Altered connectivity and action model formation in autism is autism

Abstract

Internal action models refer to sensory-motor programs that form the brain basis for a wide range of skilled behavior and for understanding others' actions. Development of these action models, particularly those reliant on visual cues from the external world, depends on connectivity between distant brain regions. Studies of children with autism reveal anomalous patterns of motor learning and impaired execution of skilled motor gestures. These findings robustly correlate with measures of social and communicative function, suggesting that anomalous action model formation may contribute to impaired development of social and communicative (as well as motor) capacity in autism. Examination of the pattern of behavioral findings, as well as convergent data from neuroimaging techniques, further suggests that autism-associated action model formation may be related to abnormalities in neural connectivity, particularly decreased function of long-range connections. This line of study can lead to important advances in understanding the neural basis of autism and, more critically, can be used to guide effective therapies targeted at improving social, communicative, and motor function.

Figures

Figure 1

Brain regions associated with praxis and imitative function include the primary visual cortex (V1); the visual region associated with recognition of movement (V5), the superior temporal sulcus (STS), which is associated with the perception of biological movement; the inferior parietal region, which is associated with storage of motor programs; the premotor regions, which are associated with transcoding of motor programs; and the primary motor cortex, which is associated with execution of motor programs. Connectivity between inferior parietal cortex and premotor cortex (red box), when lesioned, can lead to apraxia.

Figure 2

(a) Subjects undergoing testing using the upper extremity robot first develop internal action models by training to the task in the left workspace (1). They then demonstrate generalization of the internal action models by performing the task in the right workspace. The performance of the task may be done either in visual coordinates that were similar to the training (2) or in proprioceptive coordinates that were similar to the training (3), allowing differential examination of the contribution of visual and proprioceptive feedback during the development of the internal action model. (b) Children with autism and typically developing (TD) children have similar performance during the training (target 1). Children with autism show significantly more proprioceptively guided generalization (to target 3) in contrast to visually guided generalization (target 2). (c) Generalization to proprioceptive coordinates (target 3) correlates with Autism Diagnostic Observation Schedule–General (ADOS-G) score in autistic subjects (r = 0.572, P = .032). ASD = autism spectrum disorder. (d) In all children (blue dots = TD children; red dots = autistic children), relative generalization to proprioceptive coordinates (target 3) versus visual coordinates (target 2) correlates negatively with imitative function (r = -0.57, P = .006). This figure first appeared in a modified form in Nature Neuroscience (Haswell and others 2009); reprinted with permission.

Figure 3

The event-related causality technique, which uses EEG data, can show information flow from one region to another associated with a cognitive task. Here, a single subject performing a praxis task demonstrates flow (red arrows) from left parietal regions to midline premotor regions and from right parietal regions to right lateral premotor regions.

Figure 4

In our model, parietal-premotor connectivity is necessary for a number of related phenomena, including online visual-motor integration (i.e., motor imitation), formation of internal action models (i.e., procedural learning), and execution of internal action models, including motor action models (i.e., praxis) and social/communicative action models (i.e., normal social/communicative function).