Reduced saccadic resilience and impaired saccadic adaptation due to cerebellar disease

Abstract

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.

Cerebellar-dependent motor learning is based on pruning a Purkinje cell population response

“…In addition to this putative active mechanism, saccade velocity may be influenced by a second, passive mechanism, contributing to the decline in peak velocity, characterizing gain-decrease saccades of monkeys (this study) and those of human subjects (16), a decline in peak velocity that is fully accountable for the amplitude reduction because saccade duration does not change. Similar decreases in peak velocity can be seen when subjects carry out long series of saccades, causing ''fatigue,'' either because of a reduced efficacy of the eye muscles and other components of the oculomotor periphery or because of a loss of attention or motivation (16). In such fatigue experiments, the drop in eye velocity is typically compensated by an increase in duration, keeping saccade amplitude stable.…”

“…In such fatigue experiments, the drop in eye velocity is typically compensated by an increase in duration, keeping saccade amplitude stable. Similar to the loss of outward adaptation, this velocity duration tradeoff preventing fatigue is irreversibly lost after lesions involving the OV region (16). However, even in cases in which outward adaptation is completely lost, at least some inward adaptation may still be observed, arguably reflecting uncompensated fatigue (16,17).…”

“…Similar to the loss of outward adaptation, this velocity duration tradeoff preventing fatigue is irreversibly lost after lesions involving the OV region (16). However, even in cases in which outward adaptation is completely lost, at least some inward adaptation may still be observed, arguably reflecting uncompensated fatigue (16,17). Hence, the lesion observations suggest that the amplitude reduction of inward-adapted saccades has two components, a first, passive component that capitalizes on the reduced velocity resulting from natural fatigue, not affected by the OV lesion, and a second, active one dependent on the PC PB, lost after the lesion.…”

Error Correction, Sensory Prediction, and Adaptation in Motor Control

“…If a target is presented and they are instructed to look in the opposite direction, saccade velocities are much lower than if they are asked to look to the target (Smit et al, 1987). Repeating a visual target (Straube et al, 1997;Chen-Harris et al, 2008;Golla et al, 2008) or reducing the reward associated with that stimulus (Takikawa et al, 2002) also reduces saccade velocities. On the other hand, increasing the reward associated with the target (Takikawa et al, 2002), making the target the goal of both the eye and the arm movements (van Donkelaar, 1997;Snyder et al, 2002), or unexpectedly changing the characteristics of the target (Xu-Wilson et al, 2009a) all result in increased saccade velocities without altering saccade amplitude.…”

Mislocalization of Flashed and Stationary Visual Stimuli after Adaptation of Reactive and Scanning Saccades

“…Over the course of successive trials with consistent displacement, the amplitude of the primary saccade is gradually changed to immediately reach the displaced target location. The adaptation involves gain changes in cerebellar and other subcortical structures (Desmurget et al, 1998;Robinson and Fuchs, 2001;Catz et al, 2008;Golla et al, 2008). The adaptation-induced mislocalization suggests effects of adaptation on the cortical level, or at least feedback from cerebellar or subcortical structures onto cortical localization mechanisms (Gaymard et al, 2001;Awater et al, 2005).…”