Activation of cerebellum and basal ganglia during the observation and execution of manipulative actions

Antonino Errante,Leonardo Fogassi

doi:10.1038/s41598-020-68928-w

Abstract

Studies on action observation mostly described the activation of a network of cortical areas, while less investigation focused specifically on the activation and role of subcortical nodes. In the present fMRI study, we investigated the recruitment of cerebellum and basal ganglia during the execution and observation of object manipulation performed with the right hand. The observation conditions consisted in: (a) observation of manipulative actions; (b) observation of sequences of random finger movements. In the execution conditions, participants had to perform the same actions or movements as in (a) and (b), respectively. The results of conjunction analysis showed significant shared activations during both observation and execution of manipulation in several subcortical structures, including: (1) cerebellar lobules V, VI, crus I, VIIIa and VIIIb (bilaterally); (2) globus pallidus, bilaterally, and left subthalamic nucleus; (3) red nucleus (bilaterally) and left thalamus. These findings support the hypothesis that the action observation/execution network also involves subcortical structures, such as cerebellum and basal ganglia, forming an integrated network. This suggests possible mechanisms, involving these subcortical structures, underlying learning of new motor skills, through action observation and imitation.

Highlights

Studies on action observation mostly described the activation of a network of cortical areas, while less investigation focused on the activation and role of subcortical nodes
The activation pattern was largely symmetrical in both cerebellar hemispheres, with clusters of activity in lobules V, VI, crus I, VIIIa and VIIIb, some of them seem more lateralized to the right hemisphere, ipsilateral to the observed hand, such as, for example, the local maxima in lobule VI
The results, mainly focused on subcortical structures, indicate that: (a) both observation and execution of manipulative actions versus simple finger tapping movements activate subcortical structures, including basal ganglia, thalamus and cerebellum; (b) in both conditions, the activations are mainly bilateral, in the cerebellum activation intensity is higher in the right hemisphere; (c) shared voxels between observation and execution of manipulation showing increased activity with respect to control conditions are present in cerebellar lobules V, VI, crus I, VIIIa and VIIIb, in globus pallidus (GP) and subthalamic nucleus (STN) of basal ganglia, in the thalamus and in the red nucleus (RN); (d) Region of Interest (ROI) analyses performed for comparing the two main conditions confirmed the general results of the conjunction analysis, revealing a significant differential activation only in the IPS and lobule VIIIa of the cerebellum

Summary

Introduction

Studies on action observation mostly described the activation of a network of cortical areas, while less investigation focused on the activation and role of subcortical nodes. A large number of electrophysiological and brain imaging studies demonstrated the existence of an action observation/execution system in h umans[26,27,28,29,30] These studies showed that the observation of goal-directed actions done by others results in increased activations in visual areas, and in the inferior parietal lobule (IPL) and in PMv, as well as in the caudal part of the inferior frontal gyrus (IFG)[31,32]. These latter three areas have motor properties and closely correspond to the areas containing mirror neurons in the monkey. Functional MRI (fMRI) s tudies[30,32,33] investigating shared cortical activations during both action observation and execution showed common activated voxels in the classical parieto-premotor MNS, Scientific Reports | (2020) 10:12008

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Results

Discussion

Conclusion