Motor Learning Relies on Integrated Sensory Inputs in ADHD, but Over‐Selectively on Proprioception in Autism Spectrum Conditions

Abstract

Lay Abstract Children with autism spectrum disorder (ASD) show deficits in development of motor skills, in addition to core deficits in social skill development. In a previous study (Haswell et al., 2009) we found that children with autism show a key difference in how they learn motor actions, with a bias for relying on joint position rather than visual feedback; further, this pattern of motor learning predicted impaired motor, imitation and social abilities. We were interested in finding out whether this altered motor learning pattern was specific to autism. To do so, we examined children with Attention Deficit Hyperactivity Disorder (ADHD), who also show deficits in motor control. Children learned a novel movement and we measured rates of motor learning, generalization patterns of motor learning, and variability of motor speed during learning. We found children with ASD show a slower rate of learning and, consistent with previous findings, an altered pattern of generalization that was predictive of impaired motor, imitation, and social impairment. In contrast, children with ADHD showed a normal rate of learning and a normal pattern of generalization; instead, they (and they alone), showed excessive variability in movement speed. The findings suggest that there is a specific pattern of altered motor learning associated with autism. Scientific Abstract The brain builds an association between action and sensory feedback to predict the sensory consequence of self-generated motor commands. This internal model of action is central to our ability to adapt movements, and may also play a role in our ability to learn from observing others. Recently we reported that the spatial generalization patterns that accompany adaptation of reaching movements were distinct in children with Autism Spectrum Disorder (ASD) as compared to typically developing (TD) children. To test whether the generalization patterns are specific to ASD, here we compared the patterns of adaptation to those in children with Attention Deficit Hyperactivity Disorder (ADHD). Consistent with our previous observations, we found that in ASD the motor memory showed greater than normal generalization in proprioceptive coordinates compared with both TD children and children with ADHD; children with ASD also showed slower rates of adaptation compared with both control groups. Children with ADHD did not show this excessive generalization to the proprioceptive target, but did show excessive variability in the speed of movements with an increase in the exponential distribution of responses (τ) as compared with both TD children and children with ASD. The results suggest that slower rate of adaptation and anomalous bias towards proprioceptive feedback during motor learning is characteristic of autism; whereas increased variability in execution is characteristic of ADHD.

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

“…In another example of better than normal performance in autism, and the inspiration for our current study, we found that children with ASD showed greater than normal generalization of force field adaptation in intrinsic, or proprioceptive, coordinates (Haswell et al, 2009;Izawa et al, 2012b). In other words, after learning to fully compensate for a force field, children with ASD expressed that learning better than controls in a new workspace that was proprioceptively similar to the original workspace.…”

“…In a recent series of studies we examined motor learning in ASD, focusing on a reaching task in which the children learned to compensate for a perturbation. We found that children with ASD constructed an internal model that was different than healthy controls, potentially relying more than normal on proprioception, as evidenced by their generalization patterns (Haswell et al, 2009;Izawa et al, 2012b). In contrast, children (Johnson et al, 2013) and adults (Mosconi et al, 2013) with ASD showed slower learning in a saccade adaptation paradigm, in which errors were purely visual in nature.…”

“…In other words, after learning to fully compensate for a force field, children with ASD expressed that learning better than controls in a new workspace that was proprioceptively similar to the original workspace. We had interpreted this to reflect an increased ability to learn from proprioceptive error during motor adaptation (Haswell et al, 2009;Izawa et al, 2012b), but had been unable to directly measure learning from proprioception. In the current paper, we relied on single trial learning with a mix of visual and proprioceptive errors, and were able to measure learning from proprioceptive and visual errors to directly test our hypothesis.…”

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

“…Deficits in motor adaption implicate the cerebellum, where cell abnormalities in the cerebellar vermis and hemispheres are a robust feature of ASC (Fatemi et al, 2012;Rogers et al, 2013). 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).…”

Visual Behavior Analysis Between Neuro-typical Children and Children with Autism Spectrum Disorder

“…This result was inferred to indicate flawed cerebellum vermis. The cerebellum vermis plays a vital role in maintaining a consistent accuracy of saccades and correcting systematic errors in saccade amplitudes [14]. In a second E.O.G study, Minshew, Luna and Sweeney [15] recorded the saccade velocity, latency and accuracy of 26 adolescents with ASD using a visually guided saccade.…”