Disrupting the experience of control in the human brain: pre-supplementary motor area contributes to the sense of agency

Abstract

The feeling of controlling events through one's actions is fundamental to human experience, but its neural basis remains unclear. This 'sense of agency' (SoA) can be measured quantitatively as a temporal linkage between voluntary actions and their external effects. We investigated the brain areas underlying this aspect of action awareness by using theta-burst stimulation to locally and reversibly disrupt human brain function. Disruption of the pre-supplementary motor area (pre-SMA), a key structure for preparation and initiation of a voluntary action, was shown to reduce the temporal linkage between a voluntary key-press action and a subsequent electrocutaneous stimulus. In contrast, disruption of the sensorimotor cortex, which processes signals more directly related to action execution and sensory feedback, had no significant effect. Our results provide the first direct evidence of a pre-SMA contribution to SoA.

Figure 1.

(a) Experimental set-up used in the study. See text for details. (b) Putative sites of cTBS stimulation (based on neuro-navigation in a separate group of three participants).

Figure 2.

(a) Upper row: in experimental conditions, actions were followed by shocks 250 ms later. Lower three rows: changes in the perceived time of actions and effects following cTBS in each condition. Black circles indicate the mean perceived time of actions, dashed vertical lines indicate the baseline judgements of actions in that session. Grey triangles indicate the mean perceived time of shocks, and dashed vertical lines indicate baseline shock judgements in that session. Numbers indicate the size of the shift in ms. Note the reduced binding following pre-SMA cTBS. (b) Mean overall binding between action and effect (action shift minus shock shift) in ms for each site of stimulation. Bars represent standard error of the mean across participants. **p < 0.01.