Area MSTd Neurons Encode Visual Stimuli in Eye Coordinates During Fixation and Pursuit

Abstract

Visual signals generated by self-motion are initially represented in retinal coordinates in the early parts of the visual system. Because this information can be used by an observer to navigate through the environment, it must be transformed into body or world coordinates at later stations of the visual-motor pathway. Neurons in the dorsal aspect of the medial superior temporal area (MSTd) are tuned to the focus of expansion (FOE) of the visual image. We performed experiments to determine whether focus tuning curves in area MSTd are represented in eye coordinates or in screen coordinates (which could be head, body, or world-centered in the head-fixed paradigm used). Because MSTd neurons adjust their FOE tuning curves during pursuit eye movements to compensate for changes in pursuit and translation speed that distort the visual image, the coordinate frame was determined while the eyes were stationary (fixed gaze or simulated pursuit conditions) and while the eyes were moving (real pursuit condition). We recorded extracellular responses from 80 MSTd neurons in two rhesus monkeys (Macaca mulatta). We found that the FOE tuning curves of the overwhelming majority of neurons were aligned in an eye-centered coordinate frame in each of the experimental conditions [fixed gaze: 77/80 (96%); real pursuit: 77/80 (96%); simulated pursuit 74/80 (93%); t-test, P < 0.05]. These results indicate that MSTd neurons represent heading in an eye-centered coordinate frame both when the eyes are stationary and when they are moving. We also found that area MSTd demonstrates significant eye position gain modulation of response fields much like its posterior parietal neighbors.