Eye proprioception used for visual localization only if in conflict with the oculomotor plan

Abstract

Both the corollary discharge of the oculomotor command and eye muscle proprioception provide eye position information to the brain. Two contradictory models have been suggested about how these two sources contribute to visual localization: (1) only the efference copy is used whereas proprioception is a slow recalibrator of the forward model, and (2) both signals are used together as a weighted average. We had the opportunity to test these hypotheses in a patient (R.W.) with a circumscribed lesion of the right postcentral gyrus that overlapped the human eye proprioceptive representation. R.W. was as accurate and precise as the control group (n = 19) in locating a lit LED that she viewed through the eye contralateral to the lesion. However, when the task was preceded by a brief (<1 s), gentle push to the closed eye, which perturbed eye position and stimulated eye proprioceptors in the absence of a motor command, R.W.'s accuracy significantly decreased compared with both her own baseline and the healthy control group. The data suggest that in normal conditions, eye proprioception is not used for visual localization. Eye proprioception is, however, continuously monitored to be incorporated into the eye position estimate when a mismatch with the efference copy of the motor command is detected. Our result thus supports the first model and, furthermore, identifies the limits for its operation.

Figure 1.

The lesion of patient R.W. overlaps with the Brodmann Areas 3a, 1 and 2 and the cortical projection for eye proprioception in the postcentral gyrus. The lesion (arrow) is shown in 3 orthogonal projections through the coordinates (x, y, z = 34, −32, 42) on a T1-weighted MR-image of the patient's brain normalized to the MNI space (A–D). In B, the color overlays show the probabilistic atlas for area 3a (yellow), 2 (blue), and 1 (green), probabilities 10–100%. The red overlay shows the representation of eye proprioception for the left (C) and the right (D) eye muscles as identified by fMRI in a group of 18 healthy subjects (Balslev et al., 2011). The threshold for this functional overlay is z-score >2.61, p < 0.005, uncorrected for multiple comparisons.

Figure 2.

Accuracy and precision for locating an LED relative to the body in monocular vision and in darkness. Mean error (A, B) and SD (C, D) for the patient and a group of 19 healthy controls are shown in baseline and in push condition, separately for the left eye (A, C) and right eye (B, D). Error bars represent one SD. The arrow on the x-axis label shows the direction of the push. Filled circles, patient; empty circles, controls; asterisk denotes a p value <0.05 for a single-case t test testing for a difference between the patient and the control group (N = 19).