Eye movements of laterally eyed birds are not independent

Abstract

SUMMARYMost birds have laterally placed eyes with two largely separated visual fields. According to studies in pigeons laterally eyed birds move their eyes independently in most situations, eye coordination just occurred during converging saccades towards frontal stimuli. Here we demonstrate for the first time that laterally eyed zebra finches show coordinated eye movements, regarding direction and amplitude. Spontaneous and visually elicited movements of the two eyes were recorded simultaneously, using a newly developed eye tracking system. We found that, if one eye moves in a certain direction, the other eye simultaneously performs a counter-movement in the opposite direction. Based on these data we developed a hypothesis of how laterally eyed birds cope with the situation in which the left and right eye simultaneously obtain images with different content. We suggest that the counter-movements maintain the spatial relationship of the two visual fields. 'Oculospatial constancy', as we call it, facilitates the combination of the left and right visual percept on the level of peripheral or unattended viewing, and the localization of appearing stimuli within the whole visual field. As soon as two visual stimuli simultaneously appear in the left and right visual field, the birds decide on one stimulus and direct the fovea of the appropriate eye towards it for high resolution analysis, the other eye simultaneously performing a counter-saccade. This leads to the assumption that, in contrast to simultaneous peripheral perception with two eyes, the processing of foveal information is possible only for one eye at one time.

Oculomotor strategy of an avian ground forager: tilted and weakly yoked eye saccades

“…Similar weakly yoked saccades have also been found in phylogenetically distant species within Accipitriformes and Caprimulgiformes (Wallman and Pettigrew, 1985). However, the weakly yoked saccades are different from the conjugate or strongly yoked saccades present in other Passeriformes, like the zebra finch (Voss and Bischof, 2009). Functionally speaking, weakly yoked saccades could actually be deemed similar to independent saccades.…”

“…A horizontal eye movement axis, which has previously been found in chickens (Schwarz et al, 2013) and zebra finches (Voss and Bischof, 2009), would allow birds to keep their centers of acute vision along the prominent horizon. However, contrary to our expectations, we found that European starlings primarily move their eyes along a tilted axis (13.46 deg) (Fig.…”

“…Zebra finches (Taeniopygia guttata) have both a central fovea and temporal area (Voss, 2005). In this case, both the axis between the fovea and the area and the axis of eye movement are aligned with the horizon (Voss and Bischof, 2009). Pigeons (Columba livia), which have a central fovea and a dorso-temporally shifted area, have a more complex pattern of eye movement .…”

“…conjugate) saccades for frontal viewing but independent saccades for lateral viewing . Functionally, yoked saccades maintain a constant relationship between the two eyes, potentially allowing the brain to perceive a joint panoramic visual field rather than separate left and right hemifields (Voss and Bischof, 2009). Independent saccades, in contrast, release the two eyes from restricting one another's movement patterns, allowing them to concomitantly execute alternative tasks.…”

“…Other species show different patterns. The eyes of the tawny frogmouth (Podargus strigoides) and little eagle (Hieraaetus morphnoides) are weakly yoked (Wallman and Pettigrew, 1985), whereas zebra finch eyes are strongly yoked (Voss and Bischof, 2009).…”