Atypical lateralization of motor circuit functional connectivity in children with autism is associated with motor deficits

Abstract

BackgroundAtypical lateralization of language-related functions has been repeatedly found in individuals with autism spectrum conditions (ASC). Few studies have, however, investigated deviations from typically occurring asymmetry of other lateralized cognitive and behavioural domains. Motor deficits are among the earliest and most prominent symptoms in individuals with ASC and precede core social and communicative symptoms.MethodsHere, we investigate whether motor circuit connectivity is (1) atypically lateralized in children with ASC and (2) whether this relates to core autistic symptoms and motor performance. Participants comprised 44 right-handed high-functioning children with autism (36 males, 8 females) and 80 typically developing control children (58 males, 22 females) matched on age, sex and performance IQ. We examined lateralization of functional motor circuit connectivity based on homotopic seeds derived from peak activations during a finger tapping paradigm. Motor performance was assessed using the Physical and Neurological Examination for Subtle Signs (PANESS).ResultsChildren with ASC showed rightward lateralization in mean motor circuit connectivity compared to typically developing children, and this was associated with poorer performance on all three PANESS measures.ConclusionsOur findings reveal that atypical lateralization in ASC is not restricted to language functions but is also present in circuits subserving motor functions and may underlie motor deficits in children with ASC. Future studies should investigate whether this is an age-invariant finding extending to adolescents and adults and whether these asymmetries relate to atypical lateralization in the language domain.Electronic supplementary materialThe online version of this article (doi:10.1186/s13229-016-0096-6) contains supplementary material, which is available to authorized users.

Processing of Real‐World, Dynamic Natural Stimuli in Autism is Linked to Corticobasal Function

“…The left-lateralized hypoactivation seen in the ASD group in the present study was consistent with two resting-state functional connectivity studies that reported atypical right-hemisphere lateralization of motor circuit connectivity in ASD [Cardinale, Shih, Fishman, Ford, & Muller, 2013;Floris et al, 2016]. Consequently, performing the task of anticipating when the basketball would bounce based on visual motion information may have been readily processed by left corticobasal circuits in the TD group.…”

What can autism teach us about the role of sensorimotor systems in higher cognition? New clues from studies on language, action semantics, and abstract emotional concept processing

“…They found abnormalities in the connections between the motor and sensory hand regions which was associated with poorer performance in the pegboard test. Interestingly, the differences in correlations between control and autistic groups suggested a lack of the typical left dominance for motor performance in the autistic group, and that this reduced asymmetry was related to poorer performance, as also found by Floris et al (2016).…”

“…Precisely 49 studies comparing ASC and typically-developing (TD) control groups answer this question in the affirmative. The more methodologically rigorous studies, those which a) either matched for chronological and/or mental age and/or IQ or b) controlled for these in their analyses, and c) had more sizeable groups (>30 per group) demonstrate that motor impairments occur more often than might be expected in TD children (AbuDahab, Skidmore, Holm, Rogers, & Minshew, 2013;Ament et al, 2015;Dewey, Cantell, & Crawford, 2007;Dowell, Mahone, & Mostofsky, 2009;Duffield et al, 2013;Dziuk et al, 2007;Floris et al, 2016;Sumner, Leonard, & Hill, 2016;Travers et al, 2015Travers et al, , 2016. A meta-analysis of 41 studies confirmed that, despite substantial variation, effect sizes are large with TD participants significantly outperforming individuals with autism in motor coordination, arm movements, gait and postural stability (Fournier, Hass, Naik, Lodha, & Cauraugh, 2010), and that these effects did not seem affected by publication bias.…”

“…Many studies addressed this question with movement assessment batteries with normative percentiles for performance and objective scoring: for example, the PANESS (Dowell et al, 2009;Dziuk et al, 2007;Floris et al, 2016;Jansiewicz et al, 2006;Mostofsky, Burgess, & Gidley Larson, 2007), the M-ABC or M-ABC2 (Ament et al, 2015;Green, Baird et al, 2002;Green, Moore, & Reilly, 2002;Green et al, 2009;Hanaie et al, 2013;Hanaie et al, 2014;Kopp, Beckung, & Gillberg, 2010;McPhillips, Finlay, Bejerot, & Hanley, 2014;Miyahara et al, 1997;Sumner et al, 2016;Whyatt & Craig, 2012), or the Bruininks-Oseretsky test (Dewey et al, 2007;Ghaziuddin & Butler, 1998;Hilton, Zhang, Whilte, Klohr, & Constantino, 2012;Pan, 2014). These measures yield total scores which were sometimes analysed alone, but they each assess a range of fine and gross motor skills, including balance and gait, hopping or jumping, repetitive sequential movements of the hands and feet, manual dexterity and ball skills (catching and throwing).…”

Lateralization of Brain Networks and Clinical Severity in Toddlers with Autism Spectrum Disorder: A HARDI Diffusion MRI Study

“…Adolescents and young adults with high‐functioning ASD were found to have atypical lateralization of diffusion indexes in the Cingulate, AF, and Uncinate Fasciculus (UF) [Fletcher et al, ; Knaus et al, ; Lo et al, ], in the Superior Temporal Gyrus (STG) [Lange et al, ], in the pathways involving the fusiform [Conturo et al, ], in the temporal lobe (parahippocampal gyrus, STG, sagittal stratum) [Peterson, Mahajan, Crocetti, Mejia, & Mostofsky, ] or within the corpus callosum [Floris et al, ]. An atypical laterality pattern was also reported in functional magnetic resonance imaging (MRI) studies showing altered asymmetry in brain representation of language‐related networks [Lindell & Hudry, ] or even in motor circuits [Floris, Barber, Nebel, & Mostofsky, ]. Emerging evidence suggests that an atypical lateralization is already present in younger children.…”