Neural computation of self-motion from optic flow in primate visual cortex

Abstract

Area MSTd is involved in the computation of heading direction from the focus of expansion (FOE) of the visual image. Our laboratory previously found that MSTd neurons adjust their focus tuning curves to compensate for shifts in the FOE produced by eye rotation (Bradley et al., 1996) as well as for changes in pursuit speed (Shenoy et al., 2002). The translation speed of an observer also affects the shift of the FOE. To investigate whether MSTd neurons can adjust their focus tuning curves to compensate for varying translation speeds, we recorded extracellular responses from 93 focus-tuned MSTd neurons in two rhesus monkeys (Macaca mulatta) performing pursuit eye movements across displays of varying translation speeds. We found that MSTd neurons had larger shifts in their tuning curves for slow translation speeds and smaller shifts for fast translation speeds. These shifts aligned the focus tuning curves with the true heading direction and not with the retinal position of the FOE. These results indicate that retinal cues related both to translation speed and extraretinal signals from pursuit eye movements are used by MSTd neurons to compute heading direction. Although there is much evidence that MSTd neurons are involved in heading computation, it was not known in which coordinate frame the tuning curves were represented. We performed a second set of experiments to determine whether focus tuning curves in MSTd were represented in eye, head, body, or world coordinates. The coordinate frame was determined while the eyes were stationary (fixed gaze, simulated pursuit condition) and while the eyes were moving (real pursuit condition). We recorded extracellular responses from 80 MSTd neurons and found that the FOE tuning curves of the overwhelming majority of neurons were aligned in an eye-centered coordinate frame as opposed to head, body, or world-centered coordinates (fixed gaze: 77/80 (96%); real pursuit: 77/80 (96%); simulated pursuit 74/80 (93%); t-test, p