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Keywords:

  • exploratory eye movements;
  • gender differences;
  • reproducibility;
  • visual cognition

Abstract

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. METHODS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES

Exploratory eye movements were recorded using an eye-mark recorder in 48 normal subjects (24 male and 24 female). Gender differences were examined regarding four eye movement parameters such as the mean gazing time, the total number of gazing points, and the mean eye scanning length and the total eye scanning length. The mean gazing time of women was significantly longer than that of men, and the total number of gazing points of women was significantly less than that of men. The mean eye-scanning length of men and women did not differ. The total eye scanning length of men was significantly longer than that of women. Reproducibility between sessions of the four eye movement parameters above was expressed as Pearson correlation coefficients (r) in 24 healthy adults before and after a month interval, yielding respective coefficients of 0.65, 0.42, 0.56 and 0.61. These results suggested that differences in exploratory eye movements between men and women may reflect differences in the characteristics of visual information processing and also confirmed the reproducibility of exploratory eye movement parameters.


INTRODUCTION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. METHODS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES

Exploratory eye movements have been evaluated as biological markers in investigating mechanisms of visual information processing in healthy subjects and in patients with cognitive disorders such as schizophrenia, depression, or dementia. 1,2,3 Kojima et al.2 have reported in detail on exploratory eye movements using an original S-shaped figure for normal subjects and schizophrenic patients and have suggested that exploratory eye movements may be a trait marker of schizophrenia and a useful biological marker in cognitive studies.

It is fundamentally important to evaluate gender and age differences in normal subjects. Anatomical gender differences have been widely reported in the brain. 4,5 A consistent finding is that men perform better than women in spatial motor tasks. 6,7 Indeed, women are reported to have a poor performance in scanning the visual field. 8 Furthermore, scattered reports have suggested possible gender differences, such as in sensorimotor gating of the acoustic startle which could reflect hormonal differences rather than neuroanatomical differences. 9,10 Thus, it is important whether or not the exploratory eye movements is a characteristic of gender difference in normal subjects. However, no previous studies on gender difference and exploratory eye movements have used an eye-mark recorder to investigate visual information processing.

Also, reproducibility of a subject’s eye movement data has not been studied sufficiently. 11,12 Determining whether eye movement parameter as the mean gazing time, the total number of gazing points, the mean scanning length of gazing points, and the total scanning length of gazing points can be altered by state and/or trait effects is particularly important in clinical applications. Exploratory eye movement reproducibility in healthy subjects requires repeated assessments to search for stable parameters. The present study was performed both to test for gender differences in eye movements and to evaluate reproducibility after a month.

METHODS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. METHODS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES

Subjects

The group of normal volunteers consisted of doctors and nursing staff of Horikawa Hospital. Forty-eight normal subjects (24 female, mean age 39.8 ± 19.0 SD; 24 male, mean age 38.9 ± 15.5 SD) were tested in the study of gender differences. The reliability study included 24 normal subjects (12 men and 12 women). No significant age differences were apparent between the men and women. All were healthy, had normal hearing, and had no history of psychiatric disease, substance abuse, neurological, or visual disorders. Female subjects were not tested at any particular time during their menstrual cycle. Each subject gave informed consent for participation.

Exploratory eye movement recording procedure

In a dark room where non-visual sensory stimuli were attenuated, exploratory eye movements were recorded using an eye-mark recorder (SK-2, Nac Institute, Osaka, Japan). Recordings were obtained between 0900 and 1200 h. Before eye movements were recorded, subjects were asked to draw each picture presented immediately after viewing in order to increase their visual attention. The gazing point was determined from a gazing time exceeding 0.2 s, the time required for the perception to occur in the visual cortex. 13 The gazing point was determined within 1 degree of the visual angle. 2 Exploratory eye movements and fixation points during perception of the figures were examined. Pictures were projected onto a screen, where they appeared 90 cm wide and 70 cm tall and maximum angles of sightlines were 30° horizontally and 20° vertically. Each session consisted of a series of six views. Subjects were required to complete six views in 15 s with the exception of Picture 3* (10 s).

We used pictures of a geometrical pattern as a circle, and scene, happy faces because eye movements have been reported from viewing a simple geometrical shape and a happy face. 14,15 Four pictures were used: Picture 1, an open circle which was simple and non-stressed but examined set and/or motivation of subjects; 2 Picture 2, a ‘happy face’ which examined the effect of emotional influences; Picture 3, a ‘happy face’ with lines added beside the mouth which examined a recognition of the differences from Picture 2; Picture 3*, identical to Picture 3 but this time subjects were asked to search for any additional differences for testing of confidence; 2,3 Picture 4, a scene with 1–0 elements including four different animals, the sun, an airplane, five trees, a house, two mountains, and a river which examined visual ability and short memory; and Picture 5, identical to Picture 1, an open circle which examined any influence of the stimulus of Picture 4 and any habituation. For Picture 4, all subjects were required to note all the elements present immediately after viewing. We evaluated the total numbers of identified elements as attention points (element score points or ESP, totaling 13 points).

Exploratory eye movements were analyzed for four parameters: the mean gazing time, the total number of gazing points, the mean eye scanning length of gazing points, the total eye scanning length of gazing points. 2 Data analyzed were for the left eye as we have noted, because there was not any difference between the data of right eye and that of left eye (Morita et al., unpubl. obs., 1997) ( Fig. 1).

image

Figure 1. Test pictures and comparing typical two series of eye movements.

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Statistical analysis

Two-way analysis of variance ( ANOVA) was used to compute the main session effect for the group (women and men). Fisher’s protected least square deviation (LSD) was then applied as a posthoc test. Next, one-way ANOVA was used to compute the differences for each picture. Reproducibility between sessions was expressed as Pearson’s product–moment correlation coefficient (r). Bartlett’s t-test was used to evaluate statistical significance. A level of P < 0.05 was accepted as statistically significant. In the present study, a correlation coefficient over 0.5 was considered acceptable. 16

RESULTS

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. METHODS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES

Gender difference

Mean gazing time

The mean gazing time of women was 0.437 + 0.11 s (n = 24) and that of men was 0.384 + 0.088 s (n = 24). The mean gazing time of women was significantly longer than that of men by two-way ANOVA (gender × picture; F22,23, P < 0.0001). No interaction was found between gender and pictures. The last two pictures, the scene (Picture 4; F8,99, P < 0.01) and the open circle (Picture 5; F9,71, P < 0.01) of women were significantly less than for that of men in two-way ANOVA.

Total number of gazing points

The total number of gazing points was 20.32 ± 5.43 (n = 24) in women and 24.64 ± 5.33 (n = 24) in men. The total number of gazing points of women was significantly less than that of men by two-way ANOVA (gender × pictures; F60,52, P < 0.0001). No interaction was found between gender and pictures. For each picture, significant differences were apparent between men and women (Picture 1, F6,23, P < 0.05; Picture 2, F8,62, P < 0.01; Picture 3, F6,46, P < 0.05; Picture 4, F23.92, P < 0.0001; Picture 5, F19.54, P < 0.0001). Pictures 4 and 5 showed larger differences (P < 0.0001) between men and women than the others as shown in Fig. 2.

image

Figure 2. Mean gazing time (a) and total numbers of gazing points (b). Mean gazing time and total number of gazing points (ordinates) as a function of test pictures (abscissa). Note that mean gazing time of (○) women was significantly longer than that of (□) men in Pictures 4 and 5 (a). Each bar means + SE. *, P < 0.05; **, P < 0.01; ***, P < 0.001.

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Mean eye scanning length

The mean eye scanning length for women was 7.54 ± 2.53 cm (n = 24) and that of men was 8.37 ± 2.79 cm (n = 24). The mean eye scanning length of women was different from that of men by two-way ANOVA (gender × pictures; F7,41, P < 0.01). No interaction was detected between gender and pictures. No significant differences were found for each picture.

Total eye scanning length

The total eye scanning length was 141.24 ± 51.30 cm (n = 24) in women and 194.03 ± 73.9 cm (n = 24) in men. The total eye scanning length of men was significantly longer than that of women by two-way ANOVA (gender pictures; F60,26, P < 0.0001). No interaction was evident between gender and pictures. Total eye scanning length showed significant differences for all pictures. The difference between men and women for Pictures 4 (F18,27, P < 0.0001) and 5 (F27,86, P < 0.0001) were larger than for the others (Picture 1, F4,81, P < 0.05; Picture 2, F6,21, P < 0.05; Picture 3, F7,51, P < 0.01; Picture 3*, F7,89, P < 0.01) ( Fig. 3).

image

Figure 3. Mean eye scanning length of gazing points (a) and total eye scanning length of gazing points (b). Mean eye scanning length of gazing points and total eye scanning length of gazing points (ordinates) as a function of test pictures (abscissa). Note that total eye scanning lengths of gazing points were largely different between men (□) and women (○) in Pictures 4 and 5. Each bar means + SEM. *, P < 0.05; **, P < 0.01; ***, P < 0.001.

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Relationship between age and eye movement measures

There were no significant relationships between ages and four eye measures such as the mean gazing time, the total number of gazing points, the mean scanning length and the total scanning length. Also, no significant relationships were obtained between ages and the four eye measures in Picture 4 (scene) and Picture 5 (circle) for both men and women.

Reproducibility

Reproducibility between sessions was expressed as Pearson’s product–moment correlation coefficient. The correlation for the mean gazing time (r = 0.65), the mean scanning length (0.56) and the total scanning length (0.61) generally were significant (r > 0.5). Although the total number of gazing points (0.48) was less than 0.5, Bartlett’s t-test showed statistical significance ( Table 1). The correlation coefficient for all parameters exceeded 0.5 in Picture 1. The correlation coefficients of the mean gazing time, mean scanning length, and total scanning length were more than 0.5 for Pictures 4 and 5. The correlation coefficient (0.81) for the total scanning length was highest in Picture 5. The correlation coefficient (0.12) for the total number of gazing points for Picture 3 was the lowest obtained.

Table 1.  Reproducibility represented as Pearson correlation coefficients (r) for four elements of eye movements
 Mean gazing timeTotal number of gazing pointsMean scanning lengthTotal scanning length
  1. Probability calculated from Bartlett’s t-test is indicated by asterisk (*, ** and ***) in all correlation coefficients. Note that total scanning length of gazing points indicated the highest stability in each case.

  2. Values represent Pearson correlation coefficients (r).

  3. *P < 0.05; **P < 0.01; ***P < 0.001.

All picture0.65***0.42***0.56***0.61***
Picture 10.66**0.59**0.53*0.56**
Picture 20.79***0.220.420.37
Picture 30.390.120.380.45*
Picture 3*0.370.330.65***0.48*
Picture 40.74***0.280.62***0.63**
Picture 50.75***0.390.65***0.81***

DISCUSSION

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. METHODS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES

The major finding of this study is that of gender influence on eye movement parameters observed in healthy subjects. Women may have shorter scanning length than men.

Gender has been shown to influence a variety of electrophysiological measures. Adult women reportedly had a larger amplitude of brainstem and cortical-evoked responses and shorter EP latencies than men did. 17 Anatomical differences between men and women have been suggested to underlie differences in EP source origins. 18 Anatomical difference is not supported by the present findings, as gender differences varied by picture viewed (e.g. for the mean gazing time, gender differences were significant for Pictures 4 and 5, but not for the other pictures). One might expect anatomical difference to be more consistent in producing differences irrespective of the picture views.

As shown in Fig. 1, women may tend to concentrate their attention only on target parts of the pictures and do not try to look at other parts, but men may try to look at other parts as well as the target parts. Thus, women’s eye movements are fewer in the present study. Additionally, women may not concentrate their energy toward the outside of viewing picture as in Picture 1 and 5 (circle). This may be due to their decreased motivation and lack of interest in trying to get information about the pictures and to recognize them. Women reportedly have a lower recovery amplitude to repeated visual stimuli than men, 19 and show less decline in cognitive efficiency when irrelevant visual cues are introduced. 20 In the present study, women had a significantly longer mean gazing time, smaller numbers of gazing points, and shorter total scanning length compared to men, indicating less visual searching.

From consideration of above reports and the present results, repetitive stimuli such as viewing six pictures may cause reduced recovery of eye movements especially in women. Indeed, Pictures 4 and 5 were significantly different between men and women in the mean gazing time, and these were more significant than other pictures for the three other parameters. In a sensory vigilance task, young women (18–19 years) had slower reaction times to target stimuli than men of similar ages and women detected fewer targets. 21 The authors suggested that these effects may have reflected different arousal levels in men and women. Thus, arousal may decline during the presentation of six pictures. Also the order effects of six pictures were not examined, it should be considered for the differences of the eye measures in different order. However, element score points (ESP) in Picture 4 did not differ significantly between men and women. Yet, we cannot rule out the possibility that the arousal level of women may have been lower than for men, especially in the last two pictures.

Hormonal influence has been implicated in gender differences in ERP (event-related potentials). 22 In a study spanning many subject ages women reportedly had a higher mean amplitude response of P50 to a first stimulus than men. 23 The pattern reversal of EP amplitude gender differences over many subjects’ ages suggested a hormonal influence on visual spatial frequency processing. 17 We speculate that hormonal influences are a likely cause of gender differences in visual information processing which could be marked in younger individuals but less evident between age-matched postpubertal men and women (Miyahira, unpubl. data, 1998). Although there was no report on hormonal effect on eye movement measures, Kimura and Hampson have reported that cognitive patterns in men and women may be influenced by sex hormones. 24 Further study with respect to age is needed to examine the hormonal elements underlying gender differences in visual information processing.

Reproducibility

In repeated studies of groups, values for reproducibility between sessions (r) were more than 0.5 except for the total number of gazing points in summarized table. Thus, the reproducibility of eye movement is acceptable in group research. 9 The present correlation between sessions was comparable to findings in previous ERP reports. 6,7 Pictures 1 (first open circle), 4 (scene) and 5 (last open circle) had the largest correlation coefficient. Picture 3 (‘happy face’ with lines beside the mouth) had the lowest value. The highest correlation was obtained for the total scanning length in Picture 5 (last open circle; r = 0.81, P < 0.0001). It appears to be important that eye movement measures obtained from Pictures 2 and 3 (‘happy face’) showed somewhat lower reproducibility than others. Further study is needed to clarify the mechanism underlying the differences between individual pictures.

Physiological significance

Eye movements obtained by an eye-mark recorder may reflect visual information processing and appear stable for use in repeated studies because acceptable reproducibility was demonstrated. Selective attention and/or arousal might be formed to underlie the presently observed gender differences. However, the relevance of observed gender differences to psychology is unclear. It is interesting that eye movements for the scene (Picture 4) and the second open circle (Picture 5) were significantly different between men and women in the present study, suggesting that the addition of detail such as animals and a house stimulates visual information processing differences in women and men. Indeed, it has been reported that the gender differences may exist in the spatial ability and the functional organization for language of the brain. 25,26 The present finding may reflect gender-related behavioral differences. It has been reported that men’s spatial ability may be enhanced for human hunter society. 24 As shown in Fig. 1, for the open circle, men would scan across the line and tend to look towards the outer space, but women would scan across the line and tend to look towards the inner space. These may be due to the expectation that men would be confident of the target and focus on other parts, in particular outside of the target area; however, women would focus on the target and pay particular attention to its center. Further study is needed to explore possible visual desensitization or fatigue phenomenon during repetitive viewing, which was different between men and women.

REFERENCES

  1. Top of page
  2. Abstract
  3. INTRODUCTION
  4. METHODS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES
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