Eye movements in chameleons are not truly independent – evidence from simultaneous monocular tracking of two targets

Abstract

Chameleons perform large-amplitude eye movements that are frequently referred to as independent, or disconjugate. When prey (an insect) is detected, the chameleon's eyes converge to view it binocularly and 'lock' in their sockets so that subsequent visual tracking is by head movements. However, the extent of the eyes' independence is unclear. For example, can a chameleon visually track two small targets simultaneously and monocularly, i.e. one with each eye? This is of special interest because eye movements in ectotherms and birds are frequently independent, with optic nerves that are fully decussated and intertectal connections that are not as developed as in mammals. Here, we demonstrate that chameleons presented with two small targets moving in opposite directions can perform simultaneous, smooth, monocular, visual tracking. To our knowledge, this is the first demonstration of such a capacity. The fine patterns of the eye movements in monocular tracking were composed of alternating, longer, 'smooth' phases and abrupt 'step' events, similar to smooth pursuits and saccades. Monocular tracking differed significantly from binocular tracking with respect to both 'smooth' phases and 'step' events. We suggest that in chameleons, eye movements are not simply 'independent'. Rather, at the gross level, eye movements are (i) disconjugate during scanning, (ii) conjugate during binocular tracking and (iii) disconjugate, but coordinated, during monocular tracking. At the fine level, eye movements are disconjugate in all cases. These results support the view that in vertebrates, basic monocular control is under a higher level of regulation that dictates the eyes' level of coordination according to context.

Dynamics of gaze control during prey capture in freely moving mice

“…Thus, the stable relative alignment of the two eyes during approach likely reflects stabilization of the head itself. While several species with laterally-placed eyes use convergent eye movements during prey capture to create a wider binocular field [16][17][18][19] , our results show that mice do not utilize this strategy during prey capture. These results suggest that the 40 degree binocular zone is sufficient for tracking centrally located objects.…”

“…How then do animals with laterally placed eyes target prey directly in front of them, especially when these targets can rapidly move in and out of the narrow binocular field? This could require the ability to modulate the amount of binocular overlap, through directed lateral eye movements, to generate a wider binocular field, such as in the case of cuttlefish [16] , fish [17] , many birds [18] , and chameleons [19] . In fact, these animals specifically rotate their eyes inward before striking prey, thereby creating a larger binocular zone.…”

Dynamics of gaze control during prey capture in freely moving mice

“…How then do animals with laterally placed eyes target prey directly in front of them, especially when these targets can rapidly move in and out of the narrow binocular field? This could require the modulation of the amount of binocular overlap, through directed lateral eye movements, to generate a wider binocular field, such as in the case of cuttlefish ( Feord et al, 2020 ), fish ( Bianco et al, 2011 ), many birds ( Martin, 2009 ), and chameleons ( Katz et al, 2015 ). In fact, these animals specifically rotate their eyes nasally before striking prey, thereby creating a larger binocular zone.…”

Retinal topography and microhabitat diversity in a group of dragon lizards

“…The high degree of similarity of the fovea and the horizontal streak among the six species studied here suggests that these are conserved topographic features of the retina across ecological niches and that they are likely shared by other Ctenophorus species. While independent eye movements in chameleons (Hews, Castellano, & Hara, ; Watt & Joss, ) and the lateralization of visually mediated behaviors in lizards has received some attention (Katz et al, ; Ott, ), the relevance of specific retinal regions and therefore the regions of the visual field which they subtend remains poorly understood. This novel information on the topographic specialization of neuron density in the retina of Ctenophorus species provides a solid anatomical foundation for future behavioral experiments exploring visually mediated behaviors across the visual field.…”