Extraocular muscle afferent signals modulate visual attention

Abstract

Purpose: Extraocular muscle afferent signals contribute to oculomotor control and visual localization. Prompted by the close links between the oculomotor and attention systems, it was investigated whether these proprioceptive signals also modulated the allocation of attention in space.

Methods: A suction sclera contact lens was used to impose an eye rotation on the nonviewing, dominant eye. With their viewing, nondominant eye, participants (n = 4) fixated centrally and detected targets presented at 5° in the left or right visual hemifield. The position of the viewing eye was monitored throughout the experiment. As a control, visual localization was tested using finger pointing without visual feedback of the hand, whereas the nonviewing eye remained deviated.

Results: The sustained passive rotation of the occluded, dominant eye, while the other eye maintained central fixation, resulted in a lateralized change in the detectability of visual targets. In all participants, the advantage in speed and accuracy for detecting right versus left hemifield targets that occurred during a sustained rightward eye rotation of the dominant eye was reduced or reversed by a leftward eye rotation. The control experiment confirmed that the eye deviation procedure caused pointing errors consistent with an approximately 2° shift in perceived eye position, in the direction of rotation of the nonviewing eye.

Conclusions: With the caveat of the small number of participants, these results suggest that extraocular muscle afferent signals modulate the deployment of attention in visual space.

Figure 1.

The experiment design. The design was 2 × 2 factorial with factors: (1) The side of rotation of the nonviewing eye, left (A, C) or right (B, D); (2) The visual hemifield of target presentation, left (A, B) or right (C, D). The dashed line indicates the perceived direction of gaze in the viewing eye, shifted approximately 2° in the direction of rotation of the nonviewing eye (see Results section). The hypothesis was that visual sensitivity will increase in the same direction (arrow).

Figure 2.

Reduced or reversed right minus left gradient in visual detection when the nonviewing eye is rotated to the left compared with the right. The laterality index was calculated as (H_R − H_L)/(H_R + H_L), where H_R and H_L were hit rates for right and left targets, respectively, and for reaction times (RT_L − RT_R)/(RT_R + RT_L). The index has values between +1 and −1; the more positive the value, the larger the rightward bias and the more negative, the larger the leftward bias. The symbols correspond to each participant 1, █, 2, ⧫, 3, ×, 4, ○. Participants 3 and 4 were naïve to the purpose of the experiment.