Beyond words: an investigation of fine motor skills and the verbal communication spectrum in autism

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