Smooth Pursuit-Related Information Processing in Frontal Eye Field Neurons that Project to the NRTP

Abstract

The cortical pursuit system begins the process of transforming visual signals into commands for smooth pursuit (SP) eye movements. The frontal eye field (FEF), located in the fundus of arcuate sulcus, is known to play a role in SP and gaze pursuit movements. This role is supported, at least in part, by FEF projections to the rostral nucleus reticularis tegmenti pontis (rNRTP), which in turn projects heavily to the cerebellar vermis. However, the functional characteristics of SP-related FEF neurons that project to rNRTP have never been described. Therefore, we used microelectrical stimulation (ES) to deliver single pulses (50–200 μA, 200-μs duration) in rNRTP to antidromically activate FEF neurons. We estimated the eye or retinal error motion sensitivity (position, velocity, and acceleration) of FEF neurons during SP using multiple linear regression modeling. FEF neurons that projected to rNRTP were most sensitive to eye acceleration. In contrast, FEF neurons not activated following ES of rNRTP were often most sensitive to eye velocity. In similar modeling studies, we found that rNRTP neurons were also biased toward eye acceleration. Therefore, our results suggest that neurons in the FEF–rNRTP pathway carry signals that could play a primary role in initiation of SP.

Suppression of smooth pursuit eye movements induced by electrical stimulation of the monkey frontal eye field

“…In addition, the FEF has been shown to contribute to the generation of smooth pursuit eye movements Ebata et al 2004;MacAvoy et al 1991;Tanaka and Fukushima 1998;Tian and Lynch 1996). The smooth pursuit subregion of the FEF is known to be a discrete region that is near the spur of the arcuate sulcus and has been reported to play a role in the initiation and maintenance of smooth pursuit (Ono and Mustari 2009;Tanaka and Lisberger 2002a). The pathways for pursuit that originate in the FEF constitute a parallel system with the traditional cortico-ponto-cerebellar pathways for pursuit that originate in the middle temporal area (MT) and medial superior temporal area (MST) (see reviews: Keller and Heinen 1991;Lisberger et al 1987).…”

Inactivation and stimulation of the frontal pursuit area change pursuit metrics without affecting pursuit target selection

“…The FPA is therefore well-positioned to transform motion signals into eye movement commands. Indeed, the FPA contains both cells that fire transiently at pursuit onset and cells that maintain their activity throughout the pursuit response (Ono and Mustari 2009). This makes the FPA suitable to influence every phrase of the smooth pursuit response, consistent with our inactivation results.…”

“…Neurons in this area exhibit directionally selective activity during pursuit (MacAvoy et al 1991;Tanaka and Lisberger 2002b). FPA neurons show a range of activity patterns during pursuit in the preferred direction, ranging from phasic bursts of activity at pursuit onset to slowly developing, tonic activity that is sustained throughout the pursuit response (Ono and Mustari 2009). Many FPA neurons also receive vestibular inputs (Akao et al 2007Fukushima et al 2000) that may be important for coordinating smooth eye movements during whole body movements.…”

“…Many FPA neurons also receive vestibular inputs (Akao et al 2007Fukushima et al 2000) that may be important for coordinating smooth eye movements during whole body movements. FPA neurons with different activity patterns tend to project to different precerebellar nuclei in the pons (Ono and Mustari 2009), implying that the descending output form the FPA controls multiple components of the pursuit response. The FPA also has dense reciprocal connections to both cortical areas involved in processing visual motion, such as the medial superior temporal area (MST) (Dürsteler and Wurtz 1988;Newsome et al 1988), and areas involved in cognitive aspects of pursuit control, such as the supplementary eye fields (SEF) (Heinen 1995;Lynch 1995, 1996).…”

The Response of MSTd Neurons to Perturbations in Target Motion During Ongoing Smooth-Pursuit Eye Movements

“…Several studies have put forward the suggestion that extraretinal signals play an important role in pursuit maintenance (Newsome et al 1988;Nuding et al 2008;Ono et al 2009). This is quite plausible despite the large delay of the extraretinal component in MSTd neurons.…”