Neural evidence for action-related somatosensory predictions

Abstract

The tactile consequences of self-initiated movements are thought to be predicted by a forward model, yet the precise neural implementation of these predictions remains unclear. In non-motor contexts, expectations are thought to activate sensory neurons tuned towards the expected stimulus. This acts as a predictive template against which afferent sensory input is compared. It is unclear whether forward model predictions have a similar neural instantiation. Here we employed time-resolved multivariate decoding on human electroencephalography (EEG) during self-generated movements to examine the content of predictive neural activity. Human participants (males and females) performed index finger movements which were predictably paired with a vibration to either the index or ring finger of the opposite, passive hand. On some trials the tactile stimulus was unexpectedly omitted. Results revealed above-chance finger decoding in the pre-movement period supporting a predictive representation of expected stimulation location. As the movement approached, this predictive activity became similar to late-stage processing of a physical tactile stimulus. On omission trials, we found that despite the absence of afferent input, finger location could be decoded ∼120 ms after expected stimulus onset. This shows a stimulus-specific omission response. Together these findings indicate that self-generated movement pre-activates neurons tuned towards expected tactile consequences. Significance Statement Engaging effectively with the world relies on our ability to anticipate the sensory consequences of our own movements. To characterise how the brain encodes action-driven tactile predictions we recorded EEG while participants performed finger movements paired with vibrations to either the index or ring finger of the opposite hand. Crucially, we introduced unexpected omissions, where no stimulus followed the movement. Applying time-resolved EEG-decoding methods, we show that pre-movement neural activity encodes expected stimulation location. In addition, on omission trials, despite the absence of bottom-up stimulation, we could decode expected stimulation location. Such predictions of self-produced tactile events likely ensure accurate dissociation of self from other and promote a sense of agency over our own motor actions.