Response properties of Frontal Eye Field (FEF) neurons during volitional smooth pursuit and optokinetic eye movements

Abstract

Purpose: Volitional smooth pursuit (SP) eye movements are used to maintain the image of a moving target on the fovea. Our studies seek to define the relationship of FEF neuronal response to components of eye or visual motion during volitional and reflex driven eye movements.

Methods: Our studies were conducted in 3 monkeys (M. mulatta) trained to perform SP, fixation during visual motion and reflex ocular following in response to sudden movement of a large-field pattern. We tested volitional SP by requiring the monkeys to track a small diameter target (0.1°) moving in step-ramp (SR) or band-limited white-noise (WN) trajectories. Visual responses of FEF neurons were tested during large-field (50x50°) visual motion during fixation and without a fixation point to elicit an ocular following response (OFR). The location of the FEF was confirmed using structural MRI. Extracellular single unit recording was accomplished using tungsten microelectrodes and standard signal processing methods. Eye movements were recorded using electromagnetic methods employing scleral search coils.

Results: We recorded FEF neurons in 3 monkeys using SR and fixation during visual motion conditions. One of the monkeys was also tested during WN target or large-field visual motion conditions. We estimated the contributions of visual motion (velocity and acceleration) and eye motion (velocity and acceleration) to neuronal response using multiple linear regression (LR) modeling or an information theoretic (IT) approach. The LR models determined the optimal eye movement latency based on the largest coefficient of determination. The IT determines the latency based on maximizing mutual information between response variables. Both LR and IT modeling revealed that the majority of our FEF neurons are sensitive to eye velocity or acceleration. Most FEF units tested during SR or OFR conditions were related to eye motion (velocity or acceleration). SP units had response latencies that typically led the onset of tracking. FEF neurons that had a preference for retinal image velocity only had a weak response for eye motion.

Conclusions: The FEF contains neurons that respond during volitional and reflex driven behaviors. Most FEF neurons active during SP are sensitive to eye velocity or eye acceleration. These properties could play a role in initiation and maintenance of SP.

Keywords: 525 eye movements: saccades and pursuits • 508 electrophysiology: non-clinical