Frontal lobe epilepsy: an eye tracking study of memory and attention

Abstract

Objective: To explore the characteristics and mechanisms of working memory impairment in patients with frontal lobe epilepsy (FLE) through a memory game paradigm combined with eye tracking technology.

Method: We included 44 patients with FLE and 50 healthy controls (HC). All participants completed a series of neuropsychological scale assessments and a short-term memory game on an automated computer-based memory evaluation platform with an eye tracker.

Results: Memory scale scores of FLE patients including digit span (U = 747.50, p = 0.007), visual recognition (U = 766.50, p = 0.010), and logical memory (U = 544.00, p < 0.001) were significantly lower than HC. The patients with FLE took longer to complete the four levels of difficulty of the short-term memory game than healthy controls (level 1: U = 2974.50, p = 0.000; level 2: U = 3060.50, p = 0.000; level 3: U = 2465.00, p = 0.000; level 4: U = 2199.00, p = 0.000). During the memory decoding period, first fixation on the targets took significantly longer for FLE patients for all difficulty levels compared to controls (level 1: U = 3407.00, p = 0.008; level 2: U = 3618.00, p = 0.036; level 3: U = 3345.00, p = 0.006; level 4: U = 2781.00, p = 0.000). The average fixation duration per target among patients with FLE was found to be significantly longer compared to HC (level 1: U = 2994.50, p = 0.000; level 2: U = 3101.00, p = 0.000; level 3: U = 2559.50, p = 0.000; level 4: U = 2184.50, p = 0.000). The total fixation duration on AOI/total completion time of FLE patients was significantly lower than those of HC for levels 1 to 3 (level 1: U = 1557.00, p = 0.000; level 2: U = 2333.00, p = 0.000; level 3: U = 2757.00, p = 0.000). Furthermore, the eye tracking data during the memory decoding phase were correlated with neuropsychological scale scores (p < 0.05).

Conclusion: Patients with FLE exhibited short-term memory impairment probably due to deficits in attentional maintenance, especially during the memory decoding phase. Eye tracking technology provided the possibility to help separate and quantify visual attention from memory processing, contributing to exploring underlying mechanisms of memory impairment in FLE.

Keywords: eye movement; eye tracking; frontal lobe epilepsy; memory deficit; visual attention.

Figure 1

During the trial, a target was shown on the screen for 5 s (encoding), followed by the appearance of 12 (4 × 3) potential answers. Participants were required to recall and click on the correct target from the 12 objects (decoding). The targets were numbered from 1 to 4, and participants were required to choose all the correct targets during the decoding phase in order to proceed to the next level. The orange circle indicates the target and the white circle in the decoding phase is the interference graphic.

Figure 2

Comparison of (A) total completion time of the Short-Term Memory task, (B) total completion time under fractal image stimuli, and (C) total completion time under front-facing image stimuli between the HC group and FLE group at four difficulty levels. Statistical significance for each task between groups is indicated by asterisk(s) (^*p < 0.05, ^**p < 0.01, ^***p < 0.001). HC, healthy control; FLE, frontal lobe epilepsy.

Figure 3

Comparison of (A) first fixation time on target, (B) average fixation duration per target, (C) average fixation count per target, and (D) total fixation duration on AOI/total completion time of the decoding phase in all tasks between the HC group and FLE group. Statistical significance for each task between groups is indicated by asterisk(s) (^*p < 0.05, ^**p < 0.01, ^***p < 0.001). HC, healthy control; FLE, frontal lobe epilepsy.

Figure 4

Comparison of (A) first fixation time on target, (B) average fixation duration per target, (C) average fixation count per target, and (D) total fixation duration on AOI/total completion time of the decoding phase in the fractal image stimuli task between the HC group and FLE group. Statistical significance for each task between groups is indicated by asterisk(s) (^*p < 0.05, ^**p < 0.01, ^***p < 0.001). HC, healthy control; FLE, frontal lobe epilepsy.

Figure 5

Comparison of (A) average fixation duration per target, (B) average fixation count per target, and (C) total fixation duration on AOI/total completion time of the decoding phase in the front-facing image stimuli task between the HC group and FLE group. Statistical significance for each task between groups is indicated by asterisk(s) (^*p < 0.05, ^**p < 0.01, ^***p < 0.001). HC, healthy control; FLE, frontal lobe epilepsy.

Figure 6

Correlations between the scores of memory scale assessment (digit span, visual recognition, logical memory) and TCT, FFT on AOI, FFT on target, AFD per target, AFC per target, TFD on AOI/TCT, AFD per target/TFD on AOI. Statistical significance for each task between groups is indicated by asterisk(s) (^*p < 0.05, ^**p < 0.01, ^***p < 0.001). TCT, total completion time; FFT, first fixation time; AOI, area of interest; AFD, average fixation duration; AFC, average fixation count; TFD, total fixation duration.