Shabtai Barash

Saccadic Dysmetria and Adaptation after Lesions of the Cerebellar Cortex

We studied the effects of small lesions of the oculomotor vermis of the cerebellar cortex on the ability of monkeys to execute and adapt saccadic eye movements. For saccades in one horizontal direction, the lesions led to an initial gross hypometria and a permanent abolition of the capacity for rapid adaptation. Mean saccade amplitude recovered from the initial hypometria, although variability remained high. A series of hundreds of repetitive saccades in the same direction resulted in gradual decrement of amplitude. Saccades in other directions were less strongly affected by the lesions. We suggest the following. (1) The cerebellar cortex is constantly recalibrating the saccadic system, thus compensating for rapid biomechanical changes such as might be caused by muscle fatigue. (2) A mechanism capable of slow recovery from dysmetria is revealed despite the permanent absence of rapid adaptation.

Reduced saccadic resilience and impaired saccadic adaptation due to cerebellar disease

The term short‐term saccadic adaptation (STSA) captures our ability to unconsciously move the endpoint of a saccade to the final position of a visual target that has jumped to a new location during the saccade. STSA depends on the integrity of the cerebellar vermis. We tested the hypothesis that STSA reflects the working of a cerebellar mechanism needed to avoid ‘fatigue’, a gradual drop in saccade amplitude during a long series of stereotypic saccades. To this end we compared the kinematics of saccades of 14 patients suffering from different forms of cerebellar disease with those of controls in two tests of STSA and a test of saccadic resilience. Controls showed an increase in saccade amplitude (SA) for outward adaptation, prompted by outward target shifts, due to an increase in saccade duration (SD) in the face of constant peak velocity (PV). The decrease in SA due to inward adaptation was, contrariwise, accompanied by a drop in PV and SD. Whereas patients with intact vermis did not differ from controls, those with vermal pathology lacked outward adaptation: SD remained constant, as did SA and PV. In contrast, vermal patients demonstrated a significant decrease in SA, paralleled by a decrease in PV but mostly unaltered SD in the inward adaptation experiment as well as in the resilience test. These findings support the notion that inward adaptation is at least partially based on uncompensated fatigue. On the other hand, outward adaptation reflects an active mechanism for the compensation of fatigue, residing in the cerebellum.

Single-neuron evidence for a contribution of the dorsal pontine nuclei to both types of target-directed eye movements, saccades and smooth-pursuit

The primate dorsolateral pontine nucleus (DLPN) is a key link in a cerebro‐cerebellar pathway for smooth pursuit eye movements, a pathway assumed to be anatomically segregated from tegmental circuits subserving saccades. However, the existence of afferents from several cerebrocortical and subcortical centres for saccades suggests that the DLPN and neighbouring parts of the dorsal pontine nuclei (DPN) might contribute to saccades as well. In order to test this hypothesis, we recorded from the DPN of two monkeys trained to perform smooth pursuit eye movements as well as visually and memory‐guided saccades. Out of 281 neurons isolated from the DPN, 138 were responsive in oculomotor tasks. Forty‐five were exclusively activated in saccade paradigms, 68 exclusively by smooth pursuit and 25 neurons showed responses in both. Pursuit‐related responses reflected sensitivity to eye position, velocity or combinations of velocity and position with minor contributions of acceleration in many cases. When tested in the memory‐guided saccades paradigm, 65 out of 70 neurons activated in saccade paradigms showed significant saccade‐related bursts and 20 significant activity in the memory period. Our finding of saccade‐related activity in the DPN in conjunction with the existence of strong anatomical input from saccade‐related cerebrocortical areas suggests that the DPN serves as a precerebellar relay for both pursuit and saccade‐related information originating from cerebral cortex, in addition to the classical tecto‐tegmental circuitry for saccades.

Monkeys use the rod-dense retinal region rather than the fovea to visually fixate small targets in scotopic vision

Monkeys appear to visually fixate targets in scotopic conditions. The function fixations fulfill in photopic vision, keeping the target’s image on the fovea, is nullified in scotopic vision, because the fovea, with its cones, is desensitized in dim light. Here we followed the hypothesis that a previously described retinal region, the locus of maximal rod density, functionally replaces the fovea; we found that with dark background, most of the fixations direct the fovea above the target, so that the target’s image appears to fall on the line connecting the fovea with the locus of maximal rod density. There is considerable trial-by-trial variation in the fixation positions along this line. On the whole, the closer the visual conditions are to full scotopic, the higher is this gaze upshift, indicating the closer does the target fall to the locus of maximal rod density. Mesopic background induces low mean upshift. Full (45-min) dark adaptation was essential to achieving high upshift values. There is no analogous photopic effect – 45-min ‘bright adaptation’ did not shift the locus of photopic fixation.

The Role of the Cerebellum in Optimizing Saccades

Abstract How does the brain allow us to acquire a new motor skill or to adjust an available skill to new needs? This is a central question for researchers trying to understand the neural basis of motor learning. Studies of the adjustment of eye movements to new requirements have advanced our understanding of the neuronal processes in the cerebellum that underlie the unfolding of the learned behavior. Saccades are highly skilled eye movements that quickly and accurately rotate the eye so that the image of objects of interest shifts onto the fovea. In this review, we try to provide an overview of the findings on the role of the cerebellum in helping to control and to optimize saccades. We focus on the role of the major cerebellar representation of saccades, the oculomotor vermis. We concentrate on the plastic changes that are observed in the firing of the Purkinje cells of the oculomotor vermis during the acquisition of the desired saccade response. We describe how the altered activity of these neurons may interact with the brain-stem premotor circuitry for saccades.

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 targets 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.