Senior Seminar - Beyond the Two-Factor Model of the ASD Diagnostic Criteria

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REVIEW

CURRENTOPINION Motor development and delay: advances in assessment of motor skills in autism spectrum disorders

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a b b

Rujuta B. Wilson , Peter G. Enticott , and Nicole J. Rinehart

Purpose of review

Motor impairments in neurodevelopmental disorders, specifically autism spectrum disorder (ASD), are prevalent and pervasive. Moreover, motor impairments may be the first sign of atypical development in ASD and likely contribute to abnormalities in social communication. However, measurement of motor function in ASD has lagged behind other behavioral phenotyping. Quantitative and neurodiagnostic measures of motor function can help identify specific motor impairments in ASD and the underlying neural mechanisms that might be implicated. These findings can serve as markers of early diagnosis, clinical stratification, and treatment targets.

Recent findings

Here, we briefly review recent studies on the importance of motor function to other developmental domains in ASD. We then highlight studies that have applied quantitative and neurodiagnostic measures to better measure motor impairments in ASD and the neural mechanisms that may contribute to these abnormalities.

Summary

Information from advanced quantitative and neurodiagnostic methods of motor function contribute to a better understanding of the specific and subtle motor impairments in ASD, and the relationship of motor function to language and social development. Greater utilization of these methods can assist with early diagnosis and development of targeted interventions. However, there remains a need to utilize these approaches in children with neurodevelopmental disorders across a developmental trajectory and with varying levels of cognitive function.

Keywords

autism spectrum disorder, motor control, motor function

aUCLA Semel Institute of Neuroscience and Human Behavior, David Geffen School of Medicine, UCLA Division of Pediatric Neurology, Los Angeles, California, USA and bDeakin Child Study Centre, School of Psychology, Faculty of Health, Deakin University, Geelong, Victoria, Australia

Correspondence to Rujuta B. Wilson, MD, 760 Westwood Plaza, Room A7-420, Los Angeles, CA 90095, USA. Tel: +1 310 825 1746; fax: +1 310 206 4245; e-mail: [email protected]

Curr Opin Neurol 2018, 31:134–139

DOI:10.1097/WCO.0000000000000541

INTRODUCTION

The development of the motor system is critical for an individual to engage with the environment. As a child gains the ability to crawl, point, and ambulate, new opportunities arise for social interactions with caregivers and peers [1]. Neurodevelopmental disor- ders (NDDs) are a heterogeneous group of conditions that are characterized by delays or abnormalities in a variety of developmental domains, including delays in motor skills [Diagnostic and Statistical Manual of Mental Disorders Fifth Edition (DSM-5)]. Within the group of NDDs, autism spectrum disorder (ASD) is diagnosed based on core impairments in social com- munication skills. However, motor impairments are particularly prevalent in ASD, and they can be the first sign of atypical development [2,3]. With advan- ces in genetic testing, there has also been an increased identification of copy number variants and single gene disorders that confer elevated risk for ASD

[4,5 ]. Motor impairments are often the first sign of abnormal development in these genetic variants and may be more common in children with syn- dromic forms of ASD [5

,6]. Thus, the identification of early motor delays might be indicative of an indi- vidual at higher risk for a genetic disorder. Despite their clinical relevance, quantification of motor skills in ASD has been hampered by the use of standardized

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KEY POINTS

� Motor impairments are prevalent in autism spectrum disorder and are related to overall development.

� Quantitative measures of motor function can aid in identifying specific and subtle motor impairments in ASD.

� Neurodiagnostic measures of motor function can better elucidate aberrant underlying neural mechanisms contributing to motor impairments in ASD.

� Early identification of motor impairments in ASD can aid in early intervention and improved long term functioning.

Autism spectrum disorders Wilson et al.

assessments that mostly capture developmental mile- stones and rely on an individual’s ability to under- stand complex tasks [7,8]. These assessments often lead to results that do not adequately capture a child’s motor abilities or impairments. This has led research- ers to develop and utilize quantitative measures of motor function to better identify motor impairments in ASD to aid in earlier diagnosis and development of individualized interventions. In this review, we briefly discuss new findings on the relationship between motor skills, core ASD features, and cogni- tive function, and then review recent advances in quantitative and measures of motor function in ASD.

RELATIONSHIP OF MOTOR FUNCTION TO OTHER DEVELOPMENTAL DOMAINS

The development of motor function is linked to a child’s capacity for language, cognitive, and social development, and may serve as an indication of emer- gent developmental psychopathology [1,9]. Retro- spective studies of infants at high risk for ASD or with a confirmed diagnosis of ASD report the emer- gence of motor impairments before the more salient social-communicative impairment has been formally diagnosed. It is well accepted that early emergence of motor impairments has a downstream impact on key aspects of social and communicative development, for example, impairing a child’s ability to gesture, and interact with other children in play [1,2,10].

Longitudinal studies reveal that the connection between motor, language, and higher-level cogni- tive impairment continues into childhood. In the school-age period, when children may experience higher developmental demands, studies have shown a relationship between motor impairments and disturbances in emotional and behavioral func- tioning, as measured on the Developmental Behav- ior Checklist. One explanation for this association is

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that children who experience greater motor prob- lems may experience more adverse life events, for example, being excluded from school yard games and more trouble with academic tasks such as hand- writing, thus leading to the higher levels of psycho- pathology [11].

A recent study on high-risk infant siblings (defined by having a sibling with ASD) examined whether advances in sitting, and also prone loco- motion, are related to communicative development [12

]. This longitudinal study included 37 high-risk infants, with gross motor skills assessed at monthly intervals from 5 to 14 months using the Alberta Infant Motor Scale (AIMS), which is a standardized observational measure of prone postures utilized in sitting and locomotion [13]. The age of onset of verbal and nonverbal communication was also recorded. Motor delays were observed across all observations, with the majority of participants exhibiting delays by 5 and 6 months of age. Motor development recorded monthly on the AIMS was related to emergence of both verbal and nonverbal communicative milestones. As the authors hypoth- esized, the ability to sit unsupported relates to both verbal (reduplicative babbling) and nonverbal com- munication (show gesture onset), whereas prone locomotion related to nonverbal communication milestones (show and point gesture). The authors state that acquiring independent sitting increases the use of manual movements to engage with people and also allows an infant to coordinate behaviors, such as eye contact with multiple individuals [12

]. Therefore, in addition to the relationship of motor skills with other domains (such as language and communication), developments in gross motor skills can serve as the building blocks for more complex social and behavioral interactions. More- over, there can be lifelong implications if motor development is disrupted.

Another study that evaluated high-risk infant siblings (defined as having a sibling with ASD) examined the relationship between motor skills and executive functioning, which is a set of higher-level cognitive functions including atten- tion, working memory, and planning. This study compared the relationship of motor skills and exec- utive functioning in high-risk infants (both those who went on to receive an ASD diagnosis and those who did not) and low-risk infants (defined as a child without a sibling or family history of ASD) at 12 and 24 months of age. Motor function was assessed using the Mullen Scales of Early Learning (MSEL) – a standardized measure of cognitive development for children from birth to 68 months [14]. Although no group differences were seen at 12 months, at 24 months, all high-risk infants demonstrated worse

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working memory and response inhibition compared to low-risk infants. In addition, in all groups, worse gross motor skills were associated with worse response inhibition [15

]. The mounting research evidence connecting

early motor impairment to poorer global develop- mental outcomes for children at high risk for ASD supports the importance of better understanding motor impairments that might be specific to ASD and when these impairments emerge. Given the heterogeneity of ASD and the discovery of genetic syndromes highly penetrant for ASD, quantitative and neurodiagnostic measures of motor may shed light on the individual variability of motor function in these disorders.

QUANTITATIVE MEASURES OF MOTOR FUNCTION IN AUTISM SPECTRUM DISORDER

Quantitative tools of motor function often use kinetic and kinematic analysis to capture specific spatiotemporal variables of motor function (e.g. gait analysis, three-dimensional motion capture analy- sis, digitized tablets). ‘Kinetics’ refers to the study of forces that cause motion such as torque, gravity, and friction. ‘Kinematics’ is the study of movement such as displacement in time and velocity. These tools have identified gross and fine motor impairments that differentiate individuals with ASD from other groups [16,17,18

] Motor impairments in ASD are often present

beyond early childhood and can affect both gross and fine motor domains such as balance and manual dexterity [3]. These persistent deficits can affect school-based activities, which can influence cogni- tive and academic performance. For example, mea- sures of handwriting ability can shed light on multiple motor domains, such as grip strength and manual dexterity, and they provide useful infor- mation on a frequently employed school-based activity. A recent study utilized an advanced quan- titative digitized tablet to evaluate kinematic varia- bles of handwriting (tortuosity, speed, size) and its relationship to attention and ASD core symptomol- ogy in school-aged children with ASD. The task was designed to minimize additional cognitive and lin- guistic processes, which can confound studies of ASD [19

]. Participants were also evaluated using the Movement Assessment Battery for Children-2 (MABC-2), a standardized measure of motor func- tion examining three domains – manual dexterity, balance, and aiming and catching [20]. Three main findings were highlighted in the study: caregiver report indicated greater handwriting difficulties in children with ASD compared to typically developing

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age-matched peers; handwriting performance in the ASD group was characterized by significantly poorer writing quality and speed; and greater severity of ASD, attention, and motor symptoms were corre- lated with reduced handwriting performance and greater difficulties in functional handwriting perfor- mance [19

]. However, one of the most salient points of the study was the value and feasibility of a reliable, easy, and quantitative (rather than quali- tative) assessment of handwriting performance.

Similar to the evaluation of handwriting skills, there has been use of kinematic analysis for evaluate of gait. Studies utilizing gait analysis have identified differences in stride width, velocity, and stride length in children with ASD compared to typically developing children [21,22,23

]. These findings pro- vide more clarity to previous qualitative descrip- tions of gait in ASD such as ‘clumsy, rigid, and wide-based’ [24,25]. A recent study using three- dimensional motion capture to evaluate gait func- tion in ASD has shown asymmetry of gait, which is thought to be a marker of pathologic motor devel- opment. Kinetic and kinematic gait data were obtained from children 5–12 years of age with ASD using a Vicon three-dimensional motion cap- ture system. Unlike previous studies, the authors used point-to-point analysis to evaluate data across a gait cycle rather than in discrete time points. The results showed significant asymmetry in joint posi- tions (kinematic data) and nearing significance in right and leg joint force (kinetic data). Additionally, the analysis allowed evaluation at different points during the gait cycle, which can indicate greater dysfunction in positioning of the hips, knees, or ankles. The authors noted that although asymmetry might not always be detrimental, persistent asym- metry in gait starting from childhood could be problematic. When asymmetry is present, the con- tralateral leg is required to compensate in position and force, and this can place an individual at greater risk for injury [26

]. Abnormalities in gait symmetry can also lead to difficulties in social play-based activities and sports, creating a barrier for children with ASD to participate in such activities with their peers. This work also provides clearer targets for motor intervention.

These quantitative measures of motor function have increased our knowledge of more specific motor impairments in ASD and have even led researchers to use these findings to hypothesize that impairments in motor could be secondary to dis- ruptions in cerebellar or fronto-striatal networks [16,27]. The more recent utilization of neurodiag- nostic measures, such as electroencephalography (EEG), MRI, and transcranial magnetic stimulation (TMS), has provided early insights into more specific

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abnormal neural networks leading to motor impair- ments in ASD [28

,29 &

,30 &&

,31 &&

NEURODIAGNOSTIC MEASURES OF MOTOR FUNCTION

Studies of neural mechanisms used in conjunction with standardized and quantitative motor measures are essential to parse out the heterogeneity of ASD and identify targets for behavioral and pharmaco- logic interventions for motor impairments.

Electroencephalography offers an economical and noninvasive method for investigating motor- related neural activity, including neural connectiv- ity [32]. Oscillatory electrical activity, as captured by EEG, reflects aspects of neural excitation and inhi- bition, with the latter primarily modulated by GABAergic processes. Altered brain oscillatory activ- ity has been implicated in ASD (for review, see [33]). In motor output areas, the modulation (suppres- sion) of beta band oscillations (typically defined as 13–30 Hz) has emerged as a prominent signal, particularly elicited during motor specific actions. Beta oscillations might indicate ongoing sensorimo- tor integration, coordination, and motor prepara- tion, as attenuation of beta oscillations are linked to faster onset of movement [34]. Quantifying modu- lations of beta oscillations during task-dependent motor activities in individuals with ASD can provide valuable information regarding potential aberrant cortical networks that might be contributing to the motor dysfunction.

In a recent study, EEG was used to evaluate the role of oscillatory changes during a praxis motor control task in children with ASD from 8 to 13 years of age [31

]. The study chose to evaluate praxis, because this motor domain represents the perfor- mance of complex, skilled gestures that are used in functional skills and communication. EEG was recorded while the patients performed a praxis par- adigm made up of pantomiming 10 common tools. Individuals with ASD displayed reduced task-related EEG power modulation during performance on the praxis task, which suggests that dyspraxia in ASD might be associated with decreased activity in the frontal-parietal praxis network. The authors also found a correlation between decreased left central beta band desynchronization and autism severity (defined from Autism Diagnostic Observation Scale severity scores). These findings indicate aberrant neural physiology associated with motor impair- ments in ASD, and offers a potential brain-based marker that can be measured with introduction of interventions [31

]. Imaging studies using MRI, functional MRI

(fcMRI), and diffusion-tensor imaging (DTI)/

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diffusion tractography/diffusion-weighted images have identified atypical patterns of structural brain growth in ASD [35]. The use of imaging studies in conjunction with behavioral measures of motor function can allow evaluation of the neurobiology underlying motor development.

As noted earlier in this review, studies of infants at risk for ASD have primarily utilized behavioral measures to identify differences in motor develop- ment. A recent study used resting state fcMRI to identify functional brain networks associated with walking and gross motor skills in infants at low and high risk for ASD. In all, 187 infants at 12 and 24 months of age underwent gross motor assess- ments through the Mullen Scales of Early Learning (MSEL) and brain MRI. Scores for walking and gross motor function were analyzed in relation to network level functional connectivity based on fcMRI data acquired from infants and toddlers during natural sleep. The authors adapted a statistical method termed enrichment analysis to use a brain-wide approach to identify networks with a significantly increased density of connections strongly related to the studies of walking and gross motor behaviors. The findings indicated that subsets of infant/toddler brain networks show strong relationships of func- tional connectivity to walking and gross motor function, and the profile of these brain networks differs at 12 and 24 months. Additionally, these network profiles involve both positive and negative brain–behavior relationships, which implies that increases and decreases in network level connectiv- ity may underlie the developmental progression of walking and gross motor function during this age range. The description of these brain networks of early gross motor development can aid in informing neural systems contributing to typical and atypical motor outcomes and also potentially aid in differ- entiating neurodevelopmental disorders associated with motor abnormalities [36

]. Studies of neuroimaging to better identify neu-

ral mechanisms of motor dysfunction in adults with ASD has been more frequently utilized compared to younger populations. A recent study of adults with high functioning ASD combined the use of diffusion tractography and a behavioral measure of fine motor skill performance [37

]. It was found that participants with ASD had slower performance on the Purdue Pegboard test compared to typically developing adults. Additionally, diffusion tractog- raphy investigating primary motor cortex (M1) and somatosensory cortex (S1) connections showed decreased fractional anisotropy and increased per- pendicular diffusivity, which has been seen in asso- ciation with abnormalities of white matter tract structure, reduced tract coherence and organization,

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and reduced myelination. It is thought that these white matter abnormalities might underpin slower and worse performance on the Purdue Pegboard test. This study provides direct support of the role of the connections between S1, M1, and fine motor skill performance, and supports the potential development of therapeutic approaches due to the relationship of S1 input to M1 in long term potenti- ation [37

]

FUTURE DIRECTIONS AND CONCLUSION

As we move forward in the assessment of motor function in ASD it is imperative the field continue to employ these quantitative (both behavioral and neurodiagnostic) measures. This study has highlighted the advances in assessment of motor function in ASD and the contribution these assess- ments have made in better understanding more specific and subtle motor impairments in ASD and the underlying pathophysiology leading to these impairments.

Despite evidence for definitive motor dysfunc- tion in ASD, studies of motor function in ASD, how- ever, face some significant limitations, which include lack of large samples of children with ASD and varying levels of behavioral and cognitive functioning; few studies evaluating children with ASD across develop- ment to examine emergence of motor impairment and changes over time; few studies that evaluate the impact of genetic cause, ASD severity, and prevalent behavioral comorbidities (attention deficit hyperac- tivity disorder, intellectual disability, irritability) on the manifestation of motor impairments. Quantita- tive measures of motor function can alleviate the cognitive and behavioral requirements of most stan- dardized motor assessments and assess individuals with ASD across a lifespan. These qualities allow the study of a more heterogeneous sample of individ- uals with ASD. Additionally, future studies should utilize these measures to compare motor impairments in other NDDs to ASD, to establish the degree of specificity of certain motor impairments in ASD.

Recently, the literature has recognized how motor impairments in ASD not only affect other developmental domains but can also lead to reduced participation in physical activity and subsequent predisposition to poorer health outcomes [38

]. Evi- dence-based early intervention programs that target social and behavioral difficulties in children with ASD have shown to facilitate long-term improve- ments in these areas [39]. A recent systematic review highlighted the benefits of various physical activity interventions for children with ASD below 16 years of age. The study found that jogging, horseback riding, martial arts, swimming, and yoga/dance can

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result in improvements to numerous behavioral out- comes. These outcomes include stereotyped behav- iors, social–emotional functioning, cognition, and attention [40]. Another study evaluated the benefits of an Australian Football League program adapted for children with ASD. Children enrolled in the program for 1.5 h a week over a total of 11 weeks. Although there was not significant change on the objective motor assessment, standardized parent question- naire indicated significant improvement in child object control skills. Parents also noted improve- ments in coordination and social skills [41]. The positive results of these studies highlight the critical need to develop evidence-based motor and physical activity interventions for individuals with ASD.

As we begin to identify specific motor impair- ments in ASD and the timing of emergence of these impairments, we can begin to develop timely, indi- vidualized interventions and community-based ser- vices that support these individuals and improve overall neurodevelopmental outcomes and long- term functioning.

Acknowledgements

None.

Financial support and sponsorship

Dr Wilson is funded by the National Institutes of Health. Professor Enticott is funded by a Future Fellowship

from the Australian Research Council (FT160100077). He also receives funding from the Brain and Behavior Research Foundation and Fererro.

The work was supported by the Department of Psy- chiatry at UCLA and the Centre for Social and Early Emotional Development (SEED), Deakin University.

Conflicts of interest

Dr Wilson has no conflicts of interest to disclose. Prof. Enticott and Professor Rinehart receive funding from the Ferrero Group, Australia as part of its Kinder þ Sport pillar of Corporate Social Responsibility initia- tives to promote active lifestyles among young people. Ferrero Group Australia had no role in this research including the collection, analysis, and interpretation of data; in writing of the manuscript; and in the decision to submit the article for publication.

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