Persistence of the dark-background-contingent gaze upshift during visual fixations of rhesus monkeys

During visual fixations, the eyes are directed so that the image of the target (object of interest) falls on the fovea. An exception to this rule was described in macaque monkeys (though not in humans): dark background induces a gaze shift upwards, sometimes large enough to shift the target's image off the fovea. In this article we address an aspect not previously rigorously studied, the time course of the upshift. The time course is critical for determining whether the upshift is indeed an attribute of visual fixation or, alternatively, of saccades that precede the fixation. These alternatives lead to contrasting predictions regarding the time course of the upshift (durable if the upshift is an attribute of fixation, transient if caused by saccades). We studied visual fixations with dark and bright background in three monkeys. We confined ourselves to a single upshift-inducing session in each monkey so as not to study changes in the upshift caused by training. Already at their first sessions, all monkeys showed clear upshift. During the first 0.5 s after the eye reached the vicinity of the target, the upshift was on average larger, but also more variable, than later in the trial; this initial high value 1) strongly depended on target location and was maximal at locations high on the screen, and 2) appears to reflect mostly the intervals between the primary and correction saccades. Subsequently, the upshift stabilized and remained constant, well above zero, throughout the 2-s fixation interval. Thus there is a persistent background-contingent upshift genuinely of visual fixation.

Deficits in Saccades and Fixation During Muscimol Inactivation of the Caudal Fastigial Nucleus in the Rhesus Monkey

The caudal fastigial nucleus (cFN) is a major nucleus by which the cerebellum influences the accuracy of saccades. In head-restrained monkeys generating saccades from a fixation light-emitting diode (LED) toward a flashed target LED, we analyzed the effects of unilateral pharmacological inactivation of cFN on horizontal, vertical, and oblique saccades. When animals were viewing the fixation LED, usually after one or more correction saccades, the positions of the eyes were slightly offset in comparison with the positions maintained before the injection (average offset = 1.1°). The offset was ipsilateral to the injected side and did not depend on the target location. The horizontal component of all ipsilesional saccades was hypermetric and associated with a 32–42% increase in the amplitude of the deceleration displacement without significant change in the amplitude of the acceleration displacement. The horizontal component of all contralesional saccades was hypometric and associated with a decrease in the peak velocity and in the acceleration amplitude (30–35% decrease) without significant change in the deceleration amplitude. The amplitude of vertical saccades was not systematically affected, but their trajectory was always deviated toward the injected side. They missed the target with an error that depended on saccade duration or amplitude. If any, the effects of muscimol injections on the vertical component of oblique saccades were very small. The changes in fixation and the dysmetria are both viewed as consequences of an impairment in the cFN bilateral influence on the burst neurons located in the left and right brain stem.

Orienting Gaze Shifts During Muscimol Inactivation of Caudal Fastigial Nucleus in the Cat. I. Gaze Dysmetria

Goffart, Laurent and Denis Pélisson. Orienting gaze shifts during muscimol inactivation of caudal fastigial nucleus in the cat. I. Gaze dysmetria. J. Neurophysiol. 79: 1942–1958, 1998. The cerebellar control of orienting behavior toward visual targets was studied in the head-unrestrained cat by analyzing the deficits of saccadic gaze shifts after unilateral injection of muscimol in the caudal part of the fastigial nucleus (cFN). Gaze shifts are rendered strongly inaccurate by muscimol cFN inactivation. The characteristics of gaze dysmetria are specific to the direction of the movement with respect to the inactivated cFN. Gaze shifts directed toward the injected side are hypermetric. Irrespective of their starting position, all these ipsiversive gaze shifts overshoot the target by a constant horizontal error (or bias) to terminate at a “shifted goal” location. In particular, when gaze is directed initially at the future target's location, a response with an amplitude corresponding to the bias moves gaze away from the actual target. Additionally, when gaze is initially in between the target and this shifted goal location, the response again is directed toward the latter. This deficit of ipsiversive gaze shifts is characterized by a consistent increase in the y intercept of the relationship between horizontal gaze amplitude and horizontal retinal error. Slight increases in the slope sometimes are observed as well. Contraversive gaze shifts are markedly hypometric and, in contrast to ipsiversive responses, they do not converge onto a shifted goal but rather underestimate target eccentricity in a proportional way. This is reflected by a decrease in the slope of the relationship between horizontal gaze amplitude and horizontal retinal error, with, for some experiments, a moderate change in the y-intercept value. The same deficits are observed in a different setup, which permits the control of initial gaze position. Correction saccades rarely are observed when visual feedback is eliminated on initiation of the primary orienting response; instead, they occur frequently when the target remains visible. Like the primary contraversive saccades, they are hypometric and the ever-decreasing series of three to five correction saccades reduces the gaze fixation error but often does not completely eliminate it. We measured the position of gaze after the final correction saccade and found that fixation of a visible target is still shifted toward the inactivated cFN by 4.9 ± 2.4°. This fixation offset is correlated to, but on average 54% smaller than, the hypermetric bias of ipsiversive responses measured in the same experiments. In conclusion, the cFN contributes to the control of saccadic shifts of the visual axis toward a visual target. The hypometria of contraversive gaze shifts suggests a cFN role in adjusting a gain in the translation of retinal signals into gaze motor commands. On the basis of the convergence of ipsiversive gaze shifts onto a shifted goal, the straightness of gaze trajectory during these responses and the production of misdirected or inappropriately initiated responses toward this shifted goal, we propose that the cFN influences the processes that specify the goal of ipsiversive gaze shifts.