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Ocular dominancy in conjugate eye movements at reading distance
Neuroscience Research 52 (2005) 263–268 www.elsevier.com/locate/neures
Ocular dominancy in conjugate eye movements at reading distance Ayame Oishi a, Shozo Tobimatsu b,*, Kenji Arakawa a, Takayuki Taniwaki a, Jun-ichi Kira a b
a Departments of Neurology, Neurological Institute, Graduate School of Medical Sciences, Kyushu University, Fukuoka 812-8582, Japan Departments of Clinical Neurophysiology, Neurological Institute, Graduate School of Medical Sciences, Kyushu University, Fukuoka 812-8582, Japan
Received 20 July 2004; accepted 25 March 2005 Available online 4 May 2005
Abstract We recorded conjugate eye movements to elucidate whether ocular dominancy was present at reading distance in 21 normal volunteers with the right-handedness by using a video-oculographic (VOG) measurement. This included the velocity of smooth pursuits, and the latency and velocity of saccades. We defined the dominant eye for each subject by means of the near–far alignment test and 20 subjects showed the right dominant eyes. Although the ocular dominancy was not found in the velocity of smooth pursuit and vertical saccades, the velocity of horizontal saccades in the dominant eyes was faster than that in the non-dominant eyes. These results suggest that the dominant eye is functionally activated prior to non-dominant eye in horizontal saccades at reading distance, which thus indicates the functional dominancy of the dominant eye in conjugate eye movements. # 2005 Elsevier Ireland Ltd and the Japan Neuroscience Society. All rights reserved. Keywords: Ocular dominancy; Conjugate eye movement; Reading distance; Saccade; Smooth pursuit
1. Introduction The members of a bilateral pair of structures in the body seldom exhibit perfect equality. Often, one member of the pair tends to be preferred over the other in behavioral coordination, or it seems to manifest physiological superiority. Thus, it is defined as dominant. Relationship between handedness and dominant hemisphere has been well described. The presence of the dominant eye is also known and has often been defined as the eye whose input is favored in behavioral coordinations (Porac and Coren, 1976). Porta (1593) first suggested that the near–far alignment test was useful to determine dominant eye. Several investigators (Rombouts et al., 1996; Ibi, 1997; Kawata et al., 1991; Seyal et al., 1981) have reported the presence of the dominant eye in the visuo-oculomotor system. However, to our knowledge, the presence of ocular dominance in conjugate eye movements at reading distance has not yet been established. The velocity of a target can be accurately controlled with simple electronic equipment and the saccadic and smooth * Corresponding author. Tel.: +81 92 642 5541; fax: +81 92 642 5545. E-mail address: [email protected] (S. Tobimatsu).
pursuit eye movements can be accurately recorded with electro-oculographic (EOG) techniques, using a digital computer. Computerized EOG technique can yield reasonable recordings of horizontal eye movements whereas vertical measurements are affected by lid artifacts with considerable interindividual differences (Bechert and Koenig, 1996). Furthermore, changes in illumination and in skin resistance affect the EOG recordings. Infrared oculography provides high-resolution measurements of horizontal and vertical eye movement, but over a limited range, especially vertically. Another problem is that the signal is lost when the eyes are closed. A magnetic fieldsearch coil method uses coils embedded in a silicone rubber ring that adheres to the sclera by suction, which overcomes most of the problems that limit both EOG and infrared oculography (Collewijn et al., 1975; Yee, 1983). However, the major drawbacks of this technique are the relatively high cost and discomfort, because the surface of the eye is anesthetized. Recently, a video-oculographic (VOG) measurement system has developed (Clarke et al., 1991). This system consists of CCD sensors and digital imaging process, which allows us to evaluate the conjugate eye movements under binocular vision more objectively. Therefore, we
0168-0102/$ – see front matter # 2005 Elsevier Ireland Ltd and the Japan Neuroscience Society. All rights reserved. doi:10.1016/j.neures.2005.03.013
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A. Oishi et al. / Neuroscience Research 52 (2005) 263–268
recorded the conjugated eye movements under binocular view to elucidate the presence of ocular dominancy at reading distance by using the VOG measurement system.
2. Methods 2.1. Subjects Twenty-one normal subjects with the right-handed (10 males and 11 females), aged between 21 and 47 years (mean; 30.6 7.6 years), gave their informed consent for recording of their eye movements. Most were hospital or medical school staffs or their relatives, and all were drug-free and in good health. We defined the dominant eye for each subject by means of the near–far alignment test (Porac and Coren, 1976). Informed consent was obtained after the experimental nature had been fully explained. The Ethics committee of the Kyushu University of Faculty Medicine approved this study.
with the total amplitude of 208, and latencies and velocities ( peak velocities) of each eye were calculated by averaging 3–5 measurements in each subject. To exclude blink artifact, we adopted only vertical saccades whose fixation time was more than for 300 ms. Low time resolution of 60 Hz frame rate is overcome by the technique of ‘‘apparent peak velocity’’ because when saccadic is about 108 or larger, estimates of peak velocity on average are biased downward by less than 10% (Enright, 1998). 2.3. Statistical analysis Means and standard deviations were calculated for all parameters. Paired comparisons were made by Wilcoxon’s rank sum test, because the data were not normally distributed.
3. Results 3.1. Ocular dominancy
2.2. Visual stimuli and eye movement recordings Subjects sat on a chair with their head resting on a chinrest in a semi-darkened room, viewing the center of liquid crystal screen (29 cm 22 cm). Visual stimuli were presented at a distance of 40 cm with the 18 circle yellow target. In this paper, 108 or 208 indicates the distance between the central fixation point and target. The VOG measurement system (SMI company, Germany) was used to measure horizontal and vertical eye movements. The VOG system exploits current technology in CCD sensors mounted on a free-field mask with digital image processing (Clarke et al., 1991). We recorded binocular eye movement simultaneously, using this non-invasive system. Processing of the video images was made at a sample rate of 60 Hz for the vertical and horizontal components.
Twenty subjects showed dominant right eyes by the near– far alignment test while one male subject had dominant left eye and was excluded for further analysis. 3.2. Smooth pursuit eye movements Fig. 1 shows the raw data of a representative subject who showed the right dominant eye. There were no significant differences in the wave form and eye position between the two eyes. Mean values of smooth pursuit eye movements are summarized in Table 1. A significant difference was not found between the centripetal and centrifugal velocities. There was also no significant difference between the eye velocity in the right and left eyes in binocular pursuits. 3.3. Saccadic eye movements
2.2.1. Smooth pursuit eye movements Pursuit trials began with the appearance of the yellow fixation target at the central position on the monitor. The target moved sinusoidally with the total amplitude of 408 and peak velocity of 108/s. The mean rightward and leftward eye velocities of each eye were calculated from 7 to 10 consecutive cycles. 2.2.2. Saccadic eye movements Saccadic trials began with the appearance of the yellow target at the central position. The target stepped with predictable timing (2 s). Subjects were asked to follow the target light as soon as it moved. In the horizontal task, the target stepped pseudorandomly to the right or to the left, and latencies and velocities ( peak velocities) of each eye were calculated by averaging 10 measurements in each direction. In the vertical task, the target stepped pseudorandomly to upward or to downward
Fig. 2 shows the raw data of a representative subject with the right eye dominance. There were no significant differences in the wave form and eye position between the two eyes. Figs. 3 and 4 show scatter plots of all horizontal latencies and velocities, respectively. Mean latencies and velocities of horizontal and vertical saccades are summarized in Tables 2 and 3. On horizontal saccades, we excluded the data from two subjects because of their eyelashes artifacts. We also excluded the data from four subjects (upward) and two subjects (downward) on vertical saccades, respectively. On horizontal (leftward and rightward) saccades, there were no significant differences in the mean saccadic latencies between centrifugal and centripetal saccades (Table 2, Fig. 3). On the other hand, the mean velocities of the right eye on horizontal saccades toward the left and that of the left eye were 426.8 63.38/s and 406.8 70.08/s, respectively.
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Fig. 1. A representative example of smooth pursuit eye movement in a 32-year-old subject with the right dominant eye. There were no significant differences in the wave form and eye position between the two eyes. On leftward and rightward pursuits, the mean velocities of right eye were 148/s and 138/s while those of the left eye were 138/s and 138/s, respectively.
Thus, there was a significant difference between right (dominant) and left (non-dominant) eyes on horizontal gaze toward the left ( p < 0.05) (Fig. 4). Similarly, the mean velocities of the right eye on horizontal saccade toward the right were significantly faster than that of the left eye ( p < 0.05). On vertical (upward and downward) saccades, there were no significant differences in the mean saccadic latencies between the two eyes (Table 3). There was also no significant difference in the velocity values between centrifugal and centripetal saccades.
4. Discussion In the present study, all but one of subjects showed right dominant eye by the near–far alignment test. The mean horizontal saccadic velocities toward the right or left of the right eye were faster than those of the left eye. It has not been reported regarding the presence of the dominancy of central nervous system on conjugate eye movements. Therefore, this is the first report that demonstrates the presence of the dominant eye in conjugate eye movements at reading distance. The saccade velocity was negatively associated with age for large saccades more than 358 saccades (Wilson et al., Table 1 Mean velocities of smooth pursuit eye movement (n = 20) Side of eye
Leftward gaze (8/s)
Rightward gaze (8/s)
Left Right
13.45 1.23 13.85 1.31
13.55 1.10 13.70 1.56
1993; Warabi et al., 1984). Therefore, we examined only young to middle aged subjects to avoid any aging change by using relatively smaller (10–208) saccades. Oohira et al. (1981) reported normal saccadic eye velocities of each eye, while the subjects were examined monocularly with covered the other eye. They found no significant difference between the sides of eyes. Similarly, our data did not reveal a significant difference between centripetal and centrifugal velocities at reading distance under binocular view. Boghen et al. (1974) also reported that there was no significant difference between centripetal and centrifugal saccadic eye velocities. In contrast, it has been noted that abducting saccades are faster than adduction saccades under vergence (Averbuch-Heller et al., 1999). If this is the case, adduction velocity of right eye (dominant eye) should be slower than abduction velocity of left eye (non-dominant eye) on leftward gaze. However, we found that horizontal saccadic velocity of dominant eye was significantly faster than nondominant eye on leftward gaze as well as on rightward gaze. We do not have good explanation for our results, therefore, further studies are necessary to clarify the mechanism of this phenomenon. There have been several reports on the dominant eye in the visuo–oculomotor system. Ibi (1997) studied accommodation responses of dominant and non-dominant eyes and concluded that the dominant eye was in a tonic state and played the primary role in far-to-near accommodation in binocular viewing. Conversely, Kenyon et al. (1977) found that the eye motion was greater in the non-dominant eye during accommodative vergence. Kawata et al. (1991) suggested that the tonus of the ciliary muscle increased
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Fig. 2. A representative example of horizontal saccadic eye movement in a 26-year-old subject with the right dominant eye. There were no significant differences in the wave form and eye position between the two eyes, however, the velocities of the right eye was faster than the left eye. On leftward and rightward saccades, the mean velocity of the right eye were 5308/s and 4918/s while those of the left eye were 4458/s and 3858/s, respectively. A vertical dotted line indicates the onset of target movement.
unilaterally in the dominant eye alone on the basis of the finding that myopia was significantly more progressed in the dominant eye than in the non-dominant eye. Seyal et al. (1981) recorded pattern reversal visual evoked potentials by stimulating each eye. They found that the mean amplitude of the dominant eye was significantly greater than that of the non-dominant eye while the mean latency of the dominant eye was significantly shorter compared with that of the nondominant eye. Rombouts et al. (1996) also reported that when each eye was stimulated with flashing light, stimulation of the dominant eye activated a larger area of primary visual cortex than the non-dominant eye stimulation by using functional MRI (fMRI). Finally, Nakada (personal communication) found that when the subjects with the righthandedness performed saccadic eye movement, the left frontal eye field was more activated than the right frontal eye
field by using fMRI. Although which sides of the dominant eye was unknown, they indicated the ocular dominancy in the central nervous system which controls eye movements. This study may indicate that right-handed people have dominancy in the left frontal eye field as well as having dominant hemisphere in the left side. This observation partly supports the ocular dominancy in horizontal saccades found in our study. As well as eye dominance, we have reported the values of the parameter for smooth pursuit and saccadic eye movements of both eyes under binocular view. Baloh et al. (1976) found the considerable asymmetry between pursuit velocity to the rightward and to the leftward. In their report, the electrodes were placed medially and laterally to each eye for both bilateral monocular and bitemporal recordings, thus they did not specifically mention the conjugate eye
Fig. 3. Scatter plots showing horizontal latencies in all subjects. There were no significant differences between the right and left eyes.
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Fig. 4. Scatter plots showing horizontal velocities in all subjects. Mean velocities of the right eye were faster than that of the left eye on leftward and rightward saccades. Table 2 Mean latencies and velocities of horizontal saccadic eye movement (n = 18) Side of eye Leftward gaze
Rightward gaze
Latency (ms) Velocity (8/s) Left Right *
Latency (ms) Velocity (8/s)
188.2 46.5 406.8 70.0* 184.2 57.8 388.9 45.1* 195.1 35.6 426.8 63.3* 191.9 39.3 414.4 69.8*
p < 0.05.
Table 3 Mean latencies and velocities of vertical saccadic eye movement Side of eye Upward gaze (n = 16) Latency (ms) Left Right
Downward gaze (n = 18)
Velocity (8/s) Latency (ms) Velocity (8/s)
177.7 61.2.5 350.8 77.5 173.4 66.9 346.3 81.2 181.2 48.8 343.3 80.5 302.8 36.0 356.7 87.8
movements. We did not find the significant difference between centrifugal and centripetal pursuit velocity on each eye. In addition, we found no difference in the velocity between dominant eye and non-dominant eye. In other reports (Baloh et al., 1976; Moschner et al., 1994; Buttner et al., 1998), horizontal smooth pursuit eye movements were recorded at peak velocities of 11.38/s, 22.68/s, and 45.28/s. Since the parameters were gains but not velocities, we could not compare our data with theirs. However, Baloh et al. (1976) described that the eye velocity indicated a uniform high degree of pursuit accuracy (gain) in normal subjects at lower object velocities (7.38/s and 21.98/s), therefore, our data at 108/s (low object velocity) seem to be comparable with the gain data. Quantitative assessment of vertical eye movements was usually not performed because the vertical recordings represent a combination of eye and lid movement (Baloh et al., 1980; Barry and Melvill-Jones, 1965). Anatomically, superior rectus and superior oblique muscles are controlled by contralateral oculomotor complex. According to this anatomical control, there may be no significant difference in the velocity on side of eyes vertically. Although we have
shown ocular dominance in horizontal saccades, the presence of eye dominance was not evident in smooth pursuit velocities. This is probably due to the fact that each cerebral hemisphere contributes to smooth pursuit in both horizontal directions (Sharpe, 1998). The afferent pathway of the pursuit subsystem is the retino-geniculo-calcarine projections to the visual cortex (Yee, 1983). Ocular motor efferent signals are generated in both occipital lobes, perhaps in the visual association areas. For pursuit toward the left, efferent signals from the contralateral, right occipital lobe decussate via the splenium of the corpus callosum to join the efferent signals from the ipsilateral occipital lobe. In contrast, cortical neurons of the contralateral frontal eye field (Brodmann’s area 8) participate in the generation of saccades with ipsilateral direction (Yee, 1983). In our study, the viewing distance of the target (40 cm) may induce some vergence. In addition, horizontal saccades are never strictly conjugate, containing a transient divergence and convergence (Collewijn et al., 1995). However, our study showed an objective evidence that the eye dominance is present at reading distance in horizontal saccades.
References Averbuch-Heller, L., Lewis, R.F., Zee, D.S., 1999. Disconjugate adaptation of saccades: contribution of binocular and monocular mechanisms. Vision Res. 39, 341–352. Baloh, R.W., Kumley, W.E., Sills, A.W., Honrubia, V., Konrad, H.R., 1976. Quantitative measurement of smooth pursuit eye movements. Ann. Otol. 85, 111–119. Baloh, R.W., Langhofer, L., Honrubia, V., Yee, R.D., 1980. On-line analysis of eye movements using a digital computer. Aviat. Space Environ. Med. 51, 563–567. Barry, W., Melvill-Jones, G., 1965. Influence of eye lid movement upon electro-oculographic recording of vertical eye movement. Aerospace Med. 36, 855. Bechert, K., Koenig, E., 1996. A search coil system with automatic field stabilization, calibration, and geometric processing for eye movement recording in humans. Neuro. Ophthalmol. 16, 163–170.
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Boghen, D., Troost, B.T., Daroff, R.B., Dell’Osso, L.F., Birkett, J.E., 1974. Velocity characteristics of normal human saccades. Invest. Ophthalmol. 13, 619–623. Buttner, N., Geschwind, D., Jen, J.C., Perlman, S., Pulst, S.M., Baloh, R.W., 1998. Oculomotor phenotypes in autosomal dominant ataxias. Arch. Neurol. 55, 1353–1357. Clarke, A.H., Teiwes, W., Scherer, H., 1991. Video-oculography-an alternative method for measuring eye movements in all three orthogonal planes. In: Schmid, R., Zambarbieri, D. (Eds.), Oculomotor Control and Cognitive Processes-Normal and Pathological Aspects. Elsevier, Amsterdam, pp. 432–443. Collewijn, H., Mark, F., Jansen, T.C., 1975. Precise recording of human eye movements. Vision Res. 15, 447–450. Collewijn, H., Erkelens, C.J., Steinman, R.M., 1995. Voluntary binocular gaze-shifts in the plane of regard: dynamics of version and vergence. Vision Res. 35, 3335–3358. Enright, J.T., 1998. Estimating peak velocity of rapid eye movements from video recordings. Behav. Res. Meth. Instrum. Comput. 30, 349–353. Ibi, K., 1997. Characteristics of dynamic accommodation responses: comparison between the dominant and non-dominant eyes. Ophthal. Physiol. Opt. 17, 44–54. Kawata, K., Kasisho, Y., Miura, O., 1991. Ocular dominance from the viewpoint of refractive error. Folia. Ophthalmol. Jpn. 42, 1579–1583. Kenyon, R.V., Ciuffreda, K.J., Stark, L., 1977. Binocular eye movements during accomodative vergence. Vision Res. 18, 545–555.
Moschner, C., Perlman, S., Baloh, R.W., 1994. Comparison of oculomotor findings in the progressive ataxia syndromes. Brain 117, 15– 25. Oohira, A., Okamoto, M., Ozawa, T., 1981. Peak velocity of normal human saccadic eye movements. Jpn. J. Ophthalmol. 85, 167–173. Porac, C., Coren, S., 1976. The dominant eye. Psychol. Bull. 83, 880–897. Porta I.B., 1593. De refractione. Optic Parte; Libri Novem. Ex Officina Horatij Salvania. Naples: Apud Io Iacobum Carlinum and Anotnium Pacem. Rombouts, S.A.R.B., Barkhof, F., Sprenger, M., Valk, J., Scheltens, P., 1996. The functional basis of ocular dominance: functional MRI (fMRI) findings. Neurosci. Lett. 221, 1–4. Seyal, M., Sato, S., White, B.G., Porter, R.J., 1981. Visual evoked potentials and eye dominance. Electroencephalogr. Clin. Neurophysiol. 52, 424– 428. Sharpe, J.A., 1998. Neural control of ocular motor sysytems. In: Miller, N.R., Newman, NJ. (Eds.), Walsh & Hoyt’s Clinical Neuro-Opthalmology. fifth ed. Williams & Wikins, Maryland, pp. 1101–1167. Warabi, T., Kase, M., Kato, T., 1984. Effect of aging on the accuracy of visually guided saccadic eye movement. Ann. Neurol. 16, 449–454. Wilson, S.J., Glue, P., Ball, D., Nutt, D.J., 1993. Saccadic eye movement parameters in normal subjects. Electroencephalogr. Clin. Neurophysiol. 86, 69–74. Yee, R.D., 1983. Eye movement recordings as a clinical tool. Opthalmology 90, 211–222.
Ocular dominancy in conjugate eye movements at reading distance Ayame Oishi a, Shozo Tobimatsu b,*, Kenji Arakawa a, Takayuki Taniwaki a, Jun-ichi Kira a b
a Departments of Neurology, Neurological Institute, Graduate School of Medical Sciences, Kyushu University, Fukuoka 812-8582, Japan Departments of Clinical Neurophysiology, Neurological Institute, Graduate School of Medical Sciences, Kyushu University, Fukuoka 812-8582, Japan
Received 20 July 2004; accepted 25 March 2005 Available online 4 May 2005
Abstract We recorded conjugate eye movements to elucidate whether ocular dominancy was present at reading distance in 21 normal volunteers with the right-handedness by using a video-oculographic (VOG) measurement. This included the velocity of smooth pursuits, and the latency and velocity of saccades. We defined the dominant eye for each subject by means of the near–far alignment test and 20 subjects showed the right dominant eyes. Although the ocular dominancy was not found in the velocity of smooth pursuit and vertical saccades, the velocity of horizontal saccades in the dominant eyes was faster than that in the non-dominant eyes. These results suggest that the dominant eye is functionally activated prior to non-dominant eye in horizontal saccades at reading distance, which thus indicates the functional dominancy of the dominant eye in conjugate eye movements. # 2005 Elsevier Ireland Ltd and the Japan Neuroscience Society. All rights reserved. Keywords: Ocular dominancy; Conjugate eye movement; Reading distance; Saccade; Smooth pursuit
1. Introduction The members of a bilateral pair of structures in the body seldom exhibit perfect equality. Often, one member of the pair tends to be preferred over the other in behavioral coordination, or it seems to manifest physiological superiority. Thus, it is defined as dominant. Relationship between handedness and dominant hemisphere has been well described. The presence of the dominant eye is also known and has often been defined as the eye whose input is favored in behavioral coordinations (Porac and Coren, 1976). Porta (1593) first suggested that the near–far alignment test was useful to determine dominant eye. Several investigators (Rombouts et al., 1996; Ibi, 1997; Kawata et al., 1991; Seyal et al., 1981) have reported the presence of the dominant eye in the visuo-oculomotor system. However, to our knowledge, the presence of ocular dominance in conjugate eye movements at reading distance has not yet been established. The velocity of a target can be accurately controlled with simple electronic equipment and the saccadic and smooth * Corresponding author. Tel.: +81 92 642 5541; fax: +81 92 642 5545. E-mail address: [email protected] (S. Tobimatsu).
pursuit eye movements can be accurately recorded with electro-oculographic (EOG) techniques, using a digital computer. Computerized EOG technique can yield reasonable recordings of horizontal eye movements whereas vertical measurements are affected by lid artifacts with considerable interindividual differences (Bechert and Koenig, 1996). Furthermore, changes in illumination and in skin resistance affect the EOG recordings. Infrared oculography provides high-resolution measurements of horizontal and vertical eye movement, but over a limited range, especially vertically. Another problem is that the signal is lost when the eyes are closed. A magnetic fieldsearch coil method uses coils embedded in a silicone rubber ring that adheres to the sclera by suction, which overcomes most of the problems that limit both EOG and infrared oculography (Collewijn et al., 1975; Yee, 1983). However, the major drawbacks of this technique are the relatively high cost and discomfort, because the surface of the eye is anesthetized. Recently, a video-oculographic (VOG) measurement system has developed (Clarke et al., 1991). This system consists of CCD sensors and digital imaging process, which allows us to evaluate the conjugate eye movements under binocular vision more objectively. Therefore, we
0168-0102/$ – see front matter # 2005 Elsevier Ireland Ltd and the Japan Neuroscience Society. All rights reserved. doi:10.1016/j.neures.2005.03.013
264
A. Oishi et al. / Neuroscience Research 52 (2005) 263–268
recorded the conjugated eye movements under binocular view to elucidate the presence of ocular dominancy at reading distance by using the VOG measurement system.
2. Methods 2.1. Subjects Twenty-one normal subjects with the right-handed (10 males and 11 females), aged between 21 and 47 years (mean; 30.6 7.6 years), gave their informed consent for recording of their eye movements. Most were hospital or medical school staffs or their relatives, and all were drug-free and in good health. We defined the dominant eye for each subject by means of the near–far alignment test (Porac and Coren, 1976). Informed consent was obtained after the experimental nature had been fully explained. The Ethics committee of the Kyushu University of Faculty Medicine approved this study.
with the total amplitude of 208, and latencies and velocities ( peak velocities) of each eye were calculated by averaging 3–5 measurements in each subject. To exclude blink artifact, we adopted only vertical saccades whose fixation time was more than for 300 ms. Low time resolution of 60 Hz frame rate is overcome by the technique of ‘‘apparent peak velocity’’ because when saccadic is about 108 or larger, estimates of peak velocity on average are biased downward by less than 10% (Enright, 1998). 2.3. Statistical analysis Means and standard deviations were calculated for all parameters. Paired comparisons were made by Wilcoxon’s rank sum test, because the data were not normally distributed.
3. Results 3.1. Ocular dominancy
2.2. Visual stimuli and eye movement recordings Subjects sat on a chair with their head resting on a chinrest in a semi-darkened room, viewing the center of liquid crystal screen (29 cm 22 cm). Visual stimuli were presented at a distance of 40 cm with the 18 circle yellow target. In this paper, 108 or 208 indicates the distance between the central fixation point and target. The VOG measurement system (SMI company, Germany) was used to measure horizontal and vertical eye movements. The VOG system exploits current technology in CCD sensors mounted on a free-field mask with digital image processing (Clarke et al., 1991). We recorded binocular eye movement simultaneously, using this non-invasive system. Processing of the video images was made at a sample rate of 60 Hz for the vertical and horizontal components.
Twenty subjects showed dominant right eyes by the near– far alignment test while one male subject had dominant left eye and was excluded for further analysis. 3.2. Smooth pursuit eye movements Fig. 1 shows the raw data of a representative subject who showed the right dominant eye. There were no significant differences in the wave form and eye position between the two eyes. Mean values of smooth pursuit eye movements are summarized in Table 1. A significant difference was not found between the centripetal and centrifugal velocities. There was also no significant difference between the eye velocity in the right and left eyes in binocular pursuits. 3.3. Saccadic eye movements
2.2.1. Smooth pursuit eye movements Pursuit trials began with the appearance of the yellow fixation target at the central position on the monitor. The target moved sinusoidally with the total amplitude of 408 and peak velocity of 108/s. The mean rightward and leftward eye velocities of each eye were calculated from 7 to 10 consecutive cycles. 2.2.2. Saccadic eye movements Saccadic trials began with the appearance of the yellow target at the central position. The target stepped with predictable timing (2 s). Subjects were asked to follow the target light as soon as it moved. In the horizontal task, the target stepped pseudorandomly to the right or to the left, and latencies and velocities ( peak velocities) of each eye were calculated by averaging 10 measurements in each direction. In the vertical task, the target stepped pseudorandomly to upward or to downward
Fig. 2 shows the raw data of a representative subject with the right eye dominance. There were no significant differences in the wave form and eye position between the two eyes. Figs. 3 and 4 show scatter plots of all horizontal latencies and velocities, respectively. Mean latencies and velocities of horizontal and vertical saccades are summarized in Tables 2 and 3. On horizontal saccades, we excluded the data from two subjects because of their eyelashes artifacts. We also excluded the data from four subjects (upward) and two subjects (downward) on vertical saccades, respectively. On horizontal (leftward and rightward) saccades, there were no significant differences in the mean saccadic latencies between centrifugal and centripetal saccades (Table 2, Fig. 3). On the other hand, the mean velocities of the right eye on horizontal saccades toward the left and that of the left eye were 426.8 63.38/s and 406.8 70.08/s, respectively.
A. Oishi et al. / Neuroscience Research 52 (2005) 263–268
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Fig. 1. A representative example of smooth pursuit eye movement in a 32-year-old subject with the right dominant eye. There were no significant differences in the wave form and eye position between the two eyes. On leftward and rightward pursuits, the mean velocities of right eye were 148/s and 138/s while those of the left eye were 138/s and 138/s, respectively.
Thus, there was a significant difference between right (dominant) and left (non-dominant) eyes on horizontal gaze toward the left ( p < 0.05) (Fig. 4). Similarly, the mean velocities of the right eye on horizontal saccade toward the right were significantly faster than that of the left eye ( p < 0.05). On vertical (upward and downward) saccades, there were no significant differences in the mean saccadic latencies between the two eyes (Table 3). There was also no significant difference in the velocity values between centrifugal and centripetal saccades.
4. Discussion In the present study, all but one of subjects showed right dominant eye by the near–far alignment test. The mean horizontal saccadic velocities toward the right or left of the right eye were faster than those of the left eye. It has not been reported regarding the presence of the dominancy of central nervous system on conjugate eye movements. Therefore, this is the first report that demonstrates the presence of the dominant eye in conjugate eye movements at reading distance. The saccade velocity was negatively associated with age for large saccades more than 358 saccades (Wilson et al., Table 1 Mean velocities of smooth pursuit eye movement (n = 20) Side of eye
Leftward gaze (8/s)
Rightward gaze (8/s)
Left Right
13.45 1.23 13.85 1.31
13.55 1.10 13.70 1.56
1993; Warabi et al., 1984). Therefore, we examined only young to middle aged subjects to avoid any aging change by using relatively smaller (10–208) saccades. Oohira et al. (1981) reported normal saccadic eye velocities of each eye, while the subjects were examined monocularly with covered the other eye. They found no significant difference between the sides of eyes. Similarly, our data did not reveal a significant difference between centripetal and centrifugal velocities at reading distance under binocular view. Boghen et al. (1974) also reported that there was no significant difference between centripetal and centrifugal saccadic eye velocities. In contrast, it has been noted that abducting saccades are faster than adduction saccades under vergence (Averbuch-Heller et al., 1999). If this is the case, adduction velocity of right eye (dominant eye) should be slower than abduction velocity of left eye (non-dominant eye) on leftward gaze. However, we found that horizontal saccadic velocity of dominant eye was significantly faster than nondominant eye on leftward gaze as well as on rightward gaze. We do not have good explanation for our results, therefore, further studies are necessary to clarify the mechanism of this phenomenon. There have been several reports on the dominant eye in the visuo–oculomotor system. Ibi (1997) studied accommodation responses of dominant and non-dominant eyes and concluded that the dominant eye was in a tonic state and played the primary role in far-to-near accommodation in binocular viewing. Conversely, Kenyon et al. (1977) found that the eye motion was greater in the non-dominant eye during accommodative vergence. Kawata et al. (1991) suggested that the tonus of the ciliary muscle increased
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Fig. 2. A representative example of horizontal saccadic eye movement in a 26-year-old subject with the right dominant eye. There were no significant differences in the wave form and eye position between the two eyes, however, the velocities of the right eye was faster than the left eye. On leftward and rightward saccades, the mean velocity of the right eye were 5308/s and 4918/s while those of the left eye were 4458/s and 3858/s, respectively. A vertical dotted line indicates the onset of target movement.
unilaterally in the dominant eye alone on the basis of the finding that myopia was significantly more progressed in the dominant eye than in the non-dominant eye. Seyal et al. (1981) recorded pattern reversal visual evoked potentials by stimulating each eye. They found that the mean amplitude of the dominant eye was significantly greater than that of the non-dominant eye while the mean latency of the dominant eye was significantly shorter compared with that of the nondominant eye. Rombouts et al. (1996) also reported that when each eye was stimulated with flashing light, stimulation of the dominant eye activated a larger area of primary visual cortex than the non-dominant eye stimulation by using functional MRI (fMRI). Finally, Nakada (personal communication) found that when the subjects with the righthandedness performed saccadic eye movement, the left frontal eye field was more activated than the right frontal eye
field by using fMRI. Although which sides of the dominant eye was unknown, they indicated the ocular dominancy in the central nervous system which controls eye movements. This study may indicate that right-handed people have dominancy in the left frontal eye field as well as having dominant hemisphere in the left side. This observation partly supports the ocular dominancy in horizontal saccades found in our study. As well as eye dominance, we have reported the values of the parameter for smooth pursuit and saccadic eye movements of both eyes under binocular view. Baloh et al. (1976) found the considerable asymmetry between pursuit velocity to the rightward and to the leftward. In their report, the electrodes were placed medially and laterally to each eye for both bilateral monocular and bitemporal recordings, thus they did not specifically mention the conjugate eye
Fig. 3. Scatter plots showing horizontal latencies in all subjects. There were no significant differences between the right and left eyes.
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Fig. 4. Scatter plots showing horizontal velocities in all subjects. Mean velocities of the right eye were faster than that of the left eye on leftward and rightward saccades. Table 2 Mean latencies and velocities of horizontal saccadic eye movement (n = 18) Side of eye Leftward gaze
Rightward gaze
Latency (ms) Velocity (8/s) Left Right *
Latency (ms) Velocity (8/s)
188.2 46.5 406.8 70.0* 184.2 57.8 388.9 45.1* 195.1 35.6 426.8 63.3* 191.9 39.3 414.4 69.8*
p < 0.05.
Table 3 Mean latencies and velocities of vertical saccadic eye movement Side of eye Upward gaze (n = 16) Latency (ms) Left Right
Downward gaze (n = 18)
Velocity (8/s) Latency (ms) Velocity (8/s)
177.7 61.2.5 350.8 77.5 173.4 66.9 346.3 81.2 181.2 48.8 343.3 80.5 302.8 36.0 356.7 87.8
movements. We did not find the significant difference between centrifugal and centripetal pursuit velocity on each eye. In addition, we found no difference in the velocity between dominant eye and non-dominant eye. In other reports (Baloh et al., 1976; Moschner et al., 1994; Buttner et al., 1998), horizontal smooth pursuit eye movements were recorded at peak velocities of 11.38/s, 22.68/s, and 45.28/s. Since the parameters were gains but not velocities, we could not compare our data with theirs. However, Baloh et al. (1976) described that the eye velocity indicated a uniform high degree of pursuit accuracy (gain) in normal subjects at lower object velocities (7.38/s and 21.98/s), therefore, our data at 108/s (low object velocity) seem to be comparable with the gain data. Quantitative assessment of vertical eye movements was usually not performed because the vertical recordings represent a combination of eye and lid movement (Baloh et al., 1980; Barry and Melvill-Jones, 1965). Anatomically, superior rectus and superior oblique muscles are controlled by contralateral oculomotor complex. According to this anatomical control, there may be no significant difference in the velocity on side of eyes vertically. Although we have
shown ocular dominance in horizontal saccades, the presence of eye dominance was not evident in smooth pursuit velocities. This is probably due to the fact that each cerebral hemisphere contributes to smooth pursuit in both horizontal directions (Sharpe, 1998). The afferent pathway of the pursuit subsystem is the retino-geniculo-calcarine projections to the visual cortex (Yee, 1983). Ocular motor efferent signals are generated in both occipital lobes, perhaps in the visual association areas. For pursuit toward the left, efferent signals from the contralateral, right occipital lobe decussate via the splenium of the corpus callosum to join the efferent signals from the ipsilateral occipital lobe. In contrast, cortical neurons of the contralateral frontal eye field (Brodmann’s area 8) participate in the generation of saccades with ipsilateral direction (Yee, 1983). In our study, the viewing distance of the target (40 cm) may induce some vergence. In addition, horizontal saccades are never strictly conjugate, containing a transient divergence and convergence (Collewijn et al., 1995). However, our study showed an objective evidence that the eye dominance is present at reading distance in horizontal saccades.
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