Predicting the Multisensory Consequences of One’s Own Action: BOLD Suppression in Auditory and Visual Cortices

Abstract

Predictive mechanisms are essential to successfully interact with the environment and to compensate for delays in the transmission of neural signals. However, whether and how we predict multisensory action outcomes remains largely unknown. Here we investigated the existence of multisensory predictive mechanisms in a context where actions have outcomes in different modalities. During fMRI data acquisition auditory, visual and auditory-visual stimuli were presented in active and passive conditions. In the active condition, a self-initiated button press elicited the stimuli with variable short delays (0-417ms) between action and outcome, and participants had to detect the presence of a delay for auditory or visual outcome (task modality). In the passive condition, stimuli appeared automatically, and participants had to detect the number of stimulus modalities (unimodal/bimodal). For action consequences compared to identical but unpredictable control stimuli we observed suppression of the blood oxygen level depended (BOLD) response in a broad network including bilateral auditory and visual cortices. This effect was independent of task modality or stimulus modality and strongest for trials where no delay was detected (undetected<detected). In bimodal vs. unimodal conditions we found activation differences in the left cerebellum for detected vs. undetected trials and an increased cerebellar-sensory cortex connectivity. Thus, action-related predictive mechanisms lead to BOLD suppression in multiple sensory brain regions. These findings support the hypothesis of multisensory predictive mechanisms, which are probably conducted in the left cerebellum.

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

“…In other words, activity in auditory cortices was suppressed during self-generated movements independent of whether an auditory stimulus occurred or not. This is similar to our previous finding, demonstrating suppressed BOLD signal in auditory cortices during the presentation of audiovisual and visual-only stimuli (Straube et al, 2017). These findings can be explained in terms of expectation-based processing.…”

“…Suppression effects observed in sensory regions are in line with our previous study (Straube et al, 2017) À94, 14) showing functional connectivity with the left cerebellum IX (MNI coordinates: x, y, z ¼À6, À52, À32) in detected versus undetected trials during self-movements compared with externally generated movements (cluster defining threshold p , 0.001, small volume correction at the peak level p FWE , 0.05 within a priori specified ROI). (b) Scatterplot from a single participant's data illustrating correlation between the left cerebellum IX and the right SOG for self-and externally generated movements.…”

“…The task remained the same in these trials. Based on our previous finding of BOLD suppression (Straube et al, 2017), we expected to observe reduced activity in sensory areas for self-generated compared with externally generated movements. Because unimodal and bimodal conditions would be equally likely, we expected to find reduced BOLD activity in auditory regions in both unimodal and bimodal conditions when the movement was self-generated due to sensorimotor prediction.…”

“…With respect to neural correlates, our group has previously shown that perceiving single auditory or visual (unimodal) and audiovisual (bimodal) consequences of voluntary button presses lead to reduced BOLD activity in somatosensory, visual, and auditory cortices for self-generated stimuli compared with passive viewing of these stimuli. In addition, participants were more sensitive to delays between their button press and the sensory consequence of the button press in the bimodal condition, suggesting that the additional modality enhanced delay detection for self-generated movements and their consequences (Straube et al, 2017).…”

“…Despite these findings, a number of issues remain to be explored that are crucial in advancing our understanding of why the processing of voluntary actions and their sensory consequences are distinct. First, most studies investigating cross-modal perception and action so far used passive viewing of sensory stimuli as a control condition (Desantis & Haggard, 2016a;Desantis, Waszak, Moutsopoulou, & Haggard, 2016;Kawabe et al, 2013;Straube et al, 2017;. Although this condition might address the influence of self-generated movements on the perception of sensory inputs by factoring out mere sensory processing, the role of efferent feedback cannot be addressed.…”