Human and monkey studies have shown that, in addition to parietal and premotor areas, the cerebellum and subcortical structures, such as the thalamus and red nucleus, are activated during the observation of grasping actions. It has been hypothesized that the cerebellum uses the forward models to anticipate sensory outcomes of the observed actions through contralateral dentato-rubro-thalamo-cortical projections. However, it is not fully understood if the specific sectors of the dentate nucleus (DN) and thalamus involved in action observation are partially segregated from purely motor sectors. In the present study, firstly, by using an fMRI task we identified cerebellar and thalamic sectors activated during both observation and execution of grasping actions, then, we used probabilistic di!usion tractography to characterize the structural connections involving these sectors. Twenty right-handed healthy participants (11 females; mean age: 24.4 years) were instructed to observe goal-directed grasping actions or to execute the same actions. Control conditions included the observation of a static context and the execution of opening-closing hand movements, respectively. Two partially segregated sets of regions of interest were delineated: the first based on pure motor activation and the second based on conjunction analysis between observation and execution. Shared activation between observation and execution was present in the inferior parietal lobule (IPL), ventral premotor cortex (PMv), cerebellar lobules V-VI, DN, red nucleus, and thalamus. The activation of the DN and thalamus exhibited functional partial segregation with respect to purely motor sectors. The dorsal DN and ventrolateral (VL) thalamic nucleus were mostly activated during grasping execution. In contrast, the ventral DN and ventral-posterolateral (VPL) thalamic nucleus showed shared activations during both observation and execution. Moreover, the red nucleus was activated bilaterally in both motor and observation conditions. Di!usion tractography showed that tracts originating from the motor sectors of the DN project to the contralateral red nucleus and VL nucleus, in the path traveling to the contralateral rostral sector of IPL and PMv. The ventral DN was connected by partially segregated projections with the contralateral red nucleus and VPL nucleus, in the path to the contralateral caudal sector of IPL and PMv. These results provide evidence of partially segregated cerebellar outputs to thalamic and cortical regions involved in action observation and execution. Through these circuits, the cerebellum can exploit its role in motor simulation during action observation.
