Eye muscle proprioception is represented bilaterally in the sensorimotor cortex

Abstract

The cortical representation of eye position is still uncertain. In the monkey a proprioceptive representation of the extraocular muscles (EOM) of an eye were recently found within the contralateral central sulcus. In humans, we have previously shown a change in the perceived position of the right eye after a virtual lesion with rTMS over the left somatosensory area. However, it is possible that the proprioceptive representation of the EOM extends to other brain sites, which were not examined in these previous studies. The aim of this fMRI study was to sample the whole brain to identify the proprioceptive representation for the left and the right eye separately. Data were acquired while passive eye movement was used to stimulate EOM proprioceptors in the absence of a motor command. We also controlled for the tactile stimulation of the eyelid by removing from the analysis voxels activated by eyelid touch alone. For either eye, the brain area commonly activated by passive and active eye movement was located bilaterally in the somatosensory area extending into the motor and premotor cytoarchitectonic areas. We suggest this is where EOM proprioception is processed. The bilateral representation for either eye contrasts with the contralateral representation of hand proprioception. We suggest that the proprioceptive representation of the two eyes next to each other in either somatosensory cortex and extending into the premotor cortex reflects the integrative nature of the eye position sense, which combines proprioceptive information across the two eyes with the efference copy of the oculomotor command.

Figure 1

Eye muscle proprioceptive representation. (a) Suprathreshold voxels (P = 0.05 corrected for multiple comparisons using FWE and (b) suprathreshold clusters (P = 0.05 corrected for multiple comparisons). The activations are defined by the conjunction between active and passive eye movement [(active‐rest) AND (passive‐rest)] after removing the voxels activated by tactile stimulation of the eyelid (touch‐rest). The threshold of the exclusive mask (touch‐rest) was 0.05 uncorrected. Top pannel: right eye proprioceptive representation, bottom pannel: left eye proprioceptive representation. For localization purposes the functional map is overlaid on a single‐subject structural MR‐template (SPM5).

Figure 2

Activity change across conditions at the peak activated voxels. For the right eye proprioceptive representation these voxels were located in (a) the ipsilateral (right) sensorimotor cortex (x, y, z) = (36, −14, 38), (b) the contralateral (left) sensorimotor cortex (x, y, z) = (−36, −16, 40), and (c) premotor cortex (x, y, z) = (44, −6, 44). For the left eye proprioceptive representation the only suprathreshold voxel was located in (d) the ipsilateral (left) sensorimotor cortex (x, y, z) = (−38, −12, 42). The bars show percent BOLD change in the active, passive, and touch conditions relative to mean brain activity during the rest condition. The error bars show one standard error.

Figure 3

Eye muscle proprioceptive and motor representation during active eye movements The statistical parametric map was defined by the contrast (active‐rest) and thresholded at P = 0.05 corrected for multiple comparisons using FWE. Glass brain representation in three orthogonal projections (left side of the brain is shown to the left).