Initiation and Stability of Pursuit Eye Movements in Simulated Retinal Prosthesis at Different Implant Locations

Aretinal prosthesis is an electronic device composed of an electrode array attached over the inner limiting membrane (epiretinal implant) or inserted between the retina and the retinal pigment epithelium in place of degenerated photoreceptors (subretinal implant) and an image processing unit that transforms the incoming light pattern captured by a sensor into electrical charges that stimulate the remaining inner retinal neurons through the electrode array. Neural responses to the stimulation elicit a sensation of patterned light or phosphenes, called prosthetic vision.1-3 Such prostheses have been developed to restore some functional vision in those with outer retinal blindness. Although most prototype prostheses under testing use an image sensor in fixed relation to the head (head-centric), research on prostheses with the image sensor placed inside the eye (eye-centric) is under way. With eyecentric technology, prosthesis wearers may direct sight using eye movements, as is the case in natural vision. However, retinal prostheses have far lower spatial resolution than the resolution of the normal retina4,5 (Wilke R, et al. IOVS 2006; 47:ARVO E-Abstract 3202) and may have to be implanted outside the fovea because of anatomic and pathologic conditions, such as the eccentric displacement of second- and third-order neurons around the foveola. A twofold question thus arises: How will eye movements be affected by a low-resolution retinal prosthesis and by the implant location on the retina? Eye movements are a basic visual function and play an important role in acquiring visual information.6,7 Prosthetic vision with an implant location outside the fovea resembles eccentric viewing in patients with a central scotoma, caused by conditions in which foveal vision is damaged but some peripheral vision remains functional. These patients often develop a retinal area outside the scotoma, called preferred retinal locus (PRL), to be used for fixation.8-10 A PRL usually resides next to the scotoma and can be thought of as a “high-end” retinal prosthesis that is placed eccentrically and has spatial resolution lower than foveal vision but higher than the prosthetic vision made possible by current technology. Studies have shown that, through practice, patients with central scotoma and normally sighted subjects with a simulated central scotoma could direct their PRL using eye movements.11-13 PRLs have the following characteristics. First, fixation with the PRL is less stable than foveal fixation, and it decreases with increasing eccentricity, resulting in jerky saccades for refixation.14 Second, visually guided saccades with a PRL, compared with normal saccades, have longer latency, longer duration, slower velocity, and poorer accuracy.12 Those saccades are usually undershot in proportion to target eccentricity.12 For pursuit eye movements, one study on simulated central scotoma showed that spatial accuracy decreased with the increase of scotoma size or PRL eccentricity.11 Those findings suggest that extrafoveal viewing with a retinal prosthesis affect oculomotor dynamics temporally and spatially. It has been reported that PRL above or below the fovea might offer better control of horizontal eye movements.15 Studies of simulated prosthetic vision, though few, have shown effects of implant location on functional vision. For example, Sommerhalder et al.16,17 studied the effects of implant location on text reading and found that, in simulated prosthetic vision subtending a 10° × 3.5° visual field with 286 phosphenes, subjects' reading accuracy was approximately 90% when the visual field was 5° below foveal fixation but was reduced to approximately 25% to 30% when the visual field was 15° below foveal fixation. Horizontal pursuit eye movements are often used in the activities of daily living, such as in preparing food and monitoring a passing vehicle or moving object.,18,19 and are thus functionally important for future retinal prosthesis wearers. Pursuit eye movements can be characterized by two variables, latency (the time between the onset of the moving target and the onset of eye movement) and accuracy (the spatial difference between the target position and the fixation position during pursuit).7 Latency and accuracy reflect the function of oculomotor control. The present study was undertaken to assess the possible effects of implant location on latency and stability of horizontal pursuit eye movement. Stability refers to the spatial relationship between the target position and fixation position. The information to be attained from the present research can be used as a basis for future studies of eye movements in nonhorizontal directions. The investigation was carried out in normally sighted subjects in natural vision and in simulated prosthetic vision, allowing manipulation of implant location and within-subject comparisons across experimental conditions. To assess functional usefulness of such eye movements, we designed an experimental paradigm—a signal detection task— commonly used in behavioral research. The task required the subject to visually track a horizontally moving target and to press a key whenever the target briefly jumps. By measuring how quickly the subject detects a jump and reacts and how accurate the detection is, we can assess behavioral performance as a function of different viewing conditions.