Somatosensory omissions reveal action-related predictive processing

Abstract

The intricate relation between action and somatosensory perception has been studied extensively in the past decades. Generally, a forward model is thought to predict the somatosensory consequences of an action. These models propose that when an action is reliably coupled to a tactile stimulus, unexpected absence of the stimulus should elicit prediction error. Although such omission responses have been demonstrated in the auditory modality, it remains unknown whether this mechanism generalizes across modalities. This study therefore aimed to record action-induced somatosensory omission responses using EEG in humans. Self-paced button presses were coupled to somatosensory stimuli in 88% of trials, allowing a prediction, or in 50% of trials, not allowing a prediction. In the 88% condition, stimulus omission resulted in a neural response consisting of multiple components, as revealed by temporal principal component analysis. The oN1 response suggests similar sensory sources as stimulus-evoked activity, but an origin outside primary cortex. Subsequent oN2 and oP3 responses, as previously observed in the auditory domain, likely reflect modality-unspecific higher order processes. Together, findings straightforwardly demonstrate somatosensory predictions during action and provide evidence for a partially amodal mechanism of prediction error generation.

Keywords: EEG; efference copy; motor; predictive coding.

FIGURE 1

Schematic representation of the experimental design. Panel (a) shows the experimental set‐up: a participant sat in front of a screen with both arms on a table. With the right hand a button was pressed, possibly resulting in a stimulus on the left hand (indicated with green circles). Stimuli were applied by a puff of air traveling through air tubes and inflating a membrane on the left middle‐ and index‐finger. Panel (b) depicts the task over time, where participants pressed a button every 600–1200 ms. Panel (c) shows examples of the tactile effects of the button presses for all three conditions. In the 88%‐condition, there was an 88% chance of a button press resulting in a stimulus. In the 50%‐condition, the chance was 50%. In the motor condition, button presses never resulted in a tactile stimulus.

FIGURE 2

Uncorrected event‐related potentials (ERPs) for right‐lateral ROI (a: channels C6, CP6) and frontal ROI (b: channels Fz, F2). Plots show ERPs including 95% CIs for 88% omission, 50% omission, and motor‐control conditions.

FIGURE 3

Event‐related potential (ERP) amplitudes (colour map) and cluster statistics (transparency maps) for the difference between 88%‐ minus motor‐condition contrast in omission trials (panel a), 50%‐ minus motor‐condition contrast in omission trials (panel b), 88%‐ minus 50%‐condition contrast in omission trials (panel c), and 88%‐ minus 50%‐condition contrast in stimulus trials (panel d). Colour maps display the difference in ERP amplitude over time, broken down by electrode. Electrode numbers, broadly, begin at left frontal sites, ascending counter clockwise, first to posterior sites and then to right frontal sites. Statistically significant clusters (p < .05) are shown as opaque, while nonsignificant sampling points are shown as transparent.

FIGURE 4

Principal component analysis (PCA) omission components in chronological order (a–i). Plots show difference waves (condition minus motor) for reconstructed PCA (opaque) and the original event‐related potentials (ERPs) including 95% CIs (transparent) at highlighted (yellow) electrodes.

FIGURE 5

First stimulus‐evoked components in chronological order (a–c). Plots show difference wave (condition minus motor) for reconstructed principal component analysis (PCA) (opaque) and the original event‐related potentials (ERPs) including 95% CIs (transparent) at highlighted (yellow) electrodes.

FIGURE 6

Comparison of topographies between stimulus‐evoked component 5 (88%‐condition and 50%‐condition) and omission component 1 (88%‐condition). Topographies show principal component analysis (PCA) activations at peak latency.