Figure 1.
Examples of coronal, a, sagittal, c, and axial, d, images at 34+4GW, 21+1GW, and 26 GW respectively and the lines drawn to measure bulb positions and to calculate bulb deviations.
a Coronal frame of a dynamic MR sequence. A horizontal line at the level of the most caudal part of the hyperintense nasal choanae is drawn, A. Vertical line at the vertical axis of both lenses are drawn separately, B and C, craniocaudally and perpendicularly to the horizontal line A. b Schematic drawing of the eyeball on two sequential frames with the bulb radius on these frames forming an isoscles triangle and allowing the calculation of the angle δ of bulb deviation. (Details concerning the calculation of the angles of bulb deviations between sequential coronal frames can be found in the Methods section.) c Sagittal frame of a dynamic MR sequence. Two lines were marked as references to indicate the hypointense roof of the orbit, E, and the longest axis of the sagittally depicted lens, F. The angle ε enclosed by these two lines was measured and differences between the angle ε on sequential frames were calculated. d shows an axial frame of a dynamic MR sequence. Three lines were marked as references to indicate the intracranial midline, G, and the longest axis of the axially depicted lens in each eye, H and I. The angle enclosed by the line through the longest axis of the lens and the intracranial midline was measured on each side, α and β.
Table 1.
Modified classification of fetal eye movements based on a classification made by Birnholz [3] using ultrasound findings.
Table 2.
Descriptive statistics of examined fetuses.
Table 3.
Descriptive statistics of dynamic SSFP MRI sequences.
Figure 2.
Measurements of bulb positions on sequential coronal images.
a Seven sequential frames of a coronal dynamic SSFP sequence in a fetus at 34+4 GW (upper row) and the same frames with measurements of bulb positions (lower row). b Based on the measurements of bulb positions shown in Figure 2a, bulb deviations were calculated and plotted against time. Slow binocular deviations of 3.3° of the right and 4.3° of the left eyeball on seven sequential frames at an average speed of 3.3°/s (right) and 4.3°/s (left). See Table S1 for complete data on measurements and angular velocities.
Figure 3.
Measurements of bulb positions on sequential axial images.
a Thirty-three sequential frames of an axial dynamic SSFP sequence in a fetus at 26 GW (first, third, and fifth rows) and the same frames with measurements of bulb positions (second, fourth, and sixth rows). b Bulb deviations measured on the 33 sequential axial frames shown in Figure 3a were calculated and plotted against time. Initial slow binocular deviation with lateral movement of one eyeball and medial movement of the other eyeball, with amplitudes of 19.7° and 13.6°, respectively, at average velocities of 5.1°/s and 4.1°/s (0.00–4.00 s). Subsequently, the eyeballs were repositioned more rapidly at average velocities of 9.9°/s and 9.1°/s (4.00–5.33 s). See Table S2 for complete data on measurements and angular velocities.
Figure 4.
Measurements of bulb positions on sequential sagittal images.
a Eight sequential frames of a sagittal dynamic SSFP sequence in a fetus at 21+1 GW (upper row) and the same frames with measurements of bulb positions (lower row). b Bulb deviations on eight sequential sagittal frames shown in Figure 4a were calculated and plotted against time. Craniocaudal deviation of one sagittally depicted eyeball with an amplitude of 19.6° at an average velocity of 39°/s, and the subsequent reposition at an average velocity of 37°/s. See Table S3 for complete data on measurements and angular velocities.
Figure 5.
Measurements of bulb positions on sequential axial images.
a Thirty-nine sequential frames of an axial dynamic SSFP sequence in a fetus at 27+1 GW (first, third, and fifth rows) and the same frames with measurements of bulb positions (second, fourth, and sixth rows). b Bulb deviations on the 39 sequential axial frames shown in Figure 5a were calculated and plotted against time. Initially, this fetus showed a slow binocular version (0–2.17 s) with amplitudes of 14.2° and 19.1° of the right and left eye, respectively, at velocities of 6.6°/s and 8.8°/s. Subsequently, the eyeballs were repositioned (2.17–3.67 s) at average velocities of 8.3°/s (right) and 9.0°/s (left). A second version follows (3.67–4.67 s) with a fast initial component at average velocities of 65°/s and 75.8°/s for the right and the left eyeballs respectively. The second part of this deviation decreased in average to 11.8°/s and 16.2°/s respectively. The entire amplitudes of these biphasic deviations were 38.4° and 46.0°, with average velocities of 38.4°/s and 46°/s for the right and the left eyeball, respectively. The eye movements in this sequence are among the fastest observed in this study. The right bulb shows a deviation of 15.7° between 4.00 s and 4.17 s (94°/s), and the left bulb shows a deviation of 20.2° between 3.83 s and 4.00 s (121.0°/s). From 4.67–6.33 s, a slow reposition of both eyeballs at velocities of 14.8°/s (right) and 20.0°/s (left) follows. See Table S4 for complete data on measurements and angular velocities.
Figure 6.
Prevalence of different types of eye movements among all fetuses.
In 11 fetuses (15.9%), two different types of eye movements were observed.
Figure 7.
Intervals during which different types of eye movements could be observed in this study and in previous reports on prenatal ultrasound examinations [3], [4] and in premature newborns [6].
Figure 8.
Prevalence of different types of eye movements in three fetal age groups.
Asterisks and brackets indicate those types of eye movements in which significant differences were found.
Figure 9.
Prevalence of parallel bulb position and cross-eyed condition, as well as lack of images depicting both lenses to evaluate bulb position.
Figure 10.
Structures of the brainstem responsible for the generation of eye movements in fetuses.
riMLF = rostral interstitial nucleus of the medial longitudinal fasciculus; INC = interstitial nucleus of Cajal; III = nucleus of the third cranial nerve; (oculomotor nerve); IV = nucleus of the fourth cranial nerve (trochlear nerve); VI = nucleus of the sixth cranial nerve (abducent nerve); PPRF = paramedian pontine reticular formation; MVN = medial vestibular nucleus; NPH = nucleus prepositus hypoglossi.