Abstract
Smooth pursuit eye movements have frequently been used to model sensorimotor transformations in the brain. In particular, the initiation phase of pursuit can be understood as a transformation of a sensory estimate of target velocity into an eye rotation. Despite careful laboratory controls on the stimulus conditions, pursuit eye movements are frequently observed to exhibit considerable trial-to-trial variability. In theory, this variability can be caused by the variability in sensory representation of target motion, or by the variability in the transformation of sensory information to motor commands. Previous work has shown that neural variability in the middle temporal (MT) area is likely propagated to the oculomotor command, and there is evidence to suggest that the magnitude of this variability is sufficient to account for the variability of pursuit initiation. This line of reasoning presumes that the MT population is homogeneous with respect to its contribution to pursuit initiation. At the same time, there is evidence that pursuit initiation is strongly linked to a subpopulation of MT neurons (those with strong surround suppression) that collectively generate less motor variability. To distinguish between these possibilities, we have combined human psychophysics, monkey electrophysiology, and computational modeling to examine how the pursuit system reads out the MT population during pursuit initiation. We find that the psychophysical data are best accounted for by a model that gives stronger weight to surround-suppressed MT neurons, suggesting that variability in the initiation of pursuit could arise from multiple sources along the sensorimotor transformation.
Highlights
When an object of interest moves through the visual field, it can be tracked by an eye rotation that matches the target velocity
middle temporal (MT) neurons with surround suppression are more activated for stimuli of short duration, as necessarily occurs during the onset of pursuit, while non-surround-suppressed neurons respond poorly to brief stimuli (Churan et al, 2008; Tsui & Pack, 2011)
Through psychophysics experiments and computational modeling, we have provided additional evidence in this paper that MT neurons with surround suppression are likely to be the main contributors to smooth pursuit initiation
Summary
When an object of interest moves through the visual field, it can be tracked by an eye rotation that matches the target velocity. Such smooth pursuit eye movements serve to stabilize the image of a moving object on the retina (Robinson et al, 1986). The initiation phase of pursuit is relatively simple to understand, as the eye velocity during this time is mainly determined by the neural representation of the target motion. Smooth pursuit initiation can be modeled as a transformation of sensory information about target motion to a motor command that rotates the eye at the appropriate velocity (Ilg, 2008; Lisberger, 2010). Given its relatively well-known underlying neuronal basis, and the availability of precise eye tracking, smooth pursuit initiation provides a powerful model of neural coding
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