The effects of action-based predictions in early visual cortex

Abstract

During voluntary movement, predictions about the sensory consequences of an action typically result in reduced sensory sensitivity. The forward model theory proposes that this reduced sensitivity is due to neural suppression or cancellation of sensory action outcomes. However, recently this theory has been challenged by three alternative theories: the pre-activation account, sharpening, and the opposing processes theory. In this fMRI study, we directly tested and compared these four theories using univariate and multivariate analyses both prior to and during stimulus presentation. Participants performed a visual orientation discrimination task on two sequentially presented gratings, which were either presented automatically (passive condition) or triggered by their own button press (active condition). Auditory cues at trial onset indicated the overall grating orientation, followed by a preparatory phase in which participants anticipated the upcoming stimuli. During this phase, the predicted stimulus orientation was decodable from early visual cortex activity in both active and passive conditions at levels significantly above chance, indicating pre-activation of the predicted orientation, but with no difference between active and passive conditions. BOLD responses did not emerge earlier in active conditions, arguing against the pre-activation theory. During stimulus presentation, actively generated stimuli elicited larger BOLD responses than passively presented ones, contradicting the forward model theory, which predicts overall response suppression. Decoding accuracy did not differ between conditions, inconsistent with the sharpening hypothesis, which predicts enhanced neural precision for actively generated stimuli. Instead, our findings align most closely with the opposing processes theory, which posits pre-activation in both conditions. However, the stronger BOLD response for actively generated stimuli is not predicted by any existing theory, suggesting that additional mechanisms--such as heightened attention or motor-related enhancement--may contribute to sensory processing during self-initiated actions.