Top-down but not bottom-up visual scanning is affected in hereditary pure cerebellar ataxia

Abstract

The aim of this study was to clarify the nature of visual processing deficits caused by cerebellar disorders. We studied the performance of two types of visual search (top-down visual scanning and bottom-up visual scanning) in 18 patients with pure cerebellar types of spinocerebellar degeneration (SCA6: 11; SCA31: 7). The gaze fixation position was recorded with an eye-tracking device while the subjects performed two visual search tasks in which they looked for a target Landolt figure among distractors. In the serial search task, the target was similar to the distractors and the subject had to search for the target by processing each item with top-down visual scanning. In the pop-out search task, the target and distractor were clearly discernible and the visual salience of the target allowed the subjects to detect it by bottom-up visual scanning. The saliency maps clearly showed that the serial search task required top-down visual attention and the pop-out search task required bottom-up visual attention. In the serial search task, the search time to detect the target was significantly longer in SCA patients than in normal subjects, whereas the search time in the pop-out search task was comparable between the two groups. These findings suggested that SCA patients cannot efficiently scan a target using a top-down attentional process, whereas scanning with a bottom-up attentional process is not affected. In the serial search task, the amplitude of saccades was significantly smaller in SCA patients than in normal subjects. The variability of saccade amplitude (saccadic dysmetria), number of re-fixations, and unstable fixation (nystagmus) were larger in SCA patients than in normal subjects, accounting for a substantial proportion of scattered fixations around the items. Saccadic dysmetria, re-fixation, and nystagmus may play important roles in the impaired top-down visual scanning in SCA, hampering precise visual processing of individual items.

Figure 1. Discrimination tasks.

A: direction discrimination task, B: color discrimination task. In the direction discrimination task, the subject was instructed to push the button connected to the eye-tracking device as quickly as possible only when an upward-facing Landolt figure appeared at the center of monitor. In the color discrimination task, the subject was instructed to push the button only when a red Landolt figure appeared. The direction and color discrimination times were measured by the following formula: discrimination time  =  total time – simple reaction time.

Figure 2. Search tasks.

A: serial search task, B: pop-out search task. Upper panels show 4-item tasks and lower panels show 48-item tasks. In the serial search task, the subject was instructed to push the button connected to the eye-tracking device when he/she found an upward-facing Landolt figure. In the pop-out search task, the subject was instructed to push the button when he/she found a red Landolt figure. The serial and pop-out search times were measured by the following formula: search time  =  total time – simple reaction time.

Figure 3. Saliency maps in search tasks.

A: serial search task, B: pop-out search task. In the pop-out search task, the target red Landolt figure is clearly colored in red, suggesting that the subjects performed bottom-up visual scanning due to the high saliency of the target. In the serial search task, high saliency areas are uniformly distributed over the images and the target upward Landolt figure is completely masked, suggesting that the subjects performed top-down visual scanning due to the low saliency of the target.

Figure 4. Heat maps in serial search tasks.

A: SCA patients, B: normal subjects. In both 4- and 48-itemt tasks, the areas (colored areas) scanned by SCA patients were distributed more widely than those of normal subjects. The center was also colored because the starting eye-fixation position was located at the center of image.

Figure 5. Heat maps in pop-out search tasks.

A: SCA patients, B: normal subjects. In both 4- and 48-item pop-out search tasks, the areas (colored areas) scanned by both SCA patients and normal subjects were more localized than those in serial search tasks.

Figure 6. Representative eye movements.

Eye movements in the 4-item serial search task are shown for an SCA patient (A) and a normal subject (B). In the SCA patient, the ocular fixation positions frequently did not fall exactly on the visual target, but landed at points somewhat removed from the target (saccadic dysmetria). In addition, we also observed something we term “repeated fixations (re-fixations)”. Here, the gaze initially captures the target item and then moves away before returning to the target item. To count the number of re-fixations, the target Landolt figure was selected as the region of interest.

Figure 7. Oculomotor trajectories.

Careful visual observation of oculomotor trajectories provides information on saccadic dysmetria, repeated fixations (re-fixations) and nystagmus. These figures show recordings of the gaze trajectory during visual search (abscissa: time; ordinate: the distance of gaze position from the target (zero deg. in the abscissa corresponds to the target position) [blue curve]; and instantaneous velocity of gaze [red curve]) in an SCA patient (A) and a normal subject (B). Note that with time the gaze eventually approaches the target (distance becomes zero at the right end of each figure) but for an SCA patient it takes more time, with the gaze alternately approaching and leaving the target. After approaching the target, the gaze leaves the target once and eventually comes back to the target later (repeated fixations). In addition, the gaze position shows slow drifts, representing the slow phase of nystagmus, even during presumed fixation, whereas this rarely occurs in normal subjects.

Figure 8. Search time of visual tasks.

A: simple reaction time, B: direction and color discrimination time, C: serial and pop-out search time. The bars show the values of mean and standard error. Grey bars are for SCA patients and white bars for normal subjects. The simple reaction time was longer in SCA patients than in normal subjects. The direction and color discrimination time had no statistical differences. The 4- and 48-item serial search time was longer in SCA patients than in normal subjects, whereas the 4- and 48-item pop-out search time in SCA patients was almost identical to that in normal subjects. The serial search time was markedly longer than the pop-out search time in both SCA patients and normal subjects.

Figure 9. Visual scanning parameters in serial search tasks.

A: number of saccades, B: duration of fixation, C: amplitude of saccades, D: coefficient of variation (CV) of saccade amplitude, E: number of repeated fixations, F: instability ratio of fixation. The bars show the values of mean and standard error. Grey bars are for SCA patients and white bars for normal subjects. The number of saccades per second and duration of fixation in SCA patients were identical to those in normal subjects for both 4- and 48-item tasks. Amplitude of saccades was smaller in SCA patients than in normal subjects for both 4- and 48-item tasks, although these differences were not statistically significant. CV of saccade amplitude was larger in SCA patients than in normal subjects only in the 4-item task. Number of repeated fixations and instability ratio of fixation were larger in SCA patients than in normal subjects for both 4- and 48-item tasks.