Motor Skill in Autism Spectrum Disorders: A Subcortical View

doi:10.1016/B978-0-12-418700-9.00007-1

International Review of Neurobiology

Volume 113, 2013, Pages 207-249

https://doi.org/10.1016/B978-0-12-418700-9.00007-1 Get rights and content

Abstract

The earliest observable symptoms of autism spectrum disorders (ASDs) involve motor behavior. There is a growing awareness of the developmental importance of impaired motor function in ASD and its association with social skill. Compromised motor function requires increased attention, leaving fewer resources available for processing environmental stimuli and learning. This knowledge suggests that the motor system—which we know to be trainable—may be a gateway to improving outcomes of individuals living with ASD. In this review, we suggest a framework borrowed from machine learning to examine where, why, and how motor skills are different in individuals with ASD.

Section snippets

Why Study Motor Skill in Autism?

Autism is a behaviorally defined disorder characterized by deficits in social engagement, atypical verbal and nonverbal communication, and a focus on ritualized behaviors and restricted interests. Despite its absence from diagnostic criteria, differences in motor skills in individuals with autism spectrum disorder (ASD) have been observed from the earliest descriptions of the disorder (Kanner, 1943).

In his landmark 1943 description of autism, Leo Kanner noted uneven motor development, including

Overview of Motor Skill Deficits

Generalized motor deficits are common in ASD, but we lack a body of quantitative, model-driven studies yielding specific results tied to the mechanism. Clinical studies with a neurology focus have a rich history of using neurological “soft signs” to assess motor skill deficits (Haas et al., 1996). Although these tests have been quite useful for diagnostic purposes and have highlighted the generalized motor deficits of individuals diagnosed with autism, they have not been as useful for research

Mapping Autism Motor Skill Findings into a Useful Framework

The cerebellum and basal ganglia each have different local circuit architectures and synaptic learning mechanisms (Doya, 1999, Doya, 2000) that are specialized for different types of information processing. We might best approach an understanding of subcortical motor processing in ASD by asking what each area is specialized to learn. Motor skill learning and performance are, of course, the integrated product of activity in multiple cortical and subcortical brain regions. However, recent models

Can We Intervene?

What happens in the brain during motor skill learning? This question can be asked at many levels, including synaptic and subsynaptic, functional motor maps and activity, and at a range of temporal scales. Figure 7.2 represents a summary of motor skill training effects modifying the efficacy of synapses in the cerebellum and basal ganglia based on animal research findings.

Two models of motor skill learning propose interactions between two cortical–subcortical circuits, but these models differ in

Summary

This review of data on motor skills with anatomical and connectivity differences in individuals with ASD places us in a position to consider what questions, if answered, would take us to the next step in understanding the motor skill in ASD. The questions in Box 7.1 are the proverbial tip of the iceberg, but attempting to answer them will take us to the next stage of our understanding.

Despite the increased interest in motor skills in autism, most of the reports described earlier contain

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Although not included in the diagnostic criteria (APA, 2013), motor skill deficits are prevalent in individuals with ASD and were already present in the early descriptions of ASD by Kanner (1943). Also, studies have suggested that the earliest manifestation of ASD is atypical motor development being reflected as delay in achieving motor milestones (Chukoskie, Townsend, & Westerfield, 2013; Coll, Foster, Meilleur, Brambati, & Hyde, 2020; Downey & Rapport, 2012; West, 2019). Numerous recent reviews and meta-analyses have shed a light on the broad range of motor challenges in ASD (Zampella et al., 2021).
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The current study added to the evidence about motor skill deficits among children and youth with ASD. VP and VMI were not related to motor skills, suggesting that these functions – as measured in the current study – are no underlying mechanisms of motor skill deficits of children with ASD and average intelligence. Diagnostic implications are provided for the evidence of motor skill deficits among children and youth with ASD.
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The motor domain probably represents the more recognized argument to bridge the gap between ASD and cerebellar studies. Having been widely reviewed by eminent scholars in recent years, here we did not aim to systematically tackle “classical” (e.g., motor control, or motor coordination) motor difficulties in ASD (Gowen and Hamilton, 2013; Chukoskie et al., 2013; Johnson et al., 2016; Cook, 2016) or in patients with cerebellar disturbances (see Ito, 2000; Cerminara et al., 2005; Gowen and Miall, 2007; Konczak and Timmann, 2007; Morton and Bastian, 2007; Nowak et al., 2007; Manto, 2008; Dash and Thier, 2014; Koziol et al., 2014; Thach, 2014; Pisotta and Molinari, 2014; Mariën et al., 2015; Therrien and Bastian, 2015; Lefort et al., 2015; Grimaldi et al., 2016; Peterburs and Desmond, 2016). In contrast, here we propose to focus on motor components that reflect high stages of the motor hierarchy (Casartelli et al., 2017a).
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Autism Spectrum Disorder (ASD) is a multisystem neurodevelopmental disorder characterized by primary deficits in social communication skills and highly repetitive and restricted behaviors and interests (American Psychiatric Association, 2013). In addition to these diagnostic impairments, around 50–85% children with ASD demonstrate consistent deficits in several aspects of perceptuo-motor performance (Bhat, Landa, & Galloway, 2011; Chukoskie, Townsend, & Westerfield, 2013; Green et al., 2009; Hilton, Zhang, Whilte, Klohr, & Constantino, 2012). A systematic examination of motor deficits in ASD is warranted for several reasons.
Children with Autism Spectrum Disorder (ASD) have basic motor impairments in balance, gait, and coordination as well as autism-specific impairments in praxis/motor planning and interpersonal synchrony. Majority of the current literature focuses on isolated motor behaviors or domains. Additionally, the relationship between cognition, symptom severity, and motor performance in ASD is unclear. We used a comprehensive set of measures to compare gross and fine motor, praxis/imitation, motor coordination, and interpersonal synchrony skills across three groups of children between 5 and 12 years of age: children with ASD with high IQ (HASD), children with ASD with low IQ (LASD), and typically developing (TD) children. We used the Bruininks-Oseretsky Test of Motor Proficiency and the Bilateral Motor Coordination subtest of the Sensory Integration and Praxis Tests to assess motor performance and praxis skills respectively. Children were also examined while performing simple and complex rhythmic upper and lower limb actions on their own (solo context) and with a social partner (social context). Both ASD groups had lower gross and fine motor scores, greater praxis errors in total and within various error types, lower movement rates, greater movement variability, and weaker interpersonal synchrony compared to the TD group. In addition, the LASD group had lower gross motor scores and greater mirroring errors compared to the HASD group. Overall, a variety of motor impairments are present across the entire spectrum of children with ASD, regardless of their IQ scores. Both, fine and gross motor performance significantly correlated with IQ but not with autism severity; however, praxis errors (mainly, total, overflow, and rhythmicity) strongly correlated with autism severity and not IQ. Our study findings highlight the need for clinicians and therapists to include motor evaluations and interventions in the standard-of-care of children with ASD and for the broader autism community to recognize dyspraxia as an integral part of the definition of ASD.

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Chapter Seven - Motor Skill in Autism Spectrum Disorders: A Subcortical View

Abstract

Section snippets

Why Study Motor Skill in Autism?

Overview of Motor Skill Deficits

Mapping Autism Motor Skill Findings into a Useful Framework

Can We Intervene?

Summary

Biological Psychiatry

International Journal of Developmental Neuroscience

Infant Behavior & Development

Trends in Cognitive Sciences

Clinical Biomechanics

Research in Developmental Disabilities

Gait & Posture

Neuropsychologia

Gait & Posture

Neuron

Neuron

Behavioural Brain Research

Trends in Cognitive Sciences

Biological Psychiatry

Biological Psychiatry

Neural Networks

Current Opinion in Neurobiology

Neuropsychologia

Cortex

Brain & development

Gait & Posture

Current Opinion in Neurobiology

Trends in Neurosciences

Current Opinion in Neurobiology

Behavioral and Neural Biology

Cortex

NeuroImage

Current Opinion in Neurobiology

Connecting genes to brain in the autism spectrum disorders

Archives of Neurology

Underconnectivity between voice-selective cortex and reward circuitry in children with autism

Proceedings of the National Academy of Sciences of the United States of America

Attentional activation of the cerebellum independent of motor involvement

Science

Impaired structural connectivity of socio-emotional circuits in autism spectrum disorders: A diffusion tensor imaging study

PLoS One

‘Autistic psychopathology’ in childhood

Diagnostic and statistical manual of mental health disorders: DSM-5

A clinicopathological study of autism

Brain

The role of the dorsal striatum in reward and decision-making

The Journal of Neuroscience

Autism during infancy: A retrospective video analysis of sensory-motor and social behaviors at 9-12 months of age

Journal of Autism and Developmental Disorders

Efficacy of sensory and motor interventions for children with autism

Journal of Autism and Developmental Disorders

Neuroanatomic observations of the brain in autism

Autism and abnormal development of brain connectivity

The Journal of Neuroscience

Oral motor deficits in speech-impaired children with autism

Frontiers in Integrative Neuroscience

Motor control outcomes following Nintendo Wii use by a child with Down syndrome

Pediatric Physical Therapy

Excess mortality and causes of death in autism spectrum disorders: A follow up of the 1980s Utah/UCLA autism epidemiologic study

Journal of Autism and Developmental Disorders

Learning causes synaptogenesis, whereas motor activity causes angiogenesis, in cerebellar cortex of adult rats

Proceedings of the National Academy of Sciences of the United States of America

Brain development during the preschool years

Neuropsychology Review

Motor development and the mind: The potential role of motor abilities as a determinant of aspects of perceptual development

Child Development

Inverse correlation between frontal lobe and cerebellum sizes in children with autism

Brain

Impairment of actions chains in autism and its possible role in intention understanding

Proceedings of the National Academy of Sciences of the United States of America

Modulation of visual signals in macaque MT and MST neurons during pursuit eye movement

Journal of Neurophysiology