Abstract

Fig. 1. Huey’s [10] lever device to record horizontal eye movements. a Eye movements made during reading were recorded with this technique; from Huey [11]. b The tracing on the smoked drum was photographed and then engraved; from Wade et al. [1].

History of Eye Movement Recording

Very early qualitative descriptions of eye movements originated at the beginning of the 18th century [3]. More accurate descriptions, based on the observation of afterimages, were made at the end of the 18th century. Using this method, Wells [4] described the slow and fast phases of vestibular nystagmus. The occurrence of saccades during reading was first reported by Javal [5] and Lamare [6], who used a rubber tube connected to the conjunctiva and both ears. With this device, each eye movement caused a sound that was heard. Hering [7] used a similar acoustic device in combination with the technique of afterimages. The first attempts to record eye movements were made at the end of the 19th century. Ahrens [8], Delabarre [9], and Huey [10, 11] used devices consisting of a lever attached to a plaster eyecup. A bristle at the end of the lever recorded the eye movements on the smoked drum of a kymograph. A schematic outline of the system used by Huey [11] and an original recording are shown in figure 1. This method had the fundamental drawback that the inertial forces between apparatus and eye could injure the eye mechanically. The device was also too heavy for the large accelerations occurring during saccades. To overcome this problem, Javal [12] suggested recording the reflection of a light beam from a little mirror attached to the conjunctiva, a method that was not successfully applied before von Romberg and Ohm [13] used it to measure ocular torsion. This technique was, however, still too invasive to be adopted by many researchers.

A more elegant approach that avoided mechanical contact with the eye was chosen by Dodge and Cline [14]. They developed the first photographic method and recorded the corneal reflection of a bright vertical line on a moving photographic plate. This system can be considered an early antecedent of the modern system that uses light reflections from the cornea and the lens to measure the orientation of the eye without having any contact with it. These so-called double Purkinje image (DPI) eye trackers [15] reach very high resolution ( 0.017 ), accuracy (0.017 ), and bandwidth (500 Hz) (DPI Eyetracker Gen 5.5, Fourward Technologies, Inc., Buena Vista, Va., USA). However, their accuracy is much lower during the high accelerations and decelerations of saccades, because the lens is not rigidly but elastically connected to the eyeball. This causes the large dynamic overshoot of saccade traces recorded with DPI eye trackers [16]. The very high accuracy of the DPI eye tracker during steady fixation is due to the fact that they use the angular differences between light reflections which are insensitive to small translations between the eye and the tracker. The complex mechanics involved in DPI trackers make these devices very expensive (monocular: USD 60,000; binocular USD 115,000).

The electro-oculogram (EOG) was developed as another means to avoid any mechanical contact with the eye. The history of the EOG was described by Brandt and Büchele [17]. Schott [18] and Meyers [19] measured electrical potentials with skin electrodes attached near the eye. They erroneously assumed that changes of the measured potentials were mainly related to electrical activity of the eye muscles. Mowrer et al. [20] discovered that the EOG is primarily caused by the electrical dipole between cornea and retina, which moves with the eye. Jung [21] applied this method to record horizontal and vertical components of the eye position simultaneously. This signaled a remarkable progress, since previous recording techniques had been restricted to one movement direction only. Moreover, the EOG is still the only measurement technique that allows to record eye movements while the eyes are closed. This is of particular interest for sleep research. The EOG will be described in more detail in the second part.

The second noninvasive measurement technique to become widely used is based on the intensity of infrared light reflected from the eye. Infrared reflection devices (IRDs) measure the intensity of these reflections by photosensitive elements placed at different locations in front the eye. The differences between these measures are used to determine the eye position. The first system of this type was developed by Torok et al. [22]. A modern variant of the IRD will be discussed later in the second part. Because fiber optic cables can be used to spatially separate the location where light intensity is collected and the location of the photodiodes used to measure the intensity, this method was also adopted for eye movement recordings together with functional magnetic resonance imaging techniques [23].

None of the recording methods mentioned so far were able to quantify all three rotatory degrees of freedom of the eye simultaneously. Vertical and horizontal movement components could be quantified by the EOG, IRD, or the DPI tracker, but these devices cannot measure the orientation of the eye around the axis of view (ocular torsion), which is of special interest when examining the coordination of the three pairs of eye muscles. Von Romberg and Ohm [13] measured pure ocular torsion (during straight-ahead fixation) with their mirror system mentioned above. Howard and Evans [24] give a more detailed review of the early history of the measurement of ocular torsion. Already in the 19th century, the technique of afterimages had provided important findings about ocular torsion during fixation. Ruete [25] described the relation between gaze direction and ocular torsion and attributed it to his friend Listing (professor of mathematical physics in Göttingen) [26]. Von Helmholtz [27] discovered most of the geometric implications of ‘Listing’s law’. This field of research became of increasing interest when the magnetic search coil technique developed by Robinson [28] and Collewijn et al. [29] was extended by Collewijn et al. [30] and Kasper and Hess [31] to cover 3-D movements. The method is based on the voltages induced in coils by two or three orthogonal, rapidly alternating magnetic fields. The coils are embedded in a soft plastic annulus that adheres elastically to the eyeball. One coil is sufficient to measure gaze direction. Two coils with different orientations must be molded in the plastic annulus to measure gaze direction and ocular torsion simultaneously. The search coil method combines high spatial and temporal resolution and is so far the most precise method for measuring ocular torsion during eccentric gaze. With this technique it became possible to extend Helmholtz’s 3-D analysis of fixation to the full range of oculomotor performance [32].

Like other methods based on contact lenses, the search coil technique has the main disadvantage of being invasive. Therefore, considerable effort was made to evaluate the 3-D eye position on the basis of photographic images of the eye. All photographic methods are based on the detection and localization of eye-fixed markers (pupil, limbus, iris signatures, episcleral blood vessels) in image coordinates. The eye position with respect to the head can be computed from these image coordinates if the camera is firmly attached to the head. Otherwise, head-fixed markers can be used to compensate for relative translations between head and camera. Pioneers in these techniques, Brecher [33], Miller [34], Howard and Evans [24], detected and localized these markers manually and individually for each image. Howard and Evans [24] described a method for computing 3-D angular eye positions from the image coordinates of the markers.

Video-oculography (VOG), defined as the use of these methods for dynamic measure of eye movements, became feasible with the rapid development of