e o Neu ode elopmen al Diso de s (KIND), Cen e o Psychia y Resea ch, Depa men o Women’s and Child en’s Heal h, Ka olinska Ins i u e & S ockholm
Heal h Ca e Se ices, S ockholm, Sweden
ARTICLE INFO
Keywo ds:
A en ion
Social cogni ion
In an de elopmen
E olu ion
Au ism
He i abili y
Twin s udy
Compa a i e psychology
ABSTRACT
Indi idual di e ences in social looking a e commonly belie ed o e lec one single he i able dimension igh ly
linked o au ism. Ye , ecen da a sugges ha in human in an s, looking o eyes ( a he han mou h) and
p e e ence o aces ( e sus non-social objec s) e lec dis inc gene ic in luences, and nei he appea o ha e a
clea -cu ela ion o au ism.
People a y subs an ially in e ms o which a eas o a scene hey
ixa e and how much hey a end o social s imuli (Kennedy e al., 2017;
B oda and de Haas, 2024; Cons an ino e al., 2017). In es iga ing he
ae iology o such di e ences in in an s, a ecen eye acking s udy o
mo e han 500 5-mon h-old wins conduc ed in ou lab demons a ed
ha bo h eye p e e ence (looking o eyes a he han he mou h; Fig. 1a)
and ace p e e ence (looking o aces a he han non-social objec s;
Fig. 1b) o a la ge ex en e lec gene ic a ia ion (Po ugal e al., 2024;
Vik o sson e al., 2023). This indica es a biological basis o young in-
an s’ indi idual le el o a en ion o social s imuli, and he pa o he
s imuli hey ocus on. The co ela ion be ween eye and ace p e e ence
was weak, and mul i a ia e win analyses indica ed ha he wo phe-
no ypes we e linked o independen gene ic ac o s (Fig. 1c) (Po ugal
e al., 2024). This sugges s ha , a leas in in ancy, di e en social
looking beha iou s e lec di e en unde lying p ocesses, pe haps wi h
dis inc e olu iona y his o ies (Shakesha and Plomin, 2015). This
conclusion con as s wi h he iew ha indi idual di e ences in many
di e en ypes o social looking in childhood e lec one single dimen-
sion – social isual engagemen (Cons an ino e al., 2017).
Rela edly, i has been sugges ed ha di e ences in social looking in
in ancy ep esen an endopheno ype o au ism (Cons an ino e al.,
2017; Mosconi e al., 2023; Cons an ino, 2019) – a highly he i able
condi ion de ined by a ypical social communica ion. Howe e , he
mul idimensional gene ic na u e behind wo a che ypical social gaze
pheno ypes in in ancy shown in Fig. 1c aises a new ques ion: Which o
hese a e linked o au ism? A guably, exis ing s udies o in an social
looking and i s ela ion o au ism do no indica e a clea associa ion o
nei he o hem. Fo example, in he ecen in an win s udies (Po ugal
e al., 2024; Vik o sson e al., 2023), no signi ican co ela ion wi h a
polygenic sco e o au ism was ound. Fu he , he e we e no signi ican
associa ion be ween ei he eye o ace p e e ence and la e
socio-communica i e abili y o au is ic ai s. Al hough he e we e
co ela ions wi h pa en - epo ed ocabula y de elopmen a 14
mon hs, hese co ela ions we e no signi ican when language was
e-assessed a 24 mon hs. In o he wo ds, he nea -exclusi e mou h
looking obse ed in ~ 7 % o he in an popula ion canno be ega ded
as a sign o pa hology o a ypical de elopmen (Fig. 1a). One s udy o
in an s a ele a ed likelihood o au ism has sugges ed ha g oup-le el
di e ences in eye- e sus-mou h looking eme ge g adually o e he
i s yea o li e among au is ic child en (Jones and Klin, 2013). Ano he
s udy ound educed looking o people and aces (bu no o o he s’ eyes)
a 6 mon hs o age in in an s la e diagnosed wi h au ism (Chawa ska
e al., 2013). Ye , o he s udies o in an s a ele a ed likelihood o
au ism, including ones using li e eye acking o assess in an s’ gaze
du ing eal social in e ac ion owa ds he end o hei i s yea , ha e
ailed o ind a s ong link be ween educed eye o ace p e e ence and
la e au ism diagnosis (Rudling e al., 2023; Nys om e al., 2019;
Chawa ska e al., 2012, see also Elsabbagh e al., 2013). Taken oge he ,
mo e wo k is needed o unde s and link be ween di e en ypes o social
looking in in ancy and his neu ode elopmen al condi ion.
* Co espondence o: Dep o Psychology, Box 1225, Uppsala 751 42, Sweden.
E-mail add ess: [email p o ec ed].
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Neu oscience and Biobeha io al Re iews 161 (2024) 105689
2
Indi idual eye- e sus-mou h p e e ences ha e been assumed o
e lec p ocesses ha a e domain speci ic (social) (Cons an ino e al.,
2017; Vik o sson e al., 2023). Howe e , a ecen s udy o adul s e-
po ed ha eye- e sus-mou h p e e ence has a high co ela ion wi h
e ical looking p e e ences wi hin non-social s imuli (B oda and de
Haas, 2024). This highligh s he possibili y ha eye- e sus-mou h
p e e ences ea ly in li e oo may e lec di e ences in domain gene al
isual p ocessing s yle, which u u e s udies should add ess. In ac , his
could explain why eye- e sus-mou h p e e ences gene alize o e
di e en ypes o ace s imuli and con ex s ( he eyes end o always be
abo e he mou h) (Cons an ino e al., 2017; Vik o sson e al., 2023) and
why hese p e e ences we e ound o be la gely unco ela ed wi h
ace- e sus-objec p e e ence in he abo e-men ioned in an win s udy
( o ace- e sus-objec p e e ence, e ical and ho izon al posi ion o he
wo ca ego ies we e coun e balanced) (Po ugal e al., 2024).
I could be a gued ha he dissocia ion be ween ace and eye p e -
e ence ound in he in an win s udy (Fig. 1c) could be linked o he
ace- e sus-objec s imuli being s a ic while he eye- e sus-mou h
s imuli being dynamic. Howe e , he e y high ( ~ .9) co ela ion
ac oss s ill and dynamic e sions o s imuli used o assess eye- e sus-
mou h p e e ence does no suppo his explana ion (Vik o sson e al.,
2023). In he s ill a ian s, he ac o s simply looked in o he came a wi h
a neu al acial exp ession; in he dynamic a ian s, hey mo ed na u-
ally using isual and ocal signals o engage he child (e.g., singing
ph ases om child en’s songs) (Vik o sson e al., 2023).
Also in humans’ closes li ing ela i es, chimpanzees and bonobos,
he e a e no able indi idual di e ences in ace p e e ence and eye
p e e ence (B ooks e al., 2021; Kano e al., 2015), and in adul cap i e
chimpanzees, indi idual di e ences in mu ual gaze a e linked in pa o
gene ic ac o s (Hopkins e al., 2020). I is possible ha some o he
d i ing o ces behind indi idual di e ences in social looking in humans
ha e a pa allel in in o he species.
In ea ly childhood, high empo al s abili y o eye p e e ence has been
epo ed (Cons an ino e al., 2017), bu long e m s abili y beyond ha
is, o my knowledge, no known. E idence sugges gene alisabili y o eye
p e e ence om sc een-based eye acking o li e con ex s in adul hood
Fig. 1. Social looking beha iou s in in ancy show high in e -indi idual a ia ion and e lec a leas wo unde lying e iological dimensions. a) Al hough
nea ly 50 % o i e-mon h-old in an s ha e a clea eye p e e ence when looking a aces ( igh panel), he e is a la ge a ia ion, and a non-negligible mino i y look
almos exclusi ely a he mou h (le panel). b) Deg ee o p e e ence o aces is also highly a iable be ween in an s. The e ical line e lec s chance p e e ence. c)
Bo h ace p e e ence and eye p e e ence a e he i able pheno ypes. Ye , he gene ics linked o ace p e e ence we e no ela ed o eye- e sus-mou h looking (ligh
blue), and unique gene ic in luences we e associa ed wi h eye- e sus-mou h looking (da k blue; igu e shows Cholesky bi a ia e decomposi ion; A =addi i e gene ic
in luences, E =unique en i onmen al in luences; pheno ypic co ela ion be ween he wo pheno ypes was .11, p =.025). Figu es and da a a e ep oduced and
adap ed wi h pe mission om Po ugal e al. (2024), Vik o sson e al. (2023); Illus a ion in b) by A.M. Po ugal.
T. Falck-Y e
Neu oscience and Biobeha io al Re iews 161 (2024) 105689
3
(Pe e son e al., 2016) and childhood (Falck-Y e e al., 2015). To my
knowledge, no s udy has epo ed on he gene alizabili y o ace ( e sus
objec ) p e e ences om lab-based o eal-wo ld se ings, which is
impo an o es ablish.
Ini ially un ela ed ai s may ge co ela ed o e de elopmen (Van
De Maas e al., 2006). The e o e, al hough la gely un ela ed in in ancy,
ace and eye p e e ence may po en ially show a highe associa ion
(pheno ypically and e iologically) la e on (Falck-Y e e al., 2010).
Longi udinal win s udies spanning ea ly in ancy o la e in childhood
including bo h social and non-social s imuli would help us add ess his,
as well as in es iga ing he deg ee o domain speci ici y in hese pu a-
i ely social measu es (B oda and de Haas, 2024).
Funding s a emen
This wo k was unded by S i elsen Riksbankens Jubileums ond, he
Knu and Alice Wallenbe g Founda ion, S i elsen Sunne dahls Handi-
kapp ond, and he Inno a i e Medicines Ini ia i e 2 Join Unde aking
(G an 777394). This Join Unde aking ecei es suppo om he Eu-
opean Union’s Ho izon 2020 Resea ch and Inno a ion P og amme and
EFPIA and AUTISM SPEAKS, Au is ica, SFARI. The wo k was also sup-
po ed by unds om he Eu opean Commission (H2020 p ojec CANDY;
G an 847818). Any iews exp essed a e hose o he au ho and no
necessa ily hose o he unde s. The unde s had no ole in s udy design,
da a collec ion and analysis, he decision o publish o manusc ip
p epa a ion.
Decla a ion o in e es s
The au ho decla es no con lic s o in e es .
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T. Falck-Y e
