Violating instructed human agency: An fMRI study on ocular tracking of biological and nonbiological motion stimuli

- Mismatch of agency belief and motion kinematics causes medial-frontal activation.
- In the oculomotor network, the supplementary eye fields mediate this mismatch.
- Activation is asymmetric as violating computer agency yields no additional activation.
- Occipito-temporal areas including V5 show a preference for biological motion.

Previous studies have shown that beliefs about the human origin of a stimulus are capable of modulating the coupling of perception and action. Such beliefs can be based on top-down recognition of the identity of an actor or bottom-up observation of the behavior of the stimulus. Instructed human agency has been shown to lead to superior tracking performance of a moving dot as compared to instructed computer agency, especially when the dot followed a biological velocity profile and thus matched the predicted movement, whereas a violation of instructed human agency by a nonbiological dot motion impaired oculomotor tracking (Zwickel et al., 2012). This suggests that the instructed agency biases the selection of predictive models on the movement trajectory of the dot motion. The aim of the present fMRI study was to examine the neural correlates of top-down and bottom-up modulations of perception-action couplings by manipulating the instructed agency (human action vs. computer-generated action) and the observable behavior of the stimulus (biological vs. nonbiological velocity profile). To this end, participants performed an oculomotor tracking task in an MRI environment. Oculomotor tracking activated areas of the eye movement network. A right-hemisphere occipito-temporal cluster comprising the motion-sensitive area V5 showed a preference for the biological as compared to the nonbiological velocity profile. Importantly, a mismatch between instructed human agency and a nonbiological velocity profile primarily activated medial-frontal areas comprising the frontal pole, the paracingulate gyrus, and the anterior cingulate gyrus, as well as the cerebellum and the supplementary eye field as part of the eye movement network. This mismatch effect was specific to the instructed human agency and did not occur in conditions with a mismatch between instructed computer agency and a biological velocity profile. Our results support the hypothesis that humans activate a specific predictive model for biological movements based on their own motor expertise. A violation of this predictive model causes costs as the movement needs to be corrected in accordance with incoming (nonbiological) sensory information.