Fetal Eye Movements on Magnetic Resonance Imaging

Abstract

ObjectivesEye movements are the physical expression of upper fetal brainstem function. Our aim was to identify and differentiate specific types of fetal eye movement patterns using dynamic MRI sequences. Their occurrence as well as the presence of conjugated eyeball motion and consistently parallel eyeball position was systematically analyzed.MethodsDynamic SSFP sequences were acquired in 72 singleton fetuses (17–40 GW, three age groups [17–23 GW, 24–32 GW, 33–40 GW]). Fetal eye movements were evaluated according to a modified classification originally published by Birnholz (1981): Type 0: no eye movements; Type I: single transient deviations; Type Ia: fast deviation, slower reposition; Type Ib: fast deviation, fast reposition; Type II: single prolonged eye movements; Type III: complex sequences; and Type IV: nystagmoid.ResultsIn 95.8% of fetuses, the evaluation of eye movements was possible using MRI, with a mean acquisition time of 70 seconds. Due to head motion, 4.2% of the fetuses and 20.1% of all dynamic SSFP sequences were excluded.Eye movements were observed in 45 fetuses (65.2%). Significant differences between the age groups were found for Type I (p = 0.03), Type Ia (p = 0.031), and Type IV eye movements (p = 0.033). Consistently parallel bulbs were found in 27.3–45%.ConclusionsIn human fetuses, different eye movement patterns can be identified and described by MRI in utero. In addition to the originally classified eye movement patterns, a novel subtype has been observed, which apparently characterizes an important step in fetal brainstem development. We evaluated, for the first time, eyeball position in fetuses. Ultimately, the assessment of fetal eye movements by MRI yields the potential to identify early signs of brainstem dysfunction, as encountered in brain malformations such as Chiari II or molar tooth malformations.

The relationship between eye movement and vision develops before birth

“…Four fetal eye movement patterns were initially characterized based on early ultrasound observations ( Birnholz, 1981 ): Type I eye movements were described as single, transient deviations consisting of a bulb deviation, and a slower return back to the resting position, single but prolonged eye movements as Type II, complex sequences of eye movements to different directions without periodicity as Type III, and repetitive nystagmoid eye movements as Type IV. Additionally splitting of Type I eye movements into Type Ia (fast deviation, slower reposition) and Type Ib (fast deviation, equally fast reposition) was based on eye movement observation during MRI measurements ( Woitek et al, 2013 ). It has already been shown that MRI sequences provide a valuable tool for visualizing and categorizing fetal eye movements ( Brémond-Gignac et al, 1997 ; Woitek et al, 2013 ).…”

“…Additionally splitting of Type I eye movements into Type Ia (fast deviation, slower reposition) and Type Ib (fast deviation, equally fast reposition) was based on eye movement observation during MRI measurements ( Woitek et al, 2013 ). It has already been shown that MRI sequences provide a valuable tool for visualizing and categorizing fetal eye movements ( Brémond-Gignac et al, 1997 ; Woitek et al, 2013 ). While this method was initially developed to serve as an indicator for ocular development and as an indirect biomarker to detect malformations affecting the brainstem, our study investigates for the first time the networks responsible for the processing of eye movement in utero , enabling the purest form of a natural self induced stimulus, eye movement.…”

“…Responses to visual stimuli were reported from as early as the 28th gestational week using neural electromagnetic activity measures acquired with magnetic resonance encephalography (MEG; Eswaran et al, 2004 ). In utero resting state networks ( Schöpf et al, 2012 ; Thomason et al, 2013 ), and fetal eye movements ( Birnholz, 1981 ; Woitek et al, 2013 ) were observed independently, but no visual stimulus response could be located in fetal functional magnetic resonance imaging (fMRI; Fulford et al, 2003 ). It is well established that resting-state fMRI is a powerful tool to study the organization of functional brain networks ( Rosazza et al, 2012 ).…”

Fetal movements: the origin of human behaviour

“…Facial expressions such as smiling movements, pouting, or scowling can be observed during the last trimester of pregnancy by means of 4D ultrasound recordings, but their early ontogeny is not yet known. Fetal eye movements are particularly interesting (Video S5, online supporting information): fast deviations with slower/faster reposition, single prolonged eye movements, complex sequences, and nystagmoid eye movements can be observed from 15 to 17 weeks onwards 27 . From about 30 weeks onwards, clusters of rapid eye movements can be observed 8 .…”

“…Fetal eye movements are particularly interesting (Video S5, online supporting information): fast deviations with slower/faster reposition, single prolonged eye movements, complex sequences, and nystagmoid eye movements can be observed from 15 to 17 weeks onwards. 27 From about 30 weeks onwards, clusters of rapid eye movements can be observed. 8 The fetus also starts to display blinking by opening and closing eyelids at 23 to 26 weeks' gestation.…”