Distinct Roles for the Cerebellum, Angular Gyrus, and Middle Temporal Gyrus in Action–Feedback Monitoring

Abstract

Action-feedback monitoring is essential to ensure meaningful interactions with the external world. This process involves generating efference copy-based sensory predictions and comparing these with the actual action-feedback. As neural correlates of comparator processes, previous fMRI studies have provided heterogeneous results, including the cerebellum, angular and middle temporal gyrus. However, these studies usually comprised only self-generated actions. Therefore, they might have induced not only action-based prediction errors, but also general sensory mismatch errors. Here, we aimed to disentangle these processes using a custom-made fMRI-compatible movement device, generating active and passive hand movements with identical sensory feedback. Online visual feedback of the hand was presented with a variable delay. Participants had to judge whether the feedback was delayed. Activity in the right cerebellum correlated more positively with delay in active than in passive trials. Interestingly, we also observed activation in the angular and middle temporal gyri, but across both active and passive conditions. This suggests that the cerebellum is a comparator area specific to voluntary action, whereas angular and middle temporal gyri seem to detect more general intersensory conflict. Correlations with behavior and cerebellar activity nevertheless suggest involvement of these temporoparietal areas in processing and awareness of temporal discrepancies in action-feedback monitoring.

Perceiving your hand moving: BOLD suppression in sensory cortices and the role of the cerebellum in the detection of feedback delays

“…First, regions of the bilateral anterior and posterior cerebellum, including lobules IV-V and IX, were found to be significantly engaged for trials in which a delay was detected versus not detected during self-generated movements. This is in line with the notion of the cerebellum as a state estimator, modulating predicted sensory consequences of motor commands and providing error signal for the unpredicted consequences of these commands (Blakemore & Frith, 2003;Blakemore et al, 2001;Leube et al, 2003;Miall, Weir, Wolpert, & Stein, 1993;Miall et al, 2007;van Kemenade et al, 2019;Wolpert et al, 1998). Our finding of higher involvement in the cerebellar areas for subjectively delayed trials during self-compared with externallygenerated movements not only supports the cerebellum's role as generating predictions and detecting errors during sensorimotor processing, but it also provides a subjective component to the involvement of the cerebellum in processing these discrepancies.…”

“…Data from all participants was taken from a recent study by our group in which we examined contributions of different regions in action-feedback monitoring of naturalistic self-versus externally generated movements (van Kemenade et al, 2019). The experimental design and data acquisition procedures have been reported previously in van Kemenade et al 2019and restated below for the reader's convenience.…”

“…More specifically, we aimed to examine BOLD suppression regarding naturalistic visual feedback of self-generated wrist movements and the impact of an additional (auditory) modality on the detection of temporal discrepancies between self-generated movements and their visual feedback. To this end, participants were asked to perform wrist movements using the handle of a custom-made passive movement device (PMD) (see van Kemenade et al, 2019). Half of the trials involved an externally generated movement condition in which the PMD moved the hand automatically.…”

“…Citation: Arikan, B. E., van Kemenade, B. M., Podranski, K., Steinsträter, O., Straube, B., & Kircher, T. (2019). Perceiving your hand moving: BOLD suppression in sensory cortices and the role of the cerebellum in the detection of feedback delays.…”

The boundaries of the self: The sense of agency across different sensorimotor aspects

“…For example, sensitivity to alterations in the temporal aspect must rely on comparison of onset timing relations between visual and sensorimotor signals. Brain-imaging studies have shown that this is processed in parietal and cerebellar regions (Blakemore & Sirigu, 2003;Farrer, Frey, et al, 2008;Leube et al, 2003;MacDonald & Paus, 2003;Salomon, Malach, & Lamy, 2009;van Kemenade et al, 2018). However, detecting discrepancies in the spatial or anatomical aspects may require different computations, taking into account continuous action plans and somatotopic representations associated with frontal and parietal regions as well as the extrastriate body area (David et al, 2007;.…”