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Several regions of the brain are involved in smooth-pursuit eye movement (SPEM) control, including the cortical areas MST (medial superior temporal) and FEF (frontal eye field). It has been shown that the eye-movement responses to a brief perturbation of the visual target during ongoing pursuit increases with higher pursuit velocities. To further investigate the underlying neuronal mechanism of this nonlinear dynamic gain control and the contributions of different cortical areas to it, we recorded from MSTd (dorsal division of the MST area) neurons in behaving monkeys (Macaca mulatta) during step-ramp SPEM (5-20 degrees /s) with and without superimposed target perturbation (one cycle, 5 Hz, +/-10 degrees /s). Smooth-pursuit-related MSTd neurons started to increase their activity on average 127 ms after eye-movement onset. Target perturbation consistently led to larger eye-movement responses and decreasing latencies with increasing ramp velocities, as predicted by dynamic gain control. For 36% of the smooth-pursuit-related MSTd neurons the eye-movement perturbation was accompanied by detectable changes in neuronal activity with a latency of 102 ms, with respect to the eye-movement response. The remaining smooth-pursuit-related MSTd neurons (64%) did not reflect the eye-movement perturbation. For the large majority of cases this finding could be predicted by the dynamic properties of the step-ramp responses. Almost all these MSTd neurons had large visual receptive fields responding to motion in preferred directions opposite to the optimal SPEM stimulus. Based on these findings it is unlikely that MSTd plays a major role for dynamic gain control and initiation of the perturbation response. However, neurons in MSTd could still participate in SPEM maintenance. Due to their visual field properties they could also play a role in other functions such as self-motion perception.

Smooth pursuit eye movements are used to continuously track slowly moving visual objects. A peculiar property of the smooth pursuit system is the nonlinear increase in sensitivity to changes in target motion with increasing pursuit velocities. We investigated the role of the frontal eye fields (FEFs) in this dynamic gain control mechanism by application of transcranial magnetic stimulation. Subjects were required to pursue a slowly moving visual target whose motion consisted of 2 components: a constant velocity component at 4 different velocities (0, 8, 16, and 24 deg/s) and a superimposed high-frequency sinusoidal oscillation (4 Hz, +/-8 deg/s). Magnetic stimulation of the FEFs reduced not only the overall gain of the system, but also the efficacy of the dynamic gain control. We thus provide the first direct evidence that the FEF population is significantly involved in the nonlinear computation necessary for continuously adjusting the feedforward gain of the pursuit system. We discuss this with relation to current models of smooth pursuit.

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.

Two cortical areas that crucially contribute to the generation and maintenance of smooth pursuit eye movements (SPEM) are the medial superior temporal area (MST) and the pursuit area of the frontal eye fields (FEF). They both project to the brainstem premotor structures via different parallel pathways. A special property of the pursuit system is the increased sensitivity to retinal image motion for increasing pursuit velocities (dynamic gain control), which might be attributed to the FEF. On the other hand, MST is regarded as the main site for estimating the target velocity in space and therefore for maintaining an ongoing SPEM. However, neural activities in these areas during visually driven SPEM have not been fully understood. We present a simple model of smooth pursuit gain control that comprises population activities, as well as single unit sensitivities with respect to eye and retinal image motion in MST and FEF. We show that the nonlinear computation necessary for dynamic gain control may be accomplished by units that exhibit a curvilinear sensitivity to retinal image motion and eye velocity.

MSTd neurons in the behaving monkey were investigated during step-ramp smooth pursuit eye movements (SPEM), short perturbations of the small visual target during ongoing pursuit, and large-field visual stimulation inducing ocular following responses (OFR). Neurons responded with short latencies to visual motion during OFR. In contrast the non-retinal responses during SPEM and perturbations followed the eye movements by 100-150 ms and were in the opposite direction to the OFR response. Often neurons were not modulated by the perturbation. Although, both the OFR and the perturbation response are involuntary eye movements due to visual motion, it seems very unlikely that these MSTd neurons with non-retinal responses are involved in their direct control. Based on these responses, we suggest that our MSTd neurons may code for gaze direction in space based on visual estimates of self-motion and extraretinal estimates of eye-in-head motion.