Beyond wo ds: an in es iga ion
o fine mo o skills and he
e bal communica ion
spec um in au ism
Ma ian Sima o Gonzalez
1,2
*, Gessica Ni
3,4
, Vale ie Lam
2
and Ca ly Demopoulos
2,5
*
1
Spoken Language In e es G oup, Basque Cen e on Cogni ion, B ain and Language, San Sebas ian, Spain,
2
Depa men o Psychia y and Beha io al Sciences, Uni e si y o Cali o nia, San F ancisco, San F ancisco,
CA, Uni ed S a es,
3
Depa men o UCSF Epilepsy and Pedia ic B ain Cen e , Uni e si y o Cali o nia,
San F ancisco (UCSF) School o Medicine, San F ancisco, CA, Uni ed S a es,
4
Depa men o Neu ology
and Pedia ics, Uni e si y o Cali o nia, San F ancisco, San F ancisco, CA, Uni ed S a es,
5
Depa men o
Radiology and Biomedical Imaging, Uni e si y o Cali o nia, San F ancisco, San F ancisco, CA, Uni ed S a es
In oduc ion: This s udy in es iga ed he associa ions be ween fine
mo o skills and exp essi e e bal abili ies in a g oup o 97 au is ic
pa icipan s (age 8-17, mean=12.41) and 46 ypically de eloping you h (age
8-17, mean=12.48).
Me hods: Pa icipan s comple ed assessmen s o mo o and e bal
communica ion skills, including finge apping speed, g oo ed pegboa d, g ip
s eng h, isual-mo o in eg a ion asks, and measu es o speech and
communica ion skills. ASD g oup pe o mance on mo o es s was compa ed
o con ols. Non-pa ame ic es s we e used o analyze g oup di e ences and
co ela ions be ween mo o and e bal communica ionskills.Basedonp io
esea ch, we hypo hesized ha indi iduals on he au ism spec um would
exhibi defici s in fine mo o speed, dex e i y, pencil mo o con ol, bu no
manual mo o s eng h. Addi ionally, we expec ed ha impai ed fine mo o
skills would be linked o poo e pe o mance on s anda dized measu es o
e bal abili ies.
Resul s: The esul s indica ed ha 80% o au is ic pa icipan s demons a ed an
impai men on a leas one measu e o mo o skills, and as a g oup, hey
exhibi ed significan ly poo e fine mo o pe o mance compa ed o he non-
ASD g oup in dominan hand finge apping speed, bila e al fine mo o dex e i y
measu ed ia he g oo ed pegboa d ask, and pencil mo o coo dina ion and
isual-mo o in eg a ion measu ed on he Bee y-Buk enica De elopmen al
Tes o Visual-Mo o In eg a ion-Six h Edi ion. Mo eo e , impai ed fine mo o
skills we e associa ed wi h poo e pe o mance on s anda dized clinical
measu es o e bal abili ies, including a icula ion e o s, ecep i e and
exp essi e language and ocabula y, apid naming, o omo o sequencing,
and pa en epo ed unc ional communica ion skills and social
communica ion symp oms.
F on ie s in Psychia y on ie sin.o g01
OPEN ACCESS
EDITED BY
Elizabe h B. To es,
Ru ge s, The S a e Uni e si y o New Je sey,
Uni ed S a es
REVIEWED BY
Jonna Bobzien,
Old Dominion Uni e si y, Uni ed S a es
Sa a Ma ie Scha oun Benson,
Uni e si y o Windso , Canada
*CORRESPONDENCE
Ma ian Sima o Gonzalez
[email p o ec ed]
Ca ly Demopoulos
[email p o ec ed]
RECEIVED 31 Janua y 2024
ACCEPTED 06 May 2024
PUBLISHED 21 May 2024
CITATION
Sima o Gonzalez M, Ni G, Lam V and
Demopoulos C (2024) Beyond wo ds: an
in es iga ion o fine mo o skills and he
e bal communica ion spec um in au ism.
F on . Psychia y 15:1379307.
doi: 10.3389/ psy .2024.1379307
COPYRIGHT
© 2024 Sima o Gonzalez, Ni, Lam and
Demopoulos. This is an open-access a icle
dis ibu ed unde he e ms o he C ea i e
Commons A ibu ion License (CC BY). The
use, dis ibu ion o ep oduc ion in o he
o ums is pe mi ed, p o ided he o iginal
au ho (s) and he copy igh owne (s) a e
c edi ed and ha he o iginal publica ion in
his jou nal is ci ed, in acco dance wi h
accep ed academic p ac ice. No use,
dis ibu ion o ep oduc ion is pe mi ed
which does no comply wi h hese e ms.
TYPE O iginal Resea ch
PUBLISHED 21 May 2024
DOI 10.3389/ psy .2024.1379307
Discussion: O e all,ou findings sugges he e is a high p e alence o fine
mo o impai men s in ASD, and hese impai men s we e associa ed wi h a
ange o e bal abili ies. Fu he esea ch is wa an ed o be e unde s and he
unde lying mechanisms o hese associa ions and de elop a ge ed
in e en ions o add ess bo h fine mo o and e bal impai men s in ASD.
KEYWORDS
au ism, mo o skills, speech, language, communica ion
1 In oduc ion
Child en’s language, cogni ion, and social skills de elopmen
a e closely linked o hei mo o unc ion de elopmen (1,2).
P e ious esea ch has sugges ed ha mo o impai men s in
in an s a isk o , o diagnosed wi h, au ism spec um diso de
(ASD) appea be o e mo e salien social-communica i e
impai men s a e o mally diagnosed (3,4). The expanding body
o esea ch on mo o de elopmen in ASD sugges s ha au is ic
child en o en ace con inued challenges wi h g oss and fine mo o
abili ies (5,6), and hese mo o di e ences ha e been associa ed
wi h o he co e ASD symp oma ology, including language (7–9)
and social skills (10,11). Despi e ecognizing mo o delays in
ASD, specifics abou he a ec ed mo o skills emain unclea (12–
14). In es iga ing mo o abili ies and hei associa ion wi h
language de elopmen du ing childhood h ough adolescence in
au is ic indi iduals may yield aluable insigh s in o he complex
ac o s shaping hei o e all de elopmen . Such insigh s can
in o m a ge ed in e en ions aimed a add essing mo o
impai men s in his popula ion (15). Fu he mo e, ea ly
de ec ion and in e en ion o mo o di ficul ies may also lead
o imp o emen s in social communica ion o au is ic indi iduals
(16). P io esea ch on mo o skills o au is ic indi iduals has
shown significan a ia ion in esea ch design, including he
specific mo o skills assessed (e.g., gai (17,18), balance (19),
ball skills (20), pos u al de elopmen ( olling, si ing, s anding)
(21) and objec manipula ion (8)). Measu emen me hods also
a y conside ably, including pa en al ques ionnai es (22,23),
s anda dized assessmen s (8,24), beha io al coding o ideos
(25), and kinema ic mo ion cap u e (18). S udies di e in
pa icipan cha ac e is ics as well, wi h esea ch including
child en (21), adul s (17), and indi iduals ac oss he en i e
au ism spec um (14,26,27). S a is ical con ol o con ounding
a iables is also inconsis en ly applied, wi h some s udies
con olling o ac o s like IQ (25) while o he s do no (22).
This he e ogenei y makes i di ficul o d aw p ecise conclusions
abou which mo o skills a e impai ed in ASD, he magni ude o
impai men s o di e en ypes o mo o skills, he de elopmen al
ajec o y o hese impai men s, whe he mo o skill defici s a e
independen o b oade cogni i e o de elopmen al unc ioning,
o whe he mo o skill defici s a e associa ed wi h specific
subg oups o ea u es o au is ic child en (11).
Recen s udies e ealed a iabili y in mo o skills o au is ic
indi iduals based on pa en - epo ed measu es (5), s anda dized
clinical assessmen s (6,11), and neu oimaging echniques (28).
Specifically, au is ic child en had lowe sco es on pa en - epo
measu es o mo o skills compa ed o neu o ypical child en when
measu ed ia he Childhood Au ism Ra ing Scale: Mo o (CARS-M;
29), he De elopmen al Coo dina ion Diso de Ques ionnai e
(DCDQ; 30), and he Mo emen Assessmen Ba e y o Child en
(MABC-2; 23,31). Pa en epo measu es can be quickly
adminis e ed wi hou equi ing he child’s ac i e pa icipa ion.
This is pa icula ly ad an ageous o au is ic child en who may
ace challenges in adi ional es ing scena ios (32). Addi ionally,
hese measu es o e insigh s in o mo o skills ac oss di e se
se ings, including home, school, and social en i onmen s, aiding
in he iden ifica ion o s eng hs and weaknesses in mo o
de elopmen (33). Howe e , such measu es come wi h some
limi a ions, such as he subjec i e na u e o pa en obse a ions,
po en ial inaccu acies due o lack o aining, and he ocus on
obse ed beha io a he han he child’s ull capabili y.
Fo his eason, pe o mance-based s anda dized clinical
assessmen s can be used o add addi ional in o ma ion abou a
pe son’s abili ies by es ing hei pe o mance in ela ion o age-
ma ched pee s. Many s udies ha e epo ed delays and impai men s
in g oss mo o skills in au ism. A sys ema ic e iew and me a-
analysis by Whya & C aig (23) epo ed ha manual dex e i y and
ball skills (i.e., he abili y o accu a ely and e ficien ly h ow, s ike,
ca ch, and kick objec s) we e mo e impai ed han o he mo o skills,
including balance, in au is ic indi iduals, and ha objec con ol
skills we e he only mo o skills ha p edic ed la e ASD symp om
se e i y. The au ho s sugges ed ha hese impai men s may be due
o defici s in pe cep ion-ac ion coupling, he abili y o use senso y
in o ma ion o guide mo emen . These findings sugges ha objec
con ol skills may be pa icula ly impo an o unde s anding he
undamen al mechanisms unde lying mo o impai men in au ism.
This is because objec con ol skills equi e con inuous in- he-
momen in eg a ion o senso imo o eedback o adjus mo o
ou pu . In a la ge sample (N=1094), Gando a e al. (34)
iden ified a high p e alence (63–82%) o undamen al mo emen
Sima o Gonzalez e al. 10.3389/ psy .2024.1379307
F on ie s in Psychia y on ie sin.o g02
skill (FMS; i.e., balance, objec con ol, and locomo o skills)
impai men s in a sys ema ic e iew among au is ic indi iduals,
who on a e age pe o med 6.4 mon hs behind age expec a ions.
The di e ence be ween ch onological age and FMS age equi alen
inc eased p og essi ely wi h age. In addi ion, child en diagnosed
wi h ASD exhibi ed g ea e defici s in FMS compe encies,
pa icula ly in objec con ol (53–82%), locomo o skills (67–
80%), and balance skills (33–58%) when compa ed o
neu o ypical child en. Fu he mo e, s udies including pa icipan s
wi h g ea e suppo needs epo ed a highe p e alence o FMS
impai men (35). Howe e , due o gende imbalance in he
a o emen ioned s udies, wi h 85% o pa icipan s being male, he
esul s may no be gene alizable o au is ic emales.
These mo o di ficul ies ex end beyond g oss mo o skills and
encompass fine mo o skills as well. S udies examining bo h g oss
and fine mo o unc ioning ha e epo ed di ficul ies in ac i i ies
like unning and jumping, as well as isual mo o in eg a ion asks,
such as eye-hand coo dina ion and acing (36,37). The di e ences
in mo o skills be ween child en wi h and wi hou au ism we e
ound o be mos p onounced in fine mo o skills, such as hand
coo dina ion and dex e i y (6). In an s wi h high‐chance o ASD
based on amily his o y ha e been shown o ha e less de eloped
objec manipula ion on he Mullens Scale o Ea ly Lea ning (MSEL,
38)andweake fine mo o and dec eased g asping ac i i y
compa ed o in an s wi h no amilial his o y (low-chance) o ASD
(37). No ably, bo h g oups pe o med in he ypical ange on
a e age, despi e he lowe sco es in he ASD g oup. Longi udinal
assessmen s indica e ha g asping ac i i ies in high-chance in an s
inc eased be ween 6 and 10 mon hs o age o a le el compa able o
ha displayed by same-age pee s in he low-chance g oup (37). This
sugges s ha high-chance in an s may be able o ca ch up o hei
pee s in e ms o mo o de elopmen , and ha mo o skills may be
delayed a he han impai ed.
In con as , o he esea ch sugges s ha mo o impai men s
pe sis o e ime in au is ic child en compa ed o hei neu o ypical
coun e pa s and ha he g oss mo o delays we e mo e p ominen
in olde child en who we e 37–60 mon hs old (6). Simila ly, fine
mo o delays in child en wi h ASD ha e been shown o inc ease
o e ime. Fo example, oddle s on he au ism spec um be ween
he ages o 12 and 36 mon hs had significan ly lowe sco es on he
MSEL mo o scale han ypically de eloping oddle s, and hese
dispa i ies in g oss and fine mo o abili ies became mo e
p onounced wi h each 6-mon h pe iod o ch onological age (39).
Landa and Ga e -Maye (40), in hei p ospec i e s udy o 87
in an s a isk o ASD using MSEL, ound ha he child en in he
ASD g oup pe o med significan ly wo se han he o he g oups in
hei g oss and fine mo o skills as ea ly as 14 mon hs and nea ly
hal o he ASD g oup showed ‘de elopmen al wo sening’be ween
14 and 24 mon hs. These s udies indica e ha delays and/o a ypical
pa e ns in fine mo o de elopmen appea o eme ge ea ly in
au is ic child en and pe sis o e ime. Fo ins ance, Messing &
Ap ho p (27) examined uppe limb mo o skills in adolescen s wi h
ASD (aged 12–17 yea s) and ound pe sis en di ficul ies wi h mo o
coo dina ion. Simila ly, Du field e al. (26) ocusing on undamen al
mo o skills in child en (aged 7–12 yea s) wi h ASD epo ed
impai men s in balance and agili y and ound ha adolescen s
wi h ASD exhibi ed poo e balance compa ed o ypically
de eloping pee s, and Fabe e al. (14) in es iga ing gai pa e ns
in au is ic you h (aged 10–18 yea s) iden ified a ypical gai
cha ac e is ics. Mo o skills de elopmen plays a c ucial ole in
childhood, impac ing social pa icipa ion, independence,
and o e all well-being. Howe e , e en hough up o 87% o
indi iduals wi h au ism o en exhibi challenges in mo o skills
ha con ey ea ly de elopmen al isk and a e clinically significan
and ea able, hese mo o challenges ye a e o en o e looked and
unde ecognized (16).
The neu obiology o mo o di e ences has also been examined
in au ism. Child en wi h “high unc ioning au ism”(HFA) ha e
shown di e en pa e ns o ce ebella ac i i y han neu o ypical
child en du ing a finge apping mo o ask and ha e educed
unc ional connec i i y be ween he ce ebellum and o he b ain
egions in ol ed in mo o execu ion (28). Specifically, while bo h
g oups exhibi ed an icipa ed p ima y ac i a ions in co ical and
subco ical egions associa ed wi h mo o execu ion, he
neu o ypical g oup demons a ed g ea e ac i a ion in he
ipsila e al an e io ce ebellum whe eas he high- unc ioning
au ism g oup displayed heigh ened ac i a ion in he
supplemen a y mo o a ea. In addi ion, he child en wi h high-
unc ioning au ism showed educed connec i i y h oughou he
mo o execu ion ne wo k compa ed o he con ol child en.
In sum, he p io esea ch on mo o de elopmen in ASD
sugges s ha mo o delays a e appa en ea ly in de elopmen ,
o en be o e symp oms o ASD mani es , and a e associa ed wi h
social communica ion di e ences. These mo o delays may become
mo e p onounced o e ime ela i e o neu o ypical pee s, al hough
mos s udies using pe o mance-based measu es o mo o skills
ha e ocused on young child en. On he o he hand, while he e
ha e been s udies on he associa ion be ween mo o and language
skills de elopmen , hey a e o en in in an s and oddle s (e.g. 41),
bu in es iga ions in o la e childhood, adolescence, and young
adul hood a e c ucial o unde s anding he pe sis en impac o
mo o skill challenges ac oss he li espan. This pape aims o
con ibu e o a mo e comp ehensi e unde s anding o mo o
skills in ASD by ocusing on au is ic pa icipan s aged 8 o 17 yea s.
In he cu en s udy, we measu ed fine mo o abili ies o a g oup
o au is ic pa icipan s in la e childhood h ough adolescence and
examined associa ions be ween hose mo o skills and a wide ange
o e bal abili ies. Based on p io esea ch iden i ying fine mo o
di e ences in au ism (12,14,26,28,42), we hypo hesized ha
au is ic pa icipan s will sco e lowe on measu es o fine mo o
speed, dex e i y, and pencil mo o con ol, bu no manual mo o
s eng h (26). Based on ea ly de elopmen al e idence o
associa ions be ween mo o skills and language de elopmen
(7–9), we also hypo hesized ha impai ed mo o skills would be
associa ed wi h poo e pe o mance on s anda dized clinical
measu es o e bal abili ies.
Sima o Gonzalez e al. 10.3389/ psy .2024.1379307
F on ie s in Psychia y on ie sin.o g03
TABLE 1 Demog aphics (M ± SD [Range]).
ASD G oup Con ol G oup S a is ics (U)
Age 12.41 ± 2.7 [8-17.42] 12.48 ± 2.52 [8.42-16.83] 2202.50
Race (N [%])
Caucasian 55 [56.7%] 21 [45.7%]
Asian 14 [14.4%] 7 [15.2%]
A ican Ame ican 1 [1%] 0
Na i e Ame ican 1 [1%] 0
Mul i acial 24 [24.7%] 18 [39.1%]
O he 2 [2.1%] 0
E hnici y (N [%])
Hispanic 19 [19.6%] 7 [15.2%]
Non-Hispanic 78 [80.4%] 39 [84.8%]
Sex Assigned a Bi h (N [%])
Male 59 [60.82%] 22 [47.82%]
Female 38 [39.18%] 24 [52.17%]
Gende Iden ifica ion (N[%])
Female 32 [32.99%] 24 [52.17%]
Male 59 [60.82%] 21 [45.65%]
Nonbina y 3 [3.09%] 1 [2.17%]
T ansgende 3 [3.09%] 0
Handedness (N[%])
Le 12 [12.40%] 4 [8.70%]
Righ 80 [82.50%] 41 [89.10%]
Ambidex ous 5 [5.20%] 1 [2.20%]
WISC-V
FSIQ 98.33 ± 23.21 [42-138] 115.63 ± 10.76 [85-129] 1051.50**
GAI 102.08 ± 23.14 [43-143] 117.33 ± 11.22 [86-133] 1224.00**
VCI 101.88 ± 25.97 [45-139] 115.76 ± 13.59 [81-150] 1445.50*
VSI 101.82 ± 20.99 [45-138] 114.52 ± 12.94 [89-141] 1362.50**
FRI 101.38 ± 19.69 [55-140] 113.7 ± 11.4 [91-140] 1279.00**
PSI 88.06 ± 19.9 [45-123] 104.02 ± 15.23 [69-155] 1135.50**
WMI 94.59 ± 22.98 [45-146] 107.15 ± 14.38 [79-142] 1414.50*
TONI-4 102.19 ± 14.55 [63-138] 108.02 ± 9.28 [88-126] 1607.50*
CELF-5
ELI 97.13 ± 25.15 [45-139] 112.78 ± 12.62 [85-135] 1397.00**
RLI 96.39 ± 25.43 [45-141] 112.76 ± 10.26 [92-133] 1330.00**
* p < 0.01.
** p ≦0.001.
WISC-V, Wechsle In elligence Scale-Fi h Edi ion; FSIQ, Full-Scale In elligence Quo ien ; GAI, Gene al Abili y Index; FRI, Fluid Reasoning Index; PSI, P ocessing Speed Index; VCI, Ve bal
Comp ehension Index; VSI, Visual Spa ial Index; WMI, Wo king Memo y Index; TONI-4, Tes o Non e bal In elligence, Fou h Edi ion; CELF-5, Clinical E alua ion o Language
Fundamen als-5
h
Edi ion; ELI, Exp essi e Language Index; RLI, Recep i e Language Index.
Sima o Gonzalez e al. 10.3389/ psy .2024.1379307
F on ie s in Psychia y on ie sin.o g04
2 Ma e ials and me hods
2.1 Pa icipan s
Pa icipan s we e 97 English-speaking you h (59 males, 38 emales)
ages 8–17 (M = 12.41, SD = 2.7) wi h a DSM-5 (43) diagnosis o ASD
and 46 non-au is ic you h (22 males, 24 emales), ages 8–17 (M = 12.48,
SD = 2.52). Demog aphic da a a e p esen ed in Table 1.
2.2 P ocedu es
A e ob aining in o med consen and assen , pa icipan s we e
scheduled o a diagnos ic e alua ion and neu opsychological
es ing o e he cou se o 2–3 isi s. O de o es s adminis e ed
p io i ized pa icipan p e e ences and needs and hus was no
s anda dized. B eaks and p ac ice sessions we e o e ed as needed,
and when necessa y, isi s we e b oken up in o sho e sessions o
accommoda e pa icipan needs. All pa icipan s we e adminis e ed
he pa en epo measu e, he Social Communica ion
Ques ionnai e (SCQ; 44). ASD pa icipan s and hose wi hou a
p io ASD diagnosis who sco ed >10 on he SCQ we e e alua ed o
ASD using gold s anda d diagnos ic ools, including he Au ism
Diagnos ic Obse a ion Schedule-2
nd
Edi ion (ADOS-2; 45) and he
Au ism Diagnos ic In e iew-Re ised (ADI-R; 46). E alua ion o
symp oms acco ding o DSM-5 diagnos ic c i e ia was
con ex ualized acco ding o pa icipan s’language and in ellec ual
abili ies, assessed on he Clinical E alua ion o Language
Fundamen s-5
h
Edi ion (CELF-5; 47)and heWechsle
In elligence Scale o Child en-Fi h Edi ion (WISC-V; 48). The
pa icipan s’handedness was sel - epo ed and confi med ia
obse a ion o hand selec ed o w i ing asks. Fo pa icipan s
whose handedness was desc ibed as ambidex ous, hey we e
ins uc ed o use hei p e e ed hand fi s o mo o asks, and
his hand was sco ed as he dominan hand o gene a ion o no m-
e e enced sco es.
2.3 Measu es
2.3.1 Mo o es s
Finge apping speed was assessed bila e ally ia a boa d
moun ed appe wi h coun e (Finge Tapping Tes ; FTT; h ps://
www.pa inc.com/P oduc s/Pkey/114) acco ding o p ocedu es
ou lined in he Hals ed-Rei an Neu opsychological Ba e y (49).
Specifically, pa icipan s used hei index finge o dep ess and
elease he appe o he poin o ad ancing he coun e . The
numbe o aps comple ed in a 10 second window was eco ded
o each ial, sepa a ely o each hand. To ensu e consis ency o
esponses, a minimum o fi e ials was adminis e ed. I he o al
numbe o aps o each ial was no wi hin 5 aps o all o he ials,
addi ional ials we e adminis e ed un il consis ency was achie ed.
I consis ency was no achie ed wi hin 10 ials, he numbe o aps
was a e aged ac oss all 10 ials. This p ocedu e was pe o med
sepa a ely o each hand. Age scaled sco es we e hen compu ed
sepa a ely o he dominan and nondominan hand om he
Findeis & Weigh no ms published in Ba on (50).
Fine mo o dex e i y was assessed ia he G oo ed Pegboa d
Tes (GPT) acco ding o he s anda dized clinical p ocedu es
applied in he collec ion o he no ma i e da a used o compu e
age-scaled sco es (51). Specifically, pa icipan s a e equi ed o
sequen ially inse g oo ed pegs in o keyhole shaped holes as
quickly as possible using only one hand a a ime. Pe o mance
was assessed o bo h dominan and nondominan hand sepa a ely,
one ial each. The numbe o pegs d opped was also eco ded. An
age-scaled sco e was compu ed o he comple ion ime o place
pegs in o all 25 holes o pa icipan s o e eigh yea s o age. Fo
pa icipan s 8 yea s old and younge , only 10 pegs a e adminis e ed.
Manual s eng h o g ip (SOG) was measu ed by use o a hand
dynamome e acco ding o s anda dized p ocedu es employed in
de i ing he no ma i e da a used o compu e scaled sco es no med
acco ding o sex a bi h and age (52). This es equi ed he
pa icipan o hold and squeeze he dynamome e g ip in hei
hand as igh ly as possible. The a e age s eng h in kilog ams o wo
ials was eco ded o each hand. I he wo ials we e no wi hin 5
kilog ams o one ano he , a hi d ial was comple ed and he
a e age o wo ials ha we e closes o one ano he was used o
compu e a no m- e e enced sco e acco ding o age and sex a bi h,
sepa a ely o each hand (52).
Addi ionally, pa icipan s we e adminis e ed he Bee y–
Buk enica De elopmen al Tes o Visual–Mo o In eg a ion, 6 h
Edi ion (Bee y VMI; 53). The Bee y VMI includes sub ex s ha
isola e skills in isual pe cep ion, isual mo o in eg a ion (VMI),
and pencil mo o coo dina o (VMI-mo o ). The VMI and VMI-
mo o sub es age-scaled sco es we e conside ed o his s udy. The
VMI sub es equi es he pa icipan o copy geome ic o ms on
pape wi h a pencil. The accu acies o he copied geome ic o ms
a e sco ed wi h objec i e sco ing c i e ia ou lined in he es
manual. The VMI-mo o sub es equi es he pa icipan d aw he
same o ms wi hin an ou line shape ha cons ains he shape’s
o m. Age-scaled sco ed we e compu ed o bo h o hese sub es s.
2.3.2 Ve bal communica ion
Assessmen o e bal communica ion was comp ehensi e in
scope, anging om mo e basic unc ions elian on senso imo o
con ol o speech, including diadochokinesis and a icula ion, o
mo e linguis ically demanding asks. Diadochokinesis was
quan ified as he comple ion ime o 8 epe i ions o he
consecu i e p oduc ion o he sounds “puh, uh, kuh,”wi h be e
pe o mance being quan ified by sho e comple ion ime in
seconds, in acco dance wi h s anda dized p ocedu es ou lined in
he O al Speech Mechanism Sc eening Examina ion-Thi d Edi ion
(54). Simila ly, he O omo o Sequences sub es o he NEPSY-II
(55), which equi es he pa icipan o epea “ ongue wis e s”o
inc easing complexi y, is also quan ified as a aw sco e, as age-scaled
sco es we e no a ailable o ou age ange. Fo his es , aw sco es
eflec he o al numbe o i ems sco ed as co ec , wi h highe
sco es indica ing be e pe o mance. In con as , a icula ion e o s
we e o aled as a aw sco e on he Sounds-In-Wo ds sub es o he
Goldman–F is oe Tes o A icula ion–Thi d Edi ion (GFTA–3;
Sima o Gonzalez e al. 10.3389/ psy .2024.1379307
F on ie s in Psychia y on ie sin.o g05
56), wi h highe sco es indica ing mo e a icula ion e o s. Age-
scaled sco es we e used o es s o apid naming speed (Inhibi ion
Naming sub es o he NEPSY-II), audi o y and isual naming
esponse ime (Audi o y and Visual Naming Tes o Child en;
AVNT-C; 57), exp essi e (Exp essi e Vocabula y Tes Thi d
Edi ion; EVT–3; 58) and ecep i e ocabula y (Peabody Pic u e
Vocabula y Tes ™Fi h Edi ion; PPVT™–5; 59), and language
(CELF–5; 47). Fo all age-scaled sco es, highe sco es indica e be e
pe o mance. Finally, pa en epo o unc ional communica ion
and social communica ion skills we e assessed ia he age-scaled
Func ional Communica ion scale on he Beha io Assessmen
Sys em o Child en-Thi d Edi ion (BASC-3; 60) and he o al
( aw) sco e on he SCQ (44), espec i ely. Fo he BASC-3
Func ional Communica ion sco e, highe sco es indica e be e
unc ional communica ion, whe eas, on he SCQ, highe sco es
indica e g ea e deg ee o social communica ion di ficul ies.
2.4 Da a analysis
Fi s , o de e mine i mo o measu es demons a ed highe
a es o impai men in ou ASD g oup, z es s o independen
p opo ions we e compu ed o compa e he p opo ions o
impai ed sco es (>1.5 SD below he mean o he no ma i e
sample) on mo o measu es be ween g oups. Sco es ha a e >1.5
SD below he no ma i e mean would be labeled as “Below A e age”
o “Excep ionally Low”acco ding o he Ame ican Academy o
Clinical Neu opsychology consensus con e ence s a emen on
uni o m labeling o pe o mance es sco es (61). Thus, hese
sco ed we e conside ed “impai ed” o hese analyses. One sample
Kolmogo o -Smi no es s o no mali y indica ed ha he
majo i y o mo o a iables we e no no mally dis ibu ed. As
such, nonpa ame ic s a is ical es s we e pe o med o examine
g oup con as s and co ela ions. Age-scaled sco es o FTT, GPT,
SOG, VMI, and VMI Mo o we e compa ed be ween au ism and
con ol g oups using Mann Whi ney U es s. Dominan hand
a iables esul ing in s a is ically significan g oup di e ences
we e subjec o bi a ia e nonpa ame ic co ela ions o assess he
associa ion be ween e bal communica ion and mo o skills.
Co ela ions we e pe o med sepa a ely o each g oup.
Benjamin–Hochbe g p ocedu es we e applied o g oup con as s
and co ela ion analyses o con ol o ype I e o .
2.5 E hics s a emen
All s udy p ocedu es we e app o ed by he Ins i u ional Re iew
Boa d a he Uni e si y o Cali o nia-San F ancisco (IRB# 11–
05249, 21–33613). Pa en al consen and assen we e secu ed o all
pa icipan s p io o en ollmen .
3 Resul s
Impai ed sco es we e significan ly mo e common in he ASD
ela i e o he TDC g oup o he dominan hand g oo ed pegboa d
(z=-4.120, p<.001) and VMI es s (z=3.461, p=.001). The endency
o ha e a leas one impai ed sco e ac oss all mo o measu es also
was significan ly g ea e in he ASD g oup (z=-3.424, p=.001).
These sco es indica e highe o e all a es o mo o impai men in
he ASD g oup. Ra es o impai ed sco es o mo o asks in he ASD
and Non-ASD G oups a e shown in Figu e 1.
Resul s o Mann–Whi ney U Tes s iden ified s a is ically
significan g oup di e ences in dominan hand finge apping
FIGURE 1
Ra es o Impai ed Sco es on Mo o Tasks in he ASD and Non-ASD g oup.
Sima o Gonzalez e al. 10.3389/ psy .2024.1379307
F on ie s in Psychia y on ie sin.o g06
speed (U= 1464.500 p = 0. 002), dominan (U= 1011.500, p < 0.001)
and non–dominan (U=1347.000, p < 0.001) g oo ed pegboa d
pe o mance, VMI (U= 1250.500, p = 0.001), and VMI mo o (U=
1350.000, p < 0.001). Significan g oup di e ences we e no iden ified
o dominan (U=1809.500 p = 0.275) and non–dominan (U=
1767.000, p = 0.276) g ip s eng h, and non–dominan finge apping
speed (U= 1632.500, p = 0.030) a e co ec ion o mul iple
compa isons. Gi en po en ial disc epancies be ween hand
p e e ence and pe o mance in au is ic indi iduals (62,63), we
pe o med pos hoc g oup con as s o igh - and le -hand
pe o mance on all mo o measu es. The six pa icipan s who
desc ibed hei handedness as ambidex ous we e no included in
hese pos hoc analyses. Significan g oup di e ences we e iden ified
o le hand finge apping speed (U=1431.00, p=.012), and
bila e ally o g oo ed pegboa d (U=1005.50, p<.001 o igh hand;
U=1203.00, p<.001 o le hand) a e mul iple compa isons
co ec ion. Significan g oup di e ences we e no iden ified o
igh hand finge apping speed (U=1497.50, p=.017), no o igh
(U=1711.00, p=.375) o le hand g ip s eng h (U=1636.50, p=.292)
a e co ec ing o mul iple compa isons.
Al hough age scaled sco es we e used o all mo o measu es, we
examined associa ions ia Spea man co ela ions be ween he eigh
age-scaled mo o sco es and pa icipan age o de e mine i he e
was e idence o de elopmen al e ec s on de ia ion om he
no ma i e mean. A e con olling o mul iple compa isons, only
he ASD g oup demons a ed a significan co ela ion be ween one
measu e, nondominan hand g ip s eng h, and age ( =-.306,
p=.003). No ably, he magni ude o his associa ion was simila
o he TDC g oup; howe e , i did no achie e s a is ical
significance a e con olling o mul iple compa isons due o he
ela i ely smalle sample size ( =-.314, p=.041). Gi en his
significan age e ec and nonsignifican one sample Kolmogo o -
Smi no es o no mali y on his a iable, a pos -hoc analysis o
co a iance was pe o med o de e mine whe he g oups
significan ly di e ed in nondominan hand g ip s eng h a e
con olling o he e ec s o age. ANCOVA esul s we e
nonsignifican (p=.430), indica ing ha , a e con olling o
e ec s o age, g oups did no di e in s eng h o g ip.
Spea man co ela ions be ween mo o skills and e bal
communica ion in he ASD g oup a e p esen ed in Table 2.A
unique associa ion was iden ified be ween slowe diadochokine ic
a e and slowe finge apping speed, whe eas o he mo o es s had
b oade associa ions wi h a ange o communica ion skills.
Specifically, ewe a icula ion e o s and be e pe o mance on
measu es o ecep i e and exp essi e language and ecep i e
ocabula y we e associa ed wi h be e fine mo o dex e i y,
pencil mo o coo dina ion, and isual-mo o in eg a ion. Be e
pencil mo o coo dina ion and isual mo o in eg a ion we e
addi ionally associa ed wi h be e exp essi e ocabula y, apid
naming, and o omo o sequencing. Finally, pencil mo o
coo dina ion was he only a iable associa ed wi h pa en epo
measu es o unc ional and social communica ion, wi h be e
mo o coo dina ion being associa ed wi h be e unc ional
communica ion skills and ewe social communica ion symp oms.
While only powe ed o de ec la ge e ec s, co ela ion alues we e
gene ally small o he con ol g oup and we e no s a is ically
significan a e co ec ion o mul iple compa isons. These esul s
can be ound in he Supplemen a y Ma e ials (Table 3).
TABLE 2 Nonpa ame ic co ela ions ( ) be ween measu es o mo o skills and communica ion in ASD pa icipan s.
Communica ion Va iables
(Clinical Measu e)
Mo o Measu es
DGPT VMI VMI-Mo o DFTT
Diadochokinesis -0.267 -0.216 -0.223 -0.411*
A icula ion (GFTA-3) -0.402* -0.381* -0.388* -0.232
O omo o Sequences (NEPSY-II) 0.212 0.446* 0.452* 0.248
Rapid Naming (NEPSY-II) 0.253 0.378* 0.339* 0.162
Audi o y Naming Response Time (AVNT-C) 0.341 0.290 0.289 0.021
Visual Naming Response Time (AVNT-C) 0.200 0.249 0.303 0.161
Exp essi e Vocabula y (EVT-3) 0.238 0.384* 0.472* 0.101
Recep i e Vocabula y (PPVT-5) 0.333* 0.397* 0.411* 0.062
Exp essi e Language (CELF-5) 0.371* 0.521* 0.502* 0.124
Recep i e Language (CELF-5) 0.332* 0.475* 0.456* 0.107
Func ional Communica ion (BASC-3) 0.163 0.439* 0.315 0.275
Pa en Repo ed Social Communica ion (SCQ) -0.236 -0.367* -0.291 -0.191
* Significan a e Benjamin-Hochbe g co ec ion o mul iple compa isons.
GFTA-3, Goldman-F is oe Tes o A icula ion, Thi d Edi ion; EVT-3, Exp essi e Vocabula y Tes , Thi d Edi ion; AVNT-C, Audi o y and Visual Naming Tes - Child en; BASC-3, Beha io
Assessmen Sys em o Child en, Thi d Edi ion; CELF-5, Clinical E alua ion o Language Fundamen als, Fi h Edi ion; PPVT-5, Peabody Pic u e Vocabula y Tes , Fi h Edi ion; SCQ, Social
Communica ion Ques ionnai e; DGPT, Dominan Hand G oo ed Pegboa d Tes ; VMI, Bee y–Buk enica De elopmen al Tes o Visual–Mo o In eg a ion; VMI-Mo o , Bee y–Buk enica
De elopmen al Tes o Visual–Mo o In eg a ion - Mo o Coo dina ion; DFTT, Dominan Hand Finge Tapping Tes .
Sima o Gonzalez e al. 10.3389/ psy .2024.1379307
F on ie s in Psychia y on ie sin.o g07
4 Discussion
The cu en s udy compa ed manual mo o abili ies o au is ic
pa icipan s o hei non–au is ic pee s in a sample wi h an age
ange om la e childhood h ough adolescence. Associa ions
be ween hese mo o skills and e bal abili ies also we e explo ed.
As hypo hesized, lowe a e age sco es we e iden ified ac oss many
mo o es s in he ASD g oup, including dominan hand and le
hand finge apping speed, bila e al manual dex e i y, and mo o
coo dina ion and isual-mo o in eg a ion on he VMI, whe eas no
g oup di e ences we e iden ified in g ip s eng h. These esul s a e
consis en wi h o he esea ch ha has demons a ed slowe finge
apping in hose wi h highe au is ic ai s (ages 18–78) (27),
di ficul y wi h asks ha equi e hand–eye–coo dina ion in
au is ic child en and adul s (ages 5–33 yea s) (26) isual–mo o
in eg a ion in au is ic child en and you h (ages 9–15) (14), and
dissocia ion be ween hand p e e ence and pe o mance in au is ic
indi iduals (62,63).
When conside ing he clinical in e p e a ion o his da ase , he
majo i y o pa icipan s in he ASD g oup demons a ed some o m
o mo o impai men (80.9%). Mo o impai men was significan ly
less common in he non-ASD g oup (47.6%). No ably, he
p e alence o mo o impai men on any specific measu e in he
non-ASD g oup ne e eached 25%, as low a es o mo o
impai men s we e sp ead ac oss es s. In con as , he ASD g oup
had high a es o impai men ac oss measu es o dex e i y,
coo dina ion, and isual-mo o in eg a ion. Ra es o impai men
in finge apping speed and g ip s eng h did no significan ly di e
be ween g oups. Co ela ions be ween age and age-scaled sco es on
mo o es s we e gene ally low, sugges ing ha his is no a
de elopmen al e ec o impai men in hese mo o skills. The one
excep ion was ha bo h g oups demons a ed a nega i e co ela ion
o magni ude >.3 be ween age and nondominan hand age-scaled
g ip s eng h sco es; howe e , he age e ec did no impac he lack
o g oup di e ences in s eng h o g ip. No ably, all es s in which
highe a es o impai ed sco es we e iden ified in he ASD g oup
we e asks ha equi ed some le el o isual-mo o in eg a ion,
whe eas finge apping speed and g ip s eng h es s could
echnically be pe o med wi hou looking. This is consis en wi h
p io wo k desc ibing defici s in senso imo o in eg a ion as a
p ominen symp om in au ism (64).
Consis en wi h ou second hypo hesis, we ound ha poo e
pe o mance on es s o mo o skills p edic ed lowe e bal
communica ion abili ies in au is ic pa icipan s. Fi s , a unique
associa ion was iden ified o basic mo o speed in he manual
and mo o speech modali ies, as slowe diadochokine ic a e was
associa ed wi h slowe finge apping speed. This finding sugges s
ha a slowe mo o speed gene alizes ac oss manual and ocal
mo o domains o unc ioning o some indi iduals wi h au ism.
In con as , mo e complex mo o asks equi ing dex e i y,
coo dina ion, and senso imo o in eg a ion we e associa ed wi h
b oade ange o mo e complex e bal communica ion skills. Fo
example, o omo o sequencing, which equi es accu a e p oduc ion
o ongue wis e s, and apid naming we e associa ed wi h fine
mo o coo dina ion and isual-mo o in eg a ion. These fine mo o
skills also we e s ongly associa ed wi h a icula ion and exp essi e
language skills. These findings may eflec a cascade impac o
senso imo o con ol defici s, including senso imo o con ol o
speech, on de elopmen o speech and language abili ies. Fo
example, imbalance in eed o wa d and eedback con ol sys ems
has been epo ed in p io au ism s udies (3). Al hough much o his
wo k has ocused on isual-mo o o pos u al con ol, eme ging
TABLE 3 Nonpa ame ic co ela ions ( ) be ween measu es o mo o skills and communica ion in non-ASD g oup.
Communica ion Va iables
(Clinical Measu e)
Mo o Measu es
DGPT VMI VMI-Mo o DFTT
Diadochokinesis -0.05 -0.047 0.322 -0.326
A icula ion (GFTA-3) 0.255 0.061 -0.023 0.252
O omo o Sequences (NEPSY-II) 0.036 0.157 -0.145 -0.034
Rapid Naming (NEPSY-II) 0.400 0.090 -0.085 0.367
Audi o y Naming Response Time (AVNT-C) 0.097 0.045 -0.005 0.048
Visual Naming Response Time (AVNT-C) 0.118 -0.128 -0.063 -0.144
Exp essi e Vocabula y (EVT-3) 0.180 0.013 0.004 -0.019
Recep i e Vocabula y (PPVT-5) 0.211 0.186 0.155 0.069
Exp essi e Language (CELF-5) 0.056 0.104 0.082 -0.128
Recep i e Language (CELF-5) 0.369 0.205 0.281 0.035
Func ional Communica ion (BASC-3) 0.059 0.056 -0.122 0.135
Pa en Repo ed Social Communica ion (SCQ) 0.002 0.081 -0.132 -0.064
* Significan a e Benjamin-Hochbe g co ec ion o mul iple compa isons.
GFTA-3, Goldman-F is oe Tes o A icula ion, Thi d Edi ion; EVT-3, Exp essi e Vocabula y Tes , Thi d Edi ion; AVNT-C, Audi o y and Visual Naming Tes - Child en; BASC-3, Beha io
Assessmen Sys em o Child en, Thi d Edi ion; CELF-5, Clinical E alua ion o Language Fundamen als, Fi h Edi ion; PPVT-5, Peabody Pic u e Vocabula y Tes , Fi h Edi ion; SCQ, Social
Communica ion Ques ionnai e; DGPT, Dominan Hand G oo ed Pegboa d Tes ; VMI, Bee y–Buk enica De elopmen al Tes o Visual–Mo o In eg a ion; VMI-Mo o , Bee y–Buk enica
De elopmen al Tes o Visual–Mo o In eg a ion - Mo o Coo dina ion; DFTT, Dominan Hand Finge Tapping Tes .
Sima o Gonzalez e al. 10.3389/ psy .2024.1379307
F on ie s in Psychia y on ie sin.o g08
esea ch sugges s ha audi o y- ocal mo o con ol di e ences a e
common in au ism and ela ed condi ions, and a e associa ed wi h
e bal abili ies (65,66).
Di e ences in mo o speech canno accoun o all associa ions,
howe e , as ecep i e language and ocabula y also we e
significan ly co ela ed wi h fine mo o coo dina ion and
dex e i y and isual mo o in eg a ion. P io esea ch has
demons a ed such associa ions be ween mo o skills and
ecep i e language abili ies in oddle s. Fo example, Wu e al.
(67) ound a s ong co ela ion be ween ecep i e language abili ies
and mo o unc ioning in oddle s wi h ASD. Those wi h delayed
language de elopmen had lowe mo o skills sco es han hose wi h
ypical language de elopmen . This sugges s a connec ion be ween
ea ly mo o and language impai men s in ASD. Findings may
suppo mo o -based in e en ions o language de elopmen in
young ASD child en. In con as , esponse ime on audi o y and
isual naming asks we e no significan ly associa ed wi h any
mo o skill measu es, al hough a e co ec ion o mul iple
compa isons hese analyses we e only powe ed o de ec mode a e
o la ge e ec s. The e o e, i is possible ha weake associa ions
exis be ween fine mo o skills and o he e bal abili ies, such as
naming esponse ime, ha we e no de ec ed in his s udy.
Finally, pencil mo o coo dina ion was he only a iable
associa ed wi h ei he pa en epo measu e. Specifically, be e
pencil mo o coo dina ion was associa ed wi h be e unc ional
communica ion skills and ewe social communica ion symp oms,
sugges ing an o e all associa ion be ween co e symp oms o au ism
and fine mo o skills. Indeed, Oha a e al. (68) epo ed a s onge
ela ionship be ween fine mo o skills and social skills han be ween
g oss mo o skills and social skills. They also no ed ha objec
con ol skills and manual dex e i y we e he mos closely linked o
social skills wi hin each mo o skill domain. This is consis en wi h
ou finding ha pencil mo o con ol was significan ly associa ed
wi h unc ional and social communica ion skills.
Taken oge he , hese findings sugges ha child en and
adolescen s wi h ASD who ha e be e fine mo o skills end o
ha e be e e bal communica ion skills. This is consis en wi h
p e ious esea ch showing ha mo o skills and language
de elopmen in au is ic child en a e closely linked in ea ly
childhood, and may sha e common neu al unde pinnings (8,23).
Gowen and Hamil on (69) sugges a dissocia ion be ween mo o
execu ion and senso y in eg a ion o mo o planning in au ism. In
simple e ms, while au is ic indi iduals may no ha e inhe en
di ficul y execu ing mo emen s, hey migh ace challenges in
p ocessing he senso y in o ma ion necessa y o plan and
coo dina e hose mo emen s e ec i ely. This highligh s he
impo ance o examining in o ma ion p ocessing alongside mo o
execu ion when e alua ing mo o abili ies in ASD. Building on his
explo a ion o senso y in eg a ion and mo o di ficul ies in au ism, we
can ex end his concep o he ealm o communica ion and language.
Simila challenges in p ocessing senso y in o ma ion migh unde lie
di ficul ies obse ed in hese a eas as well. Jus as mo o planning may
be dis up ed by defici s in in e p e ing senso y cues o mo emen , so
oo migh he abili y o unde s and and p oduce speech be a ec ed
by p oblems in eg a ing audi o y and isual in o ma ion o by
di ficul ies ole a ing he senso y expe ience o social in e ac ion
(70–75). This highligh s he in e connec edness o senso y
p ocessing, mo o unc ion, communica ion, and social in e ac ion
in he au ism spec um. This collec i e wo k sugges s ha mo o
con ol is only one o many ac o s ha may con ibu e o language
de elopmen in au is ic child en. O he ac o s ha we e no he
ocus o he p esen s udy, such as gene ics, en i onmen , and o he
cogni i e skills, likely also play a ole.
Ou findings ha e se e al implica ions o he assessmen and
ea men o au is ic child en. Fi s , ou findings indica e ha he
majo i y o ASD pa icipan s demons a ed mo o impai men on a
leas one s anda dized es o manual mo o unc ion. This sugges s
ha fine mo o skills should be assessed ou inely in au is ic child en,
as hey may equi e ea men . Second, ou findings o associa ions
be ween mo o and e bal communica ion abili ies sugges s ha
in e en ions a ge ing mo o skills may also ha e benefi s o
de elopmen o communica ion skills. Fu u e esea ch should
in es iga e he causal mechanisms unde lying he link be ween
mo o con ol and language abili ies in child en wi h ASD.
Da a a ailabili y s a emen
The aw da a suppo ing he conclusions o his a icle will be
made a ailable by he au ho s, wi hou undue ese a ion.
E hics s a emen
The s udies in ol ing humans we e app o ed by Ins i u ional
Re iew Boa d a he Uni e si y o Cali o nia-San F ancisco. The
s udies we e conduc ed in acco dance wi h he local legisla ion
and ins i u ional equi emen s. W i en in o med consen o
pa icipa ion in his s udy was p o ided by he pa icipan s’legal
gua dians/nex o kin.
Au ho con ibu ions
MS: Concep ualiza ion, W i ing –o iginal d a , W i ing –
e iew & edi ing, Fo mal Analysis, In es iga ion. GN:
Concep ualiza ion, W i ing –o iginal d a , W i ing – e iew &
edi ing. VL: Da a cu a ion, Fo mal Analysis, Visualiza ion, W i ing
–o iginal d a , W i ing – e iew & edi ing. CD: Concep ualiza ion,
Fo mal Analysis, Funding acquisi ion, In es iga ion, Supe ision,
W i ing –o iginal d a , W i ing – e iew & edi ing, Da a
cu a ion, Valida ion.
Funding
The au ho (s) decla e financial suppo was ecei ed o he
esea ch, au ho ship, and/o publica ion o his a icle. This
esea ch was suppo ed by he Na ional Ins i u es o Heal h
(g an numbe s, K23DC016637–01A1, and R01DC019167–01A1),
Au ism Speaks Royal A chmasons Cen al Audi o y P ocessing
Diso de Awa ds (11637), and UCSF Weill Ins i u e o
Sima o Gonzalez e al. 10.3389/ psy .2024.1379307
F on ie s in Psychia y on ie sin.o g09
