Visuospatial Attention and Saccadic Inhibitory Control in Children With Cerebral Palsy

Abstract

Cerebral palsy (CP) is a non-progressive syndrome due to a pre-, peri- or post-natal brain injury, which frequently involves an impairment of non-motor abilities. The aim of this article was to examine visuospatial attention and inhibitory control of prepotent motor responses in children with CP showing a normal IQ or mild cognitive impairment, measuring their performance in oculomotor tasks. Ten children (9-16-year-old) with spastic CP and 13 age-matched, typically developing children (TDC) participated in the study. Subjects performed a simple visually-guided saccade task and a cue-target task, in which they performed a saccade towards a peripheral target, after a non-informative visual cue was flashed 150 ms before the imperative target, either at the same (valid) or at a different (invalid) spatial position. Children with CP showed severe executive deficits in maintaining sustained attention and complying with task instructions. Furthermore, saccadic inhibitory control appeared to be significantly impaired in the presence of both stimulus-driven and goal-directed captures of attention. In fact, patients showed great difficulties in suppressing saccades not only to the cue stimuli but also to the always-present target placeholders, which represented powerful attentional attractors that had to be covertly attended throughout the task execution. Moreover, impairment did not affect in equal manner the whole visual field but showed a marked spatial selectivity in each individual subject. Saccade latencies in the cue-target task were faster in the valid than in the invalid condition in both child groups, indicating the preservation of low-level visuospatial attentive capabilities. Finally, this study provides evidence that these impairments of executive skills and in inhibitory control, following early brain injuries, manifest in childhood but recover to virtually normal level during adolescence.

Keywords: cerebral palsy; cueing paradigm; executive skills; eye movements; inhibitory control; oculomotor control; saccades; visuospatial attention.

Figure 1

Experimental paradigm. (A) In each quadrant of the visual field, a square-shaped gray placeholder was displayed at 7° of eccentricity from a central cross throughout the recording session. (B) Saccadic task: the subject executed a visually-guided saccade towards a green target, randomly occurring inside one of the placeholders. (C) Cue-target task: the subject executed a saccade to the green target, disregarding a non-informative cue (50 ms luminance increase of a placeholder), which occurred 150 ms before target onset, either at the same (valid-cue condition) or at a different (invalid-cue condition) spatial location.

Figure 2

Latency and accuracy of ocular responses in the saccadic task. Scatter plot of the mean latencies vs. the mean errors of saccadic movements for every cerebral palsy (CP) and typically developing (TD) participant, tested in the saccadic task. For Children with CP (CPC), subject identifiers are shown.

Figure 3

Fixation stability during the cue-target task. Scatter plot showing the relationship between the percentage of trials with inaccurate fixation and participant’s age. Subject identifiers are reported near CPC data points. Statistically significant regression lines (dashed) are depicted for typically developing children (TDC; blue) and CPC (red), separately.

Figure 4

Representative recordings of saccadic intrusions towards placeholders in CPC. (A) A saccadic task trial; (B,C) trials during the cue-target task. Color codes are used to identify more easily the placeholders on which visual stimuli are presented and eye movements are directed to. On the column at the left-hand side, traces represent the time courses of horizontal (H) and vertical (V) eye movement recordings (up: rightwards and upwards direction), with respect to central fixation cross (dashed line). Bold horizontal lines, with the color corresponding to the placeholder of appearance, indicate timing and position of saccadic target and cue. Eye movement traces are also drawn with the color code corresponding to the placeholder to which gaze was directed. Insets on the right-hand column depict the projections of the line of gaze on the computer screen during the trial. Numbers and arrows mark sequence and direction of saccades, respectively, to ease the comparison between the two ways of representing the eye movements. Bold frames indicate the placeholder of cue appearance; little green squares indicate the place of occurrence of the saccadic target.

Figure 5

Saccadic intrusions towards “inactive” placeholders. (A) Scatter plot illustrating mean saccadic intrusions per trial as a function of participant age, for TDC and CPC. Subject identifiers are reported near CPC data points. The blue dashed line indicates the presence of a statistically significant linear regression for TDC data. (B) Distribution of saccadic intrusions among visual quadrants, made by CPC with a high rate of intrusion occurrence. In each plot, the circle areas are proportional to the relative frequency of intrusions in the corresponding quadrant (see text for details).

Figure 6

Inhibitory control of reflexive saccades in the cue-target task. (A) Scatter plot depicting the percentage of eye responses towards the cue as a function of the percentage of express saccades made by each subject. Subject identifiers are reported near CPC data points. The red dashed line indicates the presence of a statistically significant linear regression for CPC data. (B) Distribution of responses towards the cue among visual quadrants for each CP subject. In each plot, the size of the red circles reflects the percentage of responses (whose value is reported nearby), with respect to the number of trials in which the cue fell in the corresponding quadrant (indicated as reference by a black circumference). Asterisks near the subject identifiers indicate a non-random distribution of cue-directed saccades.