Expansion of direction space around the cardinal axes revealed by smooth pursuit eye movements.

It is well established that perceptual direction discrimination shows an oblique effect; thresholds are higher for motion along diagonal directions than for motion along cardinal directions. Here, we compare simultaneous direction judgments and pursuit responses for the same motion stimuli and find that both pursuit and perceptual thresholds show similar anisotropies. The pursuit oblique effect is robust under a wide range of experimental manipulations, being largely resistant to changes in trajectory (radial versus tangential motion), speed (10 versus 25 deg/s), directional uncertainty (blocked versus randomly interleaved), and cognitive state (tracking alone versus concurrent tracking and perceptual tasks). Our data show that the pursuit oblique effect is caused by an effective expansion of direction space surrounding the cardinal directions and the requisite compression of space for other directions. This expansion suggests that the directions around the cardinal directions are in some way overrepresented in the visual cortical pathways that drive both smooth pursuit and perception.

Human discrimination of visual direction of motion with and without smooth pursuit eye movements.

It has long been known that ocular pursuit of a moving target has a major influence on its perceived speed (Aubert, 1886; Fleischl, 1882). However, little is known about the effect of smooth pursuit on the perception of target direction. Here we compare the precision of human visual-direction judgments under two oculomotor conditions (pursuit vs. fixation). We also examine the impact of stimulus duration (200 ms vs. ~800 ms) and absolute direction (cardinal vs. oblique). Our main finding is that direction discrimination thresholds in the fixation and pursuit conditions are indistinguishable. Furthermore, the two oculomotor conditions showed oblique effects of similar magnitudes. These data suggest that the neural direction signals supporting perception are the same with or without pursuit, despite remarkably different retinal stimulation. During fixation, the stimulus information is restricted to large, purely peripheral retinal motion, while during steady-state pursuit, the stimulus information consists of small, unreliable foveal retinal motion and a large efference-copy signal. A parsimonious explanation of our findings is that the signal limiting the precision of direction judgments is a neural estimate of target motion in head-centered (or world-centered) coordinates (i.e., a combined retinal and eye motion signal) as found in the medial superior temporal area (MST), and not simply an estimate of retinal motion as found in the middle temporal area (MT).

LGN input to simple cells and contrast-invariant orientation tuning: an analysis.

We develop a new analysis of the lateral geniculate nucleus (LGN) input to a cortical simple cell, demonstrating that this input is the sum of two terms, a linear term and a nonlinear term. In response to a drifting grating, the linear term represents the temporal modulation of input, and the nonlinear term represents the mean input. The nonlinear term, which grows with stimulus contrast, has been neglected in many previous models of simple cell response. We then analyze two scenarios by which contrast-invariance of orientation tuning may arise. In the first scenario, at larger contrasts, the nonlinear part of the LGN input, in combination with strong push-pull inhibition, counteracts the nonlinear effects of cortical spike threshold, giving the result that orientation tuning scales with contrast. In the second scenario, at low contrasts, the nonlinear component of LGN input is negligible, and noise smooths the nonlinearity of spike threshold so that the input-output function approximates a power-law function. These scenarios can be combined to yield contrast-invariant tuning over the full range of stimulus contrast. The model clarifies the contribution of LGN nonlinearities to the orientation tuning of simple cells and demonstrates how these nonlinearities may impact different models of contrast-invariant tuning.