Further evidence for selective difficulty of upward eye pursuit in juvenile monkeys: effects of optokinetic stimulation, static roll tilt, and active head movements

Abstract

The smooth-pursuit system moves the eyes in space accurately to track slowly moving objects of interest despite visual inputs from the moving background and/or vestibular inputs during head movements. Recently, our laboratory has shown that young primates exhibit asymmetric eye movements during vertical pursuit across a textured background; upward eye velocity gain is reduced. To further understand the nature of this asymmetry, we performed three series of experiments in young monkeys. In Experiment 1, we examined whether this asymmetry was due to an un-compensated downward optokinetic reflex induced by the textured background as it moves across the retina in the opposite direction of the pursuit eye movements. For this, we examined the monkeys’ ability to fixate a stationary spot in space during movement of the textured background and compared it with vertical pursuit across the stationary textured background. We also examined gains of optokinetic eye movements induced by downward motion of the textured background during upward pursuit. In both task conditions, gains of downward eye velocity induced by the textured background were too small to explain reduced upward eye velocity gains. In Experiment 2, we examined whether the frame of reference for low-velocity, upward pursuit was orbital or earth vertical. To test this, we first applied static tilt in the roll plane until the animals were nearly positioned on their side in order to dissociate vertical or horizontal eye movements in the orbit from those in space. Deficits were observed for upward pursuit in the orbit but not in space. In Experiment 3, we tested whether asymmetry was observed during head-free pursuit that requires coordination between eye and head movements. Asymmetry in vertical eye velocity gains was still observed during head-free pursuit although it was not observed in vertical head velocity. These results, taken together, suggest that the asymmetric eye movements during vertical pursuit are specific for upward, primarily eye pursuit in the orbit

Activity of pursuit neurons in the caudal part of the frontal eye fields during static roll-tilt

“…Smooth-pursuit gains of the two monkeys during upright posture and static roll-tilt were similar to those described previously (Kasahara et al 2006). …”

“…These monkeys were the same monkeys used in previous studies (Fukushima et al 2004;Kasahara et al 2006). All procedures were performed in strict compliance with the Guide for the Care and Use of Laboratory Animals (DHEW Publication #NIH85-23, 1985).…”

“…Specific protocols were approved by the Animal Care and Use Committee of Hokkaido University School of Medicine. Methods for animal preparation, training and recording were similar to previous studies (Fukushima et al 2000;Kasahara et al 2006), and therefore are summarized here only briefly. A scleral search coil was implanted on each eye (Fuchs and Robinson 1966).…”

“…The computer monitor and the primate chair together with the monkey and the coil frame for detection of eye movements were tilted in the roll plane (around the interaural midpoint) to 40° or 60° from the earth vertical (either rightwards or leftwards, e.g., Fig. 1b, f), similar to previous studies (Kasahara et al 2006). Extracellular recordings were made in the left peri-arcuate sulcus region at Ant.…”

Latency of vestibular responses of pursuit neurons in the caudal frontal eye fields to whole body rotation

“…The inter-aural midpoint of the animals' heads was positioned close to the axis of horizontal rotation. The target was a laser spot that was back-projected onto the tangent screen 75 cm in front of the animals' eyes (monkey C, Fukushima et al 2000Fukushima et al , 2002a and a 22-inch computer display (Sony) positioned 60 cm in front of the animals' eyes (monkeys SI and SH; e.g., Kasahara et al 2006). Once pursuit-responsive single neurons were encountered, smooth pursuit responses were tested in 4 planes (vertical, horizontal and two oblique planes at 45° angles) to determine the preferred direction.…”