Behavioural and neural basis of anomalous motor learning in children with autism

Abstract

Autism spectrum disorder is a developmental disorder characterized by deficits in social and communication skills and repetitive and stereotyped interests and behaviours. Although not part of the diagnostic criteria, individuals with autism experience a host of motor impairments, potentially due to abnormalities in how they learn motor control throughout development. Here, we used behavioural techniques to quantify motor learning in autism spectrum disorder, and structural brain imaging to investigate the neural basis of that learning in the cerebellum. Twenty children with autism spectrum disorder and 20 typically developing control subjects, aged 8-12, made reaching movements while holding the handle of a robotic manipulandum. In random trials the reach was perturbed, resulting in errors that were sensed through vision and proprioception. The brain learned from these errors and altered the motor commands on the subsequent reach. We measured learning from error as a function of the sensory modality of that error, and found that children with autism spectrum disorder outperformed typically developing children when learning from errors that were sensed through proprioception, but underperformed typically developing children when learning from errors that were sensed through vision. Previous work had shown that this learning depends on the integrity of a region in the anterior cerebellum. Here we found that the anterior cerebellum, extending into lobule VI, and parts of lobule VIII were smaller than normal in children with autism spectrum disorder, with a volume that was predicted by the pattern of learning from visual and proprioceptive errors. We suggest that the abnormal patterns of motor learning in children with autism spectrum disorder, showing an increased sensitivity to proprioceptive error and a decreased sensitivity to visual error, may be associated with abnormalities in the cerebellum.

Postural Control Deficits in Autism Spectrum Disorder: The Role of Sensory Integration

“…vision), together with a lack of increase in instability between this channel and the condition in which both channels were inaccurate. Similar channel-specific impairments have been shown in ASD in a recent study using a motor learning task (Marko et al, 2015).…”

“…On the ASD side, studies have shown a reduction in purkinje cell numbers (Bailey et al, 1998;Ritvo et al, 1986) and a reduction in volume of the cerebellar vermis (Hashimoto et al, 1995;Murakami, Courchesne, Press, YeungCourchesne, & Hesselink, 1989;Scott, Schumann, Goodlin-Jones, & Amaral, 2009) and on the sensorimotor control side, it is well established that the cerebellum is critical for postural control, sensory integration and motor learning (for a review see Therrien & Bastian, 2015). While little is known about the role of the cerebellum in ASD individuals' postural control, a recent study assessed the role of the cerebellum in ASD and TD children's ability to learn a simple reaching task using visual and proprioceptive feedback (Marko et al, 2015). Children with ASD were faster than controls in proprioceptive-based learning but slower in visual-based learning.…”

Autistic-Like Traits and Cerebellar Dysfunction in Purkinje Cell PTEN Knock-Out Mice

“…Indeed, it has also been observed in a number of other mutants displaying PC loss (see for review Porras-García et al, 2013). Nonetheless, gait abnormalities, anomalous motor learning or other types of motor symptoms are often present in ASD patients, and they have been related to cerebellar malformation (Marko et al, 2015).…”

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

“…Several studies suggest that children with ASC rely on proprioceptive feedback for motor adaptation and are impaired when learning motor skills through visual input alone (Izawa et al, 2012;Mostofsky & Ewen, 2011;Sharer, Mostofsky, Pascual-Leone, & Oberman, 2015;Vanvuchelen et al, 2007;Wild, Poliakoff, Jerrison, & Gowen, 2012). Hyposensitivity and hypersensitivity to visual and proprioceptive feedback respectively is indeed correlated with abnormalities in the anterior, sensorimotor aspect of the cerebellum in children with ASC (Marko et al, 2015). The cerebellum has also been linked to gait dysfunction in ASC (Nayate, Bradshaw, & Rinehart, 2005;.…”