Eye position representation in human anterior parietal cortex

Abstract

Eye position helps locate visual targets relative to one's own body and modulates the distribution of attention in visual space. Whereas in the monkey, proprioceptive eye position signals have been recorded in the somatosensory cortex, in humans, no brain site has yet been associated with eye position. We aimed to disrupt the proprioceptive representation of the right eye in the left somatosensory cortex, presumably located near the representation of the right hand, using repetitive transcranial magnetic stimulation (rTMS). Head-fixed subjects reported their perceived visual straight-ahead position using both left and right eye monocular vision, before and after 15 min of 1 Hz rTMS. rTMS over left somatosensory but not over left motor cortex shifted the perceived visual straight ahead to the left, whereas nonvisual detection of body midline was unchanged for either brain area. These results can be explained by the underestimation of the angle of gaze of the right eye when fixating the target. To link this effect more tightly to an altered ocular proprioception, we applied a passive deviation to the right eye before the visual straight-ahead task. Passive eye displacement modulated the shift in the perceived straight ahead induced by somatosensory rTMS, without affecting the perceived straight ahead at baseline or after motor cortex rTMS. We conclude that the anterior parietal cortex in humans encodes eye position and that this signal has a proprioceptive component.

Figure 1.

rTMS induced change in the perception of straight ahead (mean ± SE) in left and right monocular vision (open bars, anterior parietal cortex; filled bars, motor cortex; push, passive eye movement in medial direction applied to the closed right eye before the task).

Figure 2.

An underestimation (β) of the rotation of the right eye at fixation shifts the perceived location of the target to the right and thus shifts the reported position of a target perceived as straight ahead to the left (black arrow). A mechanism for detecting perceived straight ahead in monocular vision is assumed based on equaling the felt angle of rotation of the two eyes (α_R and α_L); the actual angle of rotation of the right eye is (α_R + β). An underestimated passive rotation of the right eye toward the left would also lead to a leftward shift of perceived straight ahead.