Subcortical Contributions to Effective and Anatomical Connectivity In Brain Networks Supporting Imitation

Background: To fully understand the neural basis of both typical and atypical social cognition, it is necessary to investigate not just the activity of individual brain regions, but also the ways in which these sites coordinate their function. However, despite the fact that the cerebellum is increasingly recognized as playing an important role in a variety of affective and cognitive functions, its contributions to system processes are rarely considered outside of investigations of motor behavior. Given that cerebellar abnormalities are frequently reported in studies of the brains of individuals with ASD, a better understanding of the way in which this structure supports typical performance of important social behaviors, like imitation (which is often impaired in ASD), may also provide insight into the potential developmental consequences of cerebellar deficits.

Objectives: Our aims in this project were to 1) characterize functional specialization for imitation in typically developing (TD) adults in a statistically rigorous fashion, and 2) examine task-specific effective connectivity for imitation among key cortical and subcortical regions.

Methods: Using functional magnetic resonance imaging (fMRI), we investigated effective connectivity of brain networks supporting imitation in a sample of 15 TD adults. While in the scanner, participants engaged in a simple imitation paradigm with three conditions: Observe trials, in which participants passively viewed a human actor executing a sequence of four finger presses on a keypad; Imitate trials, in which participants imitated the actor’s finger presses on a keyboard; and Execute trials, in which participants also executed finger presses but did so based on visuospatial cues in the absence of the actor’s hand. Internal localizer analyses conducted on the functional data identified regions displaying functional specificity for imitation. Subsequently, we used these sites as seed regions in psychophysiological interaction (PPI) analyses, which are a data-driven means of assessing task-specific effective connectivity.

Results: Consistent with previous literature, we found parietal (SPL, IPL), premotor, and posterior STS (pSTS) activity associated with imitation, as well as IFG and anterior intraparietal sulcus (aIPS) activity possibly associated with mirroring processes. However, we also found task-sensitive changes in the degree of correlation between activity in the pSTS and bilateral regions of cerebellar lobule VII, such that the hemodynamic response in these regions was more highly correlated during imitation than during control conditions. A similar interaction existed between the right SPL and left lobule VII, as well as between the right pSTS and left IPL.

Conclusions: We found regions of the neocerebellum to display task-specific increases in connectivity with brain sites important for biological motion perception (the pSTS), spatial attention regulation (the SPL), and visual control of action (the SPL) during participants’ engagement in imitative behavior, suggesting that neocerebellar activity may help to facilitate nonmotor aspects of imitation in TD individuals. These findings in a TD population, when coupled with the histological, molecular, and functional cerebellar abnormalities observed in ASD, indicate that the neocerebellum should receive greater future attention in studies of social behavior and brain connectivity in ASD.