The pupillary light responses of animals; a review of their distribution, dynamics, mechanisms and functions

Abstract

The timecourse and extent of changes in pupil area in response to light are reviewed in all classes of vertebrate and cephalopods. Although the speed and extent of these responses vary, most species, except the majority of teleost fish, show extensive changes in pupil area related to light exposure. The neuromuscular pathways underlying light-evoked pupil constriction are described and found to be relatively conserved, although the precise autonomic mechanisms differ somewhat between species. In mammals, illumination of only one eye is known to cause constriction in the unilluminated pupil. Such consensual responses occur widely in other animals too, and their function and relation to decussation of the visual pathway is considered. Intrinsic photosensitivity of the iris muscles has long been known in amphibia, but is in fact widespread in other animals. The functions of changes in pupil area are considered. In the majority of species, changes in pupil area serve to balance the conflicting demands of high spatial acuity and increased sensitivity in different light levels. In the few teleosts in which pupil movements occur they do not serve a visual function but play a role in camouflaging the eye of bottom-dwelling species. The occurrence and functions of the light-independent changes in pupil size displayed by many animals are also considered. Finally, the significance of the variations in pupil shape, ranging from circular to various orientations of slits, ovals, and other shapes, is discussed.

Elaborate pupils in skates may help camouflage the eye

“…While it has been suggested that pupils may aid in camouflaging the eye (Muntz, 1977;Douglas 2018;Douglas et al, 1998;, this has never been tested experimentally. The two experiments reported here present evidence that the elaborate pupil shape of the skate Leucoraja erinacea may indeed serve a camouflage function.…”

“…Most pupils respond to light by constricting. This carefully regulates the amount of light entering the eye and it is a crucial component in optimizing resolution and sensitivity in the retina (Wilcox and Barlow, 1975;Hammond and Mouat, 1985;Land and Nilsson, 2012;Douglas 2018). A round, dilated pupil is often a very conspicuous structure that stands out, possibly giving away the location of a lurking predator, or camouflaging prey animal.…”

“…Some animals have unusually shaped pupils, such as the mobile W-shaped pupil of cuttlefish, or the U-shaped pupils that are seen in some skates, rays, fish and squid. Several publications state that these pupils are found in species that spend significant amounts of time camouflaging on the substrate, and that these pupils might help camouflage the eye (Muntz, 1977;Douglas 2018;Douglas et al, 1998;. By giving the pupil outline a less regular shape, allowing the eye to better blend into its surroundings, the likelihood of visual edge detectors recognizing the shape as belonging to an eye would be reduced.…”

“…Importantly, while light intensity is the most obvious driving force of the pupillary reflex, it is known that light is not the only factor influencing pupil dilation and constriction (Hess and Polt, 1964;Muntz, 1977;Messenger, 1981;Gamlin et al, 1998;Barbur et al, 2002;Einhäuser et al, 2007;Bradley et al, 2008;Douglas, 2018). For this reason, it may not be surprising to find that animals, especially those with elaborate pupil shapes, actively using their pupils for non-vision related tasks, such as camouflage.…”

Pupil diameter tracks statistical structure in the environment

“…To test whether this effect reflects a common sensorimotor strategy across species, we conducted experiments in humans and macaque monkeys. While the brainstem circuit for the PLR is preserved between these two species [11], there are systematic differences in pupil dynamics between monkeys and humans [12], and it is unclear whether the pupil is under the same amount of cortical/cognitive control.…”