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. Author manuscript; available in PMC: 2025 Sep 1.
Published in final edited form as: Autism. 2024 Mar 8;28(9):2191–2203. doi: 10.1177/13623613231225498

Developmental Associations Between Motor and Communication Outcomes in Fragile X syndrome: Variation in the Context of Co-Occurring Autism

Elizabeth A Will 1, Kimberly Hills 1, Kayla Smith 2, Samuel McQuillin 1, Jane E Roberts 1
PMCID: PMC11380705  NIHMSID: NIHMS1954326  PMID: 38456297

Abstract

Fragile X syndrome (FXS), the leading heritable cause of intellectual disability, has a co-occurrence rate of autism spectrum disorder (ASD) estimated at ~60%. The onset and rates of motor development in FXS are slower relative to neurotypical development, and even more so in the context of co-occurring FXS+ASD. Extant evidence suggests these differences are likely to affect communication, yet this developmental process or how it varies in the context of co-occurring ASD remains unknown in FXS. We aimed to delineate developmental associations between early motor abilities and their rate of development from 9- to 60-months of age on communication outcomes in 51 children with FXS, 28 of whom had co-occurring ASD. We also aimed to identify variation in these developmental associations in the context of co-occurring ASD. Results captured within-syndrome variability in these developmental associations as a function of cooccurring ASD. Fine motor proved to be a robust predictor of receptive communication regardless of cooccurring ASD, but we identified differences between FXS with and without ASD in the association between aspects of motor development and expressive outcomes. Findings provide evidence for differential developmental processes in the context of cooccurring ASD with implications for timely developmental intervention.

Motor abilities and their subsequent development provide an important mechanism for initiating and supporting the emergence of skills in adjacent domains such as communication (Iverson, 2021). This developmental process embodies Dynamic Systems Theory, which posits that the individual is a self-organizing system within which developmental pathways emerge from starting states and cascade to effect emergence in adjacent areas of development and outcomes (Smith, 2005; Smith & Thelen, 2003; Thelen, 2005). Evidence from neurotypical infant science supports this framework with a multitude of studies establishing that proficient motor skill acquisition supports action understanding, emergent cognition, and the development of language and social communication (Iverson, 2021; Mason et al., 2019; Needham & Libertus, 2011). Further, greater motor proficiency and exploration in infancy have long-term implications for optimal academic and adaptive outcomes in middle childhood and adolescence (Bornstein et al., 2013). Despite evident motor delays that may expectedly disrupt the developmental linkage between motor abilities and communication outcomes, this developmental association has also been substantiated in the context of autism spectrum disorder (ASD), including for children with an ASD diagnosis, as well as infant siblings of children with ASD who do not receive a later ASD diagnosis (Bradshaw et al., 2018; LeBarton & Iverson, 2013, 2016). While this developmental connection evidently persists despite the relatively minor motor impairments evident in the context of ASD (Bhat, 2021; Bhat et al., 2022), the extent to which this developmental linkage between motor and communication in genetic conditions with much more substantial impairments in early motor abilities remains unclear.

Fragile X syndrome (FXS) is one such genetic condition vulnerable to compounded developmental risk and compromised outcomes resulting from virtually universal intellectual disability and, potentially, an impaired motor system. A high co-occurrence rate of ASD in FXS introduces an exceptional developmental vulnerability that may translate to a more impaired motor system than in FXS or ASD alone, and one that may exert more substantial constraints and increased developmental consequences in adjacent domains like communication (Will et al., 2019). Despite bourgeoning evidence of cross-sectional associations between motor and communication in FXS (Will & Roberts, 2021), little is known regarding the effect of the delayed onset and slower rates of motor development on communication outcomes for children with FXS. Moreover, whether these effects are amplified in the context of co-occurring ASD in FXS is currently unknown. Our study aims to address these knowledge gaps by examining variation in the effect of early motor skills and the rate of development on communication outcomes from infancy through five years old in FXS with and without co-occurring ASD.

Fragile X Syndrome

Fragile X syndrome is caused by an overexpansion of CGG repeats on the FMR1 gene, which suppresses the production of FMRP, a protein critical for brain development (Loesch et al., 2004; Tassone et al., 2000). As an X-linked disorder, males are differentially affected with a higher prevalence – 1:7,000 males versus 1:11,000 females – and typically present with more severe symptomatology (Hunter et al., 2014). The FXS phenotype is partially characterized by mild-to-moderate intellectual disability, impairments in language and communication (Hahn et al., 2017; Kaufmann et al., 2017; Sterling & Warren, 2008), neurobehavioral difficulties like delayed motor development and atypical motor function (Baranek et al., 2005; Hinton et al., 2013), and elevated rates of co-occurring conditions (Klusek, Roberts, et al., 2015; Roberts et al., 2020). Many factors contribute to heterogeneity within the FXS phenotype, including sex, variation in intellectual ability, and prominently, co-occurring ASD.

Autism Spectrum Disorder in Fragile X Syndrome

Despite a high degree of phenotypic similarity between idiopathic ASD (ASD with no known genetic cause) and FXS, evidence supports ASD as a truly distinct co-occurring condition within the FXS phenotype (Klusek, Martin, et al., 2015; Roberts et al., 2020; Wolff et al., 2012). Recent estimates suggest the ASD co-occurrence rate is approximately 60.7% in preschoolers with FXS (Roberts et al., 2020), with other estimates ranging from 30–54% (Kaufmann et al., 2017; Klusek, Martin, et al., 2015). Because FXS accounts for approximately 1 – 6% of cases of ASD (Kaufmann et al., 2017), the nature of this co-occurrence is relatively well investigated apart from the exploration of any compounded developmental effects from infancy through early childhood that may arise in the context of co-occurring ASD in FXS (Kaufmann et al., 2017; Klusek, Martin, et al., 2015; Roberts et al., 2020).

Children with FXS who develop ASD (FXS+ASD) typically experience developmental differences resulting in worse outcomes across measures of cognition and adaptive function relative to children with FXS without ASD (FXS-Only) (Caravella & Roberts, 2017; Roberts et al., 2020). Thus, it appears the co-occurrence of ASD introduces additional neurodevelopmental vulnerability in children with FXS, and motor abilities may be one particularly salient area involved in compounded developmental outcomes for children with FXS+ASD. For example, differences in motor development between infants with FXS and FXS+ASD are evident prior to 12 months of age (18-months when accounting for cognitive differences) on both parent-report and direct assessment measures (Will et al., 2019). Further, both gross and fine motor skills develop at a significantly slower rate for infants with FXS+ASD relative to those with FXS-Only, even when controlling for cognitive ability (Will et al., 2019; Zingerevich et al., 2009). Given that motor abilities and their rate of development are implicated in the emergence of communication (Iverson, 2021; LeBarton & Iverson, 2016; Yu & Smith, 2012), the compounding neurodevelopmental vulnerability of ASD that impacts motor development in FXS (Will et al., 2019) is likely to have a differential effect on communication within FXS.

Communication and Motor Ability in FXS

Children with FXS experience difficulties with communication – which encompasses language and social communication – regardless of whether co-occurring ASD is present (Hinton et al., 2013). Such difficulties include overall delays in language and communication development (Roberts et al., 2001, 2002; Sterling & Warren, 2008), lower receptive and expressive communication skills relative to neurotypical controls (Will et al., 2018), and atypical social communication (Hahn et al., 2017; Klusek, Roberts, et al., 2015). Because social communication impairments are a diagnostic feature of ASD (APA, 2013; DSM-5), children with FXS+ASD clearly display greater differences with this aspect of communication relative to those with FXS-only. However, further evidence suggests that communication and language are more generally affected in the context of co-occurring ASD in FXS. For instance, children with FXS+ASD display lower rates of communication skills across early development relative to children with FXS-only (Caravella & Roberts, 2017); yet the developmental factors contributing to differential outcomes remain unclear.

Motor development is one potential factor that may contribute to differences in communication outcomes between children with FXS-only and those who develop FXS+ASD. Timely motor skill achievement appears to exert a cascading influence on communication, and evidence suggests this cascade spans from infancy through early childhood (Heiman et al., 2019; Iverson, 2021; LeBarton & Iverson, 2016). This link has been firmly established in neurotypical development (Needham & Libertus, 2011; Walle & Campos, 2014) and young children with an elevated likelihood of developing ASD (i.e., younger siblings of children with ASD; (Bhat et al., 2012; Bradshaw et al., 2018; LeBarton & Iverson, 2013; West, 2019). For instance, early motor movements emerge alongside reduplicative babbling (Iverson, 2021), and more advanced motor skills expand infants’ experiential landscape affording greater learning opportunity essential for language and communication development (Libertus & Violi, 2016; Pereira et al., 2014; Yu & Smith, 2012). Specifically, acquisition of motor skills like grasping, sitting, and walking facilitate new possibilities for exploration and increase opportunities for more complex social interactions, facilitating communication and language development (Libertus & Violi, 2016; Walle & Campos, 2014; West & Iverson, 2017; Yu & Smith, 2012). As such, disruptions in the developmental timing of motor skill acquisition may substantially affect the developmental process that contributes to communication outcomes. The degree of motor delays and protracted rate of development in FXS (Caravella & Roberts, 2017; Hinton et al., 2013) provide a precarious foundation from which the cascade to communication outcomes is initiated, and one that may be further compromised in the context of co-occurring ASD in FXS (Will et al., 2019). Delineating potential cascading effects of variable motor development as a function of ASD can improve intervention timing and efficacy, possibly mitigating the compounding effects of additional neurodevelopmental risk in FXS resulting from co-occurring ASD.

Present Study

With little-to-no evidence on the longitudinal association between motor skill acquisition and communication outcomes in FXS, the present study aimed to address these gaps. Our primary objective was to characterize the developmental association between early gross and fine motor abilities and their rate of development and receptive and communication outcomes in FXS. Further, we aimed to determine whether these associations varied between infants with FXS that developed co-occurring ASD (FXS+ASD) from those that did not (FXS-only). We anticipated that, because of the lesser extent of delays, more developmental connections between early motor and communication outcomes would emerge in FXS-only, whereas more associations would emerge between the rate of motor development and communication for those with FXS+ASD. Given prior evidence, we also anticipated that gross motor would support expressive communication, whereas fine motor would support receptive communication (Will & Roberts, 2021), but that these associations would occur in both groups.

Methods

Participants

Data were drawn from a larger ongoing prospective longitudinal study focused on characterizing the emergence of ASD in children with FXS. As part of the larger study, participants completed assessments that included measures of overall developmental ability, temperament, and ASD. Participants for this study included 51 children with FXS – 23 children with FXS-only (mean chronological age = 13.90 months at initial enrollment) and 28 children with co-occurring FXS+ASD (mean chronological age = 18.43 months at initial enrollment). Groups did not significantly differ on grand mean chronological age (p = 0.16). Across all participants, there was a total of 247 observations, with 119 in the FXS-only group and 128 in the FXS+ASD group. FXS diagnosis was confirmed through genetic reports and co-occurring ASD diagnosis was determined by our team using a clinical best estimate (CBE) procedure (see below; Table 1; Roberts et al., 2020; Will et al., 2019).

Table 1.

Participant characteristics

All
n = 51		 FXS+ASD
n = 28		 FXS-Only
n = 23
Sex (male), n(%) 37 (73%) 24 (86%) 13 (57%)
Age at enrollment (months), M(SD) 16.39(12.62) 18.43(13.40) 13.90(11.39)
NVDQ at enrollment, M(SD) 69.29(24.24) 67.89(19.77) 71.19(29.80)
Gross Motor at enrollment M(SD) 12.13(5.23) 13.18(5.07) 10.78(5.32)
Fine Motor at enrollment M(SD) 12.98(7.60) 13.00(7.02) 12.94(8.49)
Race/Ethnicity, n(%)
 American Indian/Alaska Native 2 (4%) 1 (3.67%) 1 (4.40%)
 Black 3 (6%) 1 (3.66%) 2 (9%)
 White Non-Hispanic 36 (70%) 1 (3.67%) 15 (65.20%)
 White Hispanic 1 (2%) 21 (75%) 0 (0%)
 More than one Race Non-Hispanic 8 (16%) 4 (14%) 4 (17%)
 More than one Race Hispanic 1 (2%) 0 (0%) 1 (4.40%)
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Measures

Motor abilities.

The Mullen Scales of Early Learning (MSEL; Mullen, 1995) is a standardized developmental assessment designed for children ages 0–68 months that measures skill progression in the areas of motor ability (fine and gross motor skills), visual reception, and communication (expressive and receptive language skills). Fine Motor and Gross Motor raw scores were used as indicators for each of these scales as representative of early motor foundations and rate of change in motor abilities from 9 – 60 months. The visual reception age equivalent score was used to derive a nonverbal developmental quotient (NVDQ) and included as a covariate in regression models. The MSEL was collected at each assessment to capture developmental ability. Due to the shared variance across domains of the MSEL by virtue of being from the same measure and factoring into the Early Learning Composite score, we elected to use parent-reported communication as outcome variables rather than the language domains from the MSEL.

Communication.

The Vineland Adaptive Behavior Scales, 2nd Edition (Sparrow et al., 2005) is a norm-based clinical parent/caregiver interview that measures adaptive functioning in individuals ages 0–90 years in the areas of Communication, Daily Living, Socialization, and Motor Skills. Each item is scored according to the frequency with which an individual performs a task according to caregiver report (‘0’ for Never; ‘1’ for Sometimes or Partially; and ‘2’ for Usually). For the current study, Receptive and Expressive Communication raw scores were used as dependent variables in the respective models. Raw scores were selected because floor effects with standardized scores are common in populations with intellectual and developmental disabilities (e.g., FXS). The VABS-II was administered at each assessment to contextualize adaptive functioning in relation to overall developmental ability. Receptive and Expressive Communication scores were selected from the last assessment, which was approximately 60 months of age. Use of the VABS-II Communication domains as primary outcome variables was intended to circumvent issues related to shared measurement variance that would arise from having predictors and outcomes from the same measure (e.g., MSEL).

Autism symptomatology and diagnosis.

The Autism Diagnostic Observation Schedule-2nd Edition (ADOS-2; Lord et al., 2012) is a structured observational assessment for ages 12 months through adulthood that uses play-based activities to measure social communication and repetitive behaviors that are characteristic of core ASD domains. The ADOS-2 was administered at each assessment starting at 24-months and older. The ADOS-Toddler Module was administered at 24-month assessments, followed by Modules 1 – 2 at subsequent ages as appropriate based on language level per the ADOS-2 manual. Because of language limitations inherent to FXS, only two participants received a Module 3, and this was at their 60-month assessment. In addition, the Autism Diagnostic Interview-Revised (ADI-R; Rutter et al., 2013), a standardized clinical caregiver interview, was also administered to capture the presence and severity of co-occurring ASD. The ADI-R measures developmental history and features of ASD across core domains of social affect/communication and restricted and repetitive behaviors. For the present study, the ADI-R was collected at 36- and 60- months old. These measures, in addition to measures of cognitive and adaptive abilities, were included in CBE procedures to determine presence or absence of co-occurring ASD (described below).

Procedures

All study procedures were approved by the Institutional Review Board at the University of South Carolina. Participants were recruited through local and national FXS specialty clinics and through parent groups on social media. Participants were assessed either in their homes or on the University of South Carolina campus, depending on family preference. While some participants were enrolled in the study as young as 6 months old, the target enrollment age was approximately 9 months, with follow up assessments at regular intervals (i.e., 9, 12, 24, 36, 48, and 60 months) through age 5. Participants completed standardized developmental assessments and semi-structured behavioral assessments designed to measure ASD symptomatology. Parents completed survey questionnaires and structured interviews on their child’s development and behavior. On average, assessments lasted approximately 2 – 6 hours, depending on age, and were distributed across multiple sessions as appropriate. Families received monetary compensation and a report on their child’s development in return for participating in the study.

Full case reviews were conducted following each assessment starting at 24-months to determine ASD diagnostic status per CBE procedures. Case reviews for CBE diagnoses included results from standardized developmental and adaptive behavior assessments, ADI-R scores, ADOS-2 scores, review of video segments, and overall clinical impressions. Diagnostic impressions were determined and agreed upon by the examiner present at the assessment, a licensed psychologist and certified ADOS-2 trainer, and a third team member following each full case review. In the event of disagreement, a full review of the ADOS-2 video was completed, the full case review was revisited, and consensus was reached across the research team. If data were unavailable at 36 months, CBE procedures were employed at 48- and/or 60-months. For the present study, if data were unavailable at any of these assessments, CBE diagnoses from 24-months were used.

This study did not include involvement from community members beyond informal feedback from caregivers during and after assessments, and therefore, did not provide any direct benefit to the community or government.

Analytic Approach

The analytic approach to determine the influence of early motor skills and the rate of change in motor development on communication outcomes was two-fold. First, we estimated random intercepts and random slopes multilevel models with observations nested within participant and motor skills regressed on age. We centered age at 9-months for the initial trajectory models to achieve trajectories that spanned the targeted study ages (i.e., 9 – 60-months) and because data were somewhat sparse at the youngest age of enrollment (i.e., 6-months). Models were estimated across a total of 247 observations (i.e., 119 in the FXS-only group; 128 in the FXS+ASD group). Individual intercepts and individual slopes of gross and fine motor abilities estimated from these unconditional models were retained and used as predictors of receptive and expressive communication outcomes in multiple linear regression models. Due to model complexity and modest sample sizes, we estimated separate models for each group with each communication outcome (i.e., receptive, or expressive) regressed on each type of motor ability (i.e., gross, or fine). This approach also reduced the overall number of models while maximizing statistical power. To account for potential effects of cognitive ability, NVDQ was used as a covariate in all regression models.

Results

Figure 1 depicts longitudinal trajectories for gross motor and fine motor scores across groups from infancy through 60 months. Intercepts and slopes from these models were used as predictors of communication outcomes in each regression model.

Figure 1.

Figure 1.

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Longitudinal motor trajectories across groups

Full regression model coefficients are provided in Table 2.

Table 2.

Regression Model Results

Gross Motor
Receptive Communication Expressive Communication
FXS-Only b SE(b) p 95% CI b SE(b) p 95% CI
lower upper lower Upper
Intercept 23.89 19.27 .219 −14.44 62.22 −197.46 56.54 <.001 −309.89 −85.03
Early Gross Motor 0.90 0.44 .044 0.03 1.77 7.27 1.29 <.001 4.71 9.84
Rate of Gross Motor −25.09 21.98 .257 −68.80 18.62 214.10 64.48 .002 85.87 342.32
NDVQ 0.12 0.04 .002 0.04 0.19 0.35 0.11 <.001 0.14 0.56
FXS+ASD b SE(b) p 95% CI b SE(b) p 95% CI
lower upper lower upper
Intercept −21.00 6.37 .001 −33.65 −8.35 −33.20 15.84 .039 −64.66 −1.74
Early Gross Motor 2.43 0.50 <.001 1.44 3.41 2.38 1.23 .056 −0.07 4.83
Rate of Gross Motor 10.20 5.21 .053 −0.16 20.56 36.38 12.97 .006 10.62 62.14
NDVQ 0.15 0.04 <.001 0.07 0.23 0.39 0.10 <.001 0.19 0.59
Fine Motor
Receptive Communication Expressive Communication
FXS-Only b SE(b) p 95% CI b SE(b) p 95% CI
lower upper lower upper
Intercept 0.17 3.47 .962 −6.72 7.05 −43.17 13.92 .002 −70.82 −15.52
Early Fine Motor 3.76 0.34 <.001 3.08 4.44 8.22 1.37 <.001 5.50 10.94
Rate of Fine Motor −40.05 7.06 <.001 −54.08 −26.02 12.59 28.38 .658 −43.77 68.96
NDVQ 0.02 0.03 .448 −0.03 0.06 0.08 0.11 .481 −0.14 0.30
FXS+ASD b SE(b) p 95% CI b SE(b) p 95% CI
lower upper lower upper
Intercept −33.45 5.52 <.001 −44.41 −22.50 −42.12 16.35 .001 −74.56 −9.69
Early Fine Motor 3.69 0.66 <.001 2.38 4.99 2.77 1.95 .158 −1.09 6.63
Rate of Fine Motor 52.82 8.04 <.001 36.89 68.76 161.96 23.80 <.001 114.74 209.17
NDVQ −0.06 0.03 .038 −0.12 −0.00 −0.03 0.08 .666 −0.19 0.12
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Gross Motor Models

Figure 2 depicts associations between gross motor abilities and communication outcomes across groups. Early gross motor (i.e., intercept) significantly predicted receptive communication outcomes for both children with FXS-only (b = 0.90; p = .044) and children with FXS+ASD (b = 2.43; p < .001) controlling for NVDQ. The effect of rates of gross motor development (i.e., slope) on receptive communication, were similar across groups and no significant associations were identified for the FXS-only group (b = −25.09; p = .257), or the FXS+ASD group (b = 10.20; p = .053).

Figure 2.

Figure 2.

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Associations between gross motor and communication outcomes across groups

In terms of expressive communication, early gross motor (b = 7.27; p < .001) and the rate of gross motor development significantly predicted outcomes for children with FXS-only (b = 214.10; p = .002) controlling for NVDQ. For children with FXS+ASD, the association between early gross motor and expressive outcomes did not reach statistical significance (b = 2.38; p = .056), whereas the rate of gross motor development significantly predicted expressive communication outcomes (b = 36.38; p = .006) controlling for NDVQ.

Fine Motor Models

Figure 3 depicts associations between fine motor and communication outcomes across groups. Robust patterns of association between fine motor and communication outcomes were identified across groups. Specifically, early fine motor (i.e., intercept) significantly predicted receptive communication outcomes for both children with FXS-only (b = 3.76; p < .001) and those with FXS+ASD (b = 3.69; p < .001). Likewise, the rate of fine motor development (i.e., slope) significantly predicted receptive communication outcomes for children with FXS-only (b = −40.05; p < .001), and those with FXS+ASD (b = 52.82; p < .001).

Figure 3.

Figure 3.

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Associations between fine motor and communication outcomes across groups

Differential associations specific to fine motor and expressive communication outcomes were identified across groups. Early fine motor significantly predicted expressive communication outcomes for children with FXS-only (b = 8.22; p < .001), but not for those with FXS+ASD (b = 2.77; p = .158). Conversely, the rate of fine motor development (i.e., slope) did not significantly predict expressive communication outcomes for children with FXS-only (b = 12.59; p = .66) but did for children with FXS+ASD (b = 161.96; p < .001).

Discussion

Our study examined the impact of gross and fine motor abilities at 9-months of age, and the rate of change in motor abilities from 9 – 60 months on communication outcomes in FXS and is among the first to evaluate these developmental associations in FXS. We also investigated whether there were differential effects across these developmental associations as a function of within-FXS heterogeneity resulting from co-occurring ASD. Consistent with extant literature in neurotypical and elevated ASD likelihood populations, early motor abilities (gross and fine) were associated with receptive and expressive outcomes for children with FXS-Only. Differential patterns in these developmental associations were identified in the context of co-occurring ASD. Specifically, early motor abilities, rather than rates of motor skill acquisition, were less predictive of some communication outcomes for infants with FXS who developed ASD. In contrast, early motor abilities, rather than rates of motor acquisition, appeared to have a greater effect on communication outcomes for infants with FXS-Only. However, regardless of co-occurring ASD, fine motor skills emerged as a robust predictor of receptive communication outcomes in FXS. These findings establish a developmental link between early motor skills and the rate of motor development on communication outcomes in FXS and identify the potential impact of early motor delays in the context of co-occurring ASD in FXS, as well as in FXS more broadly. Collectively, these findings suggest that intervention to support timely motor skill acquisition may mitigate the developmental consequences of co-occurring ASD on communication outcomes for children with FXS.

Gross Motor

The corpus of research on the effect of motor abilities on communication outcomes primarily emphasizes the role of gross motor abilities. This evidence is compelling in that acquisition of gross motor skills – independent sitting, cruising, and walking – translates to the most salient changes in an infant’s access to the environment. These newly afforded visual and locomotive experiences facilitate the expansion of language and communication by eliciting greater input and freeing an infant’s hands to show objects and use gestures for communication (Smith et al., 2011). Our findings substantiate this connection between gross motor abilities and communication outcomes evident in neurotypical and elevated ASD-likelihood infants (Heiman et al., 2019; LeBarton & Iverson, 2013; Libertus & Violi, 2016) in infants with FXS, but with some subtle differences.

Primarily, gross motor abilities at 9-months old were significantly associated with both receptive and expressive outcomes for children with FXS-Only. These findings parallel extant work in the context of expressive skills while providing new evidence for the role of gross motor abilities in receptive outcomes, which has been less well-studied, particularly in neurogenetic groups (Bishop et al., 2016). In a cross-sectional study examining these developmental associations in toddlers with FXS, gross motor was significantly associated with both receptive and expressive communication (Will & Roberts, 2021). However, these findings were limited in that the rate of gross motor development as a predictor of long-term communication outcomes in FXS was unexamined, as was these associations in the context of co-occurring ASD. The present findings provide further support for the developmental associations between gross motor development and expressive communication outcomes (LeBarton & Iverson, 2013) and extend this evidence to FXS regardless of the co-occurrence of ASD. Our findings also suggest, however, that gross motor development may play less of a role in receptive outcomes. That is, despite a substantial association between early gross motor and receptive and expressive communication outcomes across both groups, the rate of gross motor development did not significantly predict receptive communication outcomes for the FXS-Only group, and only trended towards significance for the FXS+ASD group. It may be the case that receptive skills are impaired to the extent that additional exploratory opportunity afforded through gross motor skill acquisition provides little-to-no expansion of receptive skills in FXS regardless of co-occurring ASD.

Children with co-occurring FXS+ASD evidence greater gross motor delays than those without co-occurring ASD, even when controlling for overall cognitive differences (Hinton et al., 2013; Will et al., 2019). Our results illustrated in Figure 1, along with prior evidence (Will et al., 2019), identify a slower rate of motor development for children with FXS+ASD relative to FXS-Only across early childhood. This protracted emergence of gross motor abilities evident in FXS+ASD may translate to greater attenuation of the effect of early gross motor skills on expressive language outcomes relative to those with FXS-Only. Interestingly, we found that early gross motor skills predicted receptive but not expressive outcomes, whereas the rate of gross motor development predicted expressive but not receptive communication outcomes for children with FXS+ASD. The more substantial gross motor delays evident in children with FXS+ASD may account for these discrepant patterns across early gross motor skills and the rate of gross motor acquisition on communication outcomes. Further, the extensive motor delays identified in children with FXS+ASD and, thereby, the consequential inability to shift their exploratory context may elicit more verbal input from caregivers, resulting in greater support for the emergence of receptive skills with less opportunity for expressive skills. As children with FXS+ASD advance in their gross motor development, the effect on communication abilities may transfer to expressive skills as typically would be expected, given evidence in other (elevated ASD-likelihood) populations. Future work should examine how the environmental context – such as environmental language exposure or communicative opportunity – may impact the association between gross motor and communication outcomes in FXS in the context of ASD.

Fine Motor

Overall, less is known regarding the role of fine motor abilities on communication outcomes, particularly in neurogenetic populations like FXS. However, considerable evidence highlights object manipulation as a critical event for language learning, and therefore, subsequent communication abilities. Neurotypical infants receive caregiver object and action labels when holding and manipulating objects (Pereira et al., 2014; Smith et al., 2011; Yu & Smith, 2012, 2017), and infants’ ability to map this input to their object-related experiences facilitates language and related communication development. Further, these dyadic experiences provide opportunities to learn and practice communications skills like gesture use, shared affect, and requesting in addition to language acquisition. Present study results suggest this developmental process is supported in FXS, regardless of co-occurring ASD.

However, the associations between fine motor abilities and communication outcomes in FXS did appear differentially affected in the context of co-occurring ASD. Despite a consistent association between early fine motor and its rate of growth with receptive communication, the direction of effects was in divergent directions across FXS-Only versus FXS+ASD. Specifically, for children with FXS-only, decelerated, or slower rates of fine motor development between 9 – 60 months significantly predicted receptive communication skills, whereas increased rates of fine motor development predicted these outcomes for those with FXS+ASD. The overall slower rates of fine motor development in those with non-syndromic ASD (West, 2019) and those with FXS+ASD (Will et al., 2019) could account for this potentially unexpected difference in direction of effect. It may be the case that infants with FXS-Only possess a foundational fine motor repertoire sufficient for supporting communication outcomes, requiring less support in from rates of fine motor development over time. Conversely, with lower fine motor abilities in early development (Will et al., 2019), children with FXS+ASD are faced with a delayed emergence in their foundational repertoire, and a steeper “catch up” process in their fine motor acquisition or rate of growth. These developmental constraints on fine motor abilities may account for the association between increased rates of fine motor growth and receptive communication outcomes evident in children with FXS+ASD but not those with FXS-Only.

Additional opposite effects were identified in the context of FXS+ASD. Specifically, early fine motor was also associated with expressive outcomes for infants with FXS-Only, but not infants who went on to develop FXS+ASD. Infants with FXS who developed ASD demonstrated significant associations between the rate of fine motor development and expressive outcomes, whereas those with FXS-Only did not. Again, evident differences in the early fine motor abilities and their rate of development between children with FXS-Only and those with FXS+ASD (Will et al., 2019) likely account for these differential effects on communication outcomes, at least to some extent. Overall, a more impaired motor system in early development that appears to accompany co-occurring ASD in FXS may contribute to challenges with incorporating expressive skills into a communication repertoire. It may also be the case that certain expressive communication skills supported by early fine motor abilities, such as gesture use, are similarly compromised across idiopathic ASD and FXS+ASD, yet somewhat intact in FXS-Only. Alternatively, additional mechanisms that contribute to communication development may facilitate differential developmental processes in children with FXS with and without ASD.

Other contributing mechanisms

By diagnostic definition, ASD is characterized by social communication impairments, so differences in aspects of communication between co-occurring ASD in FXS versus FXS-only are somewhat expected. However, characteristics specific to co-occurring ASD cannot fully account for the differences in the associations between motor development and communication outcomes we identified. As such, there are likely additional contributing factors that may differentially mediate these associations in the context of co-occurring ASD (Bruyneel et al., 2019).

Early motor abilities also serve as developmental underpinnings for executive cognitive skills (Needham et al., 2002; Needham & Libertus, 2011; Smith, 2010), including attention, working memory, inhibition, and cognitive flexibility (Diamond, 2013; Miyake et al., 2000; Miyake & Friedman, 2012). Substantial evidence highlights disruptions in these executive functions in populations that experience a greater likelihood of atypical neurodevelopmental outcomes, including ASD (St. John et al., 2016) and FXS (Schmitt et al., 2019). When examining potential foundational mechanisms of these executive cognitive skills, motor abilities have emerged as critical factors across multiple studies and conditions (St. John et al., 2016; Will, 2021). More specifically, in infants with elevated likelihood for developing ASD, motor skills significantly predicted later aspects of executive cognitive skills on A-not-B reversal trials (St. John et al., 2016), which recruit inhibition, along with working memory, shifting, and sustained attention (Miyake et al., 2000; Zelazo et al., 1997). Although effects differed across motor type – gross versus fine motor – and level of ASD features, significant effects were identified between gross and fine motor, and working memory (St. John et al., 2016), supporting the role of motor abilities in critical cognitive functions. Similar executive function impairments characterize higher-order cognition in FXS as well. Aspects of working memory, including the rate of development, are impaired in children with FXS relative to neurotypical development (Schmitt et al., 2019). Because working memory is utilized in statistical learning for vocabulary growth and encoding information into symbolic representations used in language and communication (Yu & Smith, 2012), impairments in working memory must coalesce with other executive difficulties in FXS, including decreased sustained attention and cognitive flexibility, to affect learning opportunities central to language and communication.

These difficulties may affect specific learning opportunities, such as those provided during joint attention, to a greater extent in FXS in the context of ASD (i.e., FXS+ASD). Joint attention – shared attention with a social partner around an object or event – is a well-established mechanism through which language is mapped and communication exchanged between infants or toddlers and their social partners (Bruyneel et al., 2019). As this skill requires sustained attention and cognitive flexibility to easily shift attention between the social partner and the object or event, it may additionally mediate the pathway from motor development to communication outcomes. Infants with FXS receive greater support in jointly shared exchanges and show lower rates of shared engagement with caregivers, which may affect the ability to acquire early language and communication skills (Brewe et al., 2018; Hahn et al., 2016). This developmental process may be more impacted in the context of co-occurring ASD and FXS (Bruyneel et al., 2019; Dawson et al., 2004; Mundy & Sigman, 1989). However, within-syndrome differences in joint attention abilities in the context of co-occurring FXS+ASD have been minimally investigated (but see Wolff et al., 2012), particularly regarding the potential effect on developmental outcomes. Early motor difficulties are liable to initiate a developmental cascade in which executive cognitive skills and joint attention abilities interact to affect communication outcomes in FXS with and without the cooccurrence of ASD. With limited longitudinal studies on FXS, particularly in early development, future efforts should aim to further delineate this potential developmental cascade.

Strengths and Limitations

Our study characterized the effect of early motor abilities and the rate of motor development on communication outcomes in children with FXS and is among the first to examine these associations in FXS. One major strength of our study was the inclusion of longitudinal data on both gross and fine motor abilities from infancy through five years old. This study provides much-needed longitudinal evidence on developmental processes and outcomes affected by delays that emerge during infancy. Our study did, however, include parent-reported communication abilities as the primary outcomes, and direct observation communication abilities may provide a more comprehensive profile of these developmental associations in FXS. Accordingly, future studies should aim towards replication with direct assessment communication profiles. Another strength of our study was the rigorous approach to determining co-occurring FXS+ASD (Roberts et al., 2020), which potentially advances the accurate understanding of within-syndrome variation in FXS as a function of ASD. Further, our study included a relatively large (n = 51) and comprehensive sample of children with FXS. While this approach yields information on the entire FXS phenotype, the small number of females within the total sample (n = 14) proved prohibitive in examining sex differences or sex-specific developmental associations between motor and communication as a function of ASD in females with FXS. Although models were tested with males only and yielded virtually the same pattern of results, the lack of specific results on sex effects is ultimately a limitation of the study that future work should aim to address. Likewise, models as specified did not directly test group differences, rather evaluated differential patterns of associations as a means to maximize statistical power. Future work should aim for replication across direct group comparisons for maximum insight into these associations and variation in the context of co-occurring ASD. Finally, that examining specific mechanisms of executive dysfunction and joint attention was beyond the scope of this study is a minor limitation that invites further investigation.

Conclusions

Our study examined the effects of impaired gross and fine motor development on receptive and expressive communication outcomes in FXS. We captured within-syndrome variability in these developmental associations as a function of co-occurring ASD. Our results identify similar developmental processes in some respects, fine motor as a robust predictor of receptive communication across FXS, as well as differences in the context of co-occurring ASD, which included aspects of motor and expressive communication outcomes. Characterizing developmental cascades and their variation reflected in the FXS within-syndrome heterogeneity in these developmental processes provides needed evidence to consider targeted interventions for all children with FXS.

Acknowledgements:

We would like to thank all the families that participated in this research. We greatly appreciate feedback from Drs. Jordan Wickstrom and Audrey Thurm on early drafts of this manuscript. This work was supported by the National Institutes of Health through the following awards: 1F32HD097877-01 (PI: Will); 1K99HD105980-01 (PI: Will); L40MH117727 (PI: Will); 2R01MH90194, R01MH107573 (PI: Roberts).

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