A Theory of the Dual Pathways for Smooth Pursuit Based on Dynamic Gain Control

Abstract

The smooth pursuit eye movement (SPEM) system is much more sensitive to target motion perturbations during pursuit than during fixation. This sensitivity is commonly attributed to a dynamic gain control mechanism. Neither the neural substrate nor the functional architecture for this gain control has been fully revealed. There are at least two cortical areas that crucially contribute to smooth pursuit and are therefore eligible sites for dynamic gain control: the medial superior temporal area (MST) and the pursuit area of the frontal eye fields (FEFs), which both project to brain stem premotor structures via parallel pathways. The aim of this study was to develop a model of smooth pursuit based on behavioral, anatomical, and neurophysiological results to account for nonlinear dynamic gain control. Using a behavioral paradigm in humans consisting of a sinusoidal oscillation (4 Hz, +/-8 degrees/s) superimposed on a constant velocity target motion (0-24 degrees/s), we were able to identify relevant gain control parameters in the model. A salient feature of our model is the emergence of two parallel pathways from higher visual cortical to lower motor areas in the brain stem that correspond to the MST and FEF pathways. Detailed analysis of the model revealed that one pathway mainly carries eye velocity related signals, whereas the other is associated mostly with eye acceleration. From comparison with known neurophysiological results we conclude that the dynamic gain control can be attributed to the FEF pathway, whereas the MST pathway serves as the basic circuit for maintaining an ongoing SPEM.

Evidence for a retinal velocity memory underlying the direction of anticipatory smooth pursuit eye movements

“…In support of the second hypothesis, one possibility is that there exist two parallel projections within the pursuit circuitry to the brain stem, one originating from MST and the other from the frontal eye field (FEF) (Nuding et al 2008). Nuding et al (2008) suggested that the MST pathway serves as the basic circuit for maintaining an ongoing pursuit movement, while an FEF pathway is responsible for the dynamic gain control of pursuit (Nuding et al 2008;Tanaka and Lisberger 2001.…”

Adaptations of lateral hand movements to early and late visual occlusion in catching

“…It is well established in the literature on manual interception that hand velocity (and movement time) depends on target velocity (called velocity-coupling; Brenner et al 1998;Brouwer et al 2000Brouwer et al , 2002Brouwer et al , 2005Carnahan and McFadyen 1996;Fayt et al 1997;Smeets and Brenner 1995;van Donkelaar et al 1992). This velocity-coupling may reflect a dependency of the visuomotor gain on visual target velocity (Dessing et al 2002), reminiscent of variations in the visuomotor gain of the smooth pursuit system as a function of target velocity (Churchland and Lisberger 2002;Krauzlis and Lisberger 1994;Nuding et al 2008;Robinson 1965;Tanaka and Lisberger 2001). Importantly, recent findings also suggest that for smooth pursuit this gain seems to be updated on a trial-by-trial basis (Tabata et al 2008) in a direction similar to the effects of the preceding target's velocity observed here.…”

Neuronal responses in the cortical area MSTd during smooth pursuit and ocular following eye movements

“…However, while 93% of the tested neurons (n = 15) responded to LF perturbations, only 33% (of 55) responded during SP. Again, neuronal perturbation responses preceded changes in eye movement for LF, but lagged behind eye movement for SP.For model simulations, we extended our non-linear pursuit model [3] by appropriate temporal delays. The MSTbranch of the model contains an eye-movement related signal, which lags behind the eye by about the same amount as the eye lags behind target motion (120-135 ms vs. 128 ms neuronal delay).…”

“…However, about 35% of MSTd neurons also respond to smooth pursuit eye movements, which is difficult to reconcile in the context of self-motion perception. Here, we examined neuronal responses of 55 pursuit-sensitive MSTd neurons recorded in two awake macaque monkeys [2], and related these responses to a computational model of the smooth pursuit system [3].…”

“…For model simulations, we extended our non-linear pursuit model [3] by appropriate temporal delays. The MSTbranch of the model contains an eye-movement related signal, which lags behind the eye by about the same amount as the eye lags behind target motion (120-135 ms vs. 128 ms neuronal delay).…”