Proprioception contributes to the sense of agency during visual observation of hand movements: evidence from temporal judgments of action

Abstract

The ability to recognize visually one's own movement is important for motor control and, through attribution of agency, for social interactions. Agency of actions may be decided by comparisons of visual feedback, efferent signals, and proprioceptive inputs. Because the ability to identify one's own visual feedback from passive movements is decreased relative to active movements, or in some cases is even absent, the role of proprioception in self-recognition has been questioned. Proprioception during passive and active movements may, however, differ, and so to address any role for proprioception in the sense of agency, the active movement condition must be examined. Here we tested a chronically deafferented man (I.W.) and an age-matched group of six healthy controls in a task requiring judgement of the timing of action. Subjects performed finger movements and watched a visual cursor that moved either synchronously or asynchronously with a random delay, and reported whether or not they felt they controlled the cursor. Movement accuracy was matched between groups. In the absence of proprioception, I.W. was less able than the control group to discriminate self- from computer-produced cursor movement based on the timing of movement. In a control visual discrimination task with concurrent similar finger movements but no agency detection, I.W. was unimpaired, suggesting that this effect was task specific. We conclude that proprioception does contribute to the visual identification of ownership during active movements and, thus, to the sense of agency.

Figure 1. The setup for finger movements

The subjects had their index finger on a sliding mouse that moved on a rectangular active area of size 24×30 mm surrounded by a frame. The finger was fixed to the mouse using surgical tape. For each trial, the subjects moved the finger back or forth, along the y-axis of the mouse, in a straight line between the proximal and distal edge of the mouse area (24 mm). A plastic support attached to the mouse prevented movement along the x axis.

Figure 2. Diagram of the two tasks

At the start of each trial, a cursor was presented at the centre of the computer screen and the subject moved a sliding computer mouse back or forth, from edge to edge (the solid black lines in the right images). A plastic sheet prevented direct vision of the forearm and hand. During the ownership task (A), the cursor moved along a horizontal line either to the left or right, at random, and stopped at the lateral edge of the screen. Cursor and finger could either move synchronously or asynchronously, with a random delay. Because there was no spatial correspondence between cursor and mouse, identification of ownership relied entirely on timing signals. During the cursor jump task (B) the cursor jumped briefly to the side - left or right, at random - and back. The arrows show the direction of movement in a sample trial. The coordinate system show x and y axes in register with the set-up presented in figure 1.

Figure 3. Sample trajectories from synchronous (dashed line) and asynchronous (continuous line) trials

The plots show the cursor trajectory across the screen against time, with the asynchronous trials using cursor trajectories replayed from previous trials (see Methods). A: typical trials from subject IW. B: Typical trials from a control subject. The arrows indicate the onset of mouse movement.

Figure 4. Accuracy of detecting ownership of cursor movement and direction of cursor jump

The mean data for the proprioceptively deafferented subject IW (line) and a boxplot (median, inter-quartile interval and range) for 6 healthy controls are shown.

Figure 5. Cumulative probability of a false ‘me’ response as a function of asynchrony

The scatterplot shows all valid asynchronous trials in IW (●) and for all six control subjects (○).