Parietal-Eye Photoreceptors in Lizard

This section briefly describes the lizard parietal-eye photoreceptor, for the reason that it shows very unusual antagonistic light responses, with underlying mechanisms that reveal the evolutionary path of rod and cone phototransduction.

Many lizards have a parietal eye, situated on the forehead between the two regular (lateral) eyes. The exact function of this eye is still not entirely clear, but the best suggestion so far is that it informs the animal about the passage of time in the course of the day by registering changes in the relative intensities of the spectral components of the ambient light as the day progresses.

The parietal eye resembles the lateral eyes by having a cornea, a lens, and a retina. The retina, however, has only photoreceptors, ganglion cells, and glial cells (i.e., no second-order and associative neurons, including bipolar, horizontal, and amacrine cells, and no retina pigment epithelium). It is also opposite in orientation to the lateral-eye retina in that the photoreceptors face the front of the eye and are therefore the first neurons in the retina to encounter light. The photoreceptors have a well-formed outer segment, with orderly stacked disks. Electron microscopy indicates that the disks, like those in cones, are continuous with the plasma membrane.

One very unusual feature of the parietal-eye photoreceptor is that each cell expresses two pigments: the blue-sensitive pinopsin (first found in the light-sensitive chicken pineal gland) and the green-sensitive parietopsin, an apparently ancient pigment not found in the lateral eyes. The coexistence of two pigments in a single cell fits with the physiology, which involves two antagonistic phototransduction pathways in the same cell. One of these, best activated by blue light, is identical to that in rods and cones, consisting of cGMP-PDE stimulation, decrease in cGMP concentration, closure of CNG channels, and membrane hyperpolarization. The other, best activated by green light, consists of inhibition of the same PDE, increase in cGMP concentration, opening of CNG channels, and membrane depolarization. Thus, it appears that pinopsin activates the hyperpolarizing pathway and parietopsin activates the depolarizing pathway. Interestingly, transducin is not present in these cells. Instead, gustducin appears to take its role, coupling to pinopsin. Although gustducin is not found in any other photoreceptor, it is considered to be a close transducin homolog, with a similar protein sequence and function. G o , on the other hand, appears to couple to parietopsin. G o is more different from transducin and gustducin, although still belonging to the same subfamily of G-proteins.

In vertebrates, the involvement of G o in phototransduction is unique to the parietal-eye photoreceptor. However, in invertebrates, there is precedent for its involvement in vision, notably in the scallop hyperpolarizing photoreceptor, which as mentioned at the beginning of this article, is also of the ciliary type. In this scallop photoreceptor, G o is coupled to SCOP2, an apparently ancient pigment, to activate a cGMP-signaling pathway analogous, though not identical, to that in rods and cones. Thus, all evidence suggests that a G o -mediated phototransduction pathway is ancient among ciliary photoreceptors. As such, the parietal-eye photoreceptor appears to retain features of rod and cone predecessors – a missing link between rods/cones and more primitive ciliary photoreceptors, so to speak. The notion is that a G o -mediated phototransduction pathway existed in ciliary photoreceptors long ago, before vertebrates evolved. In the course of evolution, however, a chromatically antagonistic, gustducin/transducin-mediated phototransduction pathway was added to the cells having the G o -mediated pathway for the purpose of analyzing spectral information. This chromatic antagonism is retained by the parietal-eye photoreceptor to the present day. In parallel during evolution, the lateral eyes made their appearance over time but retained only the more recent gustducin/transducin-mediated pathway, delegating the color opponency instead to downstream neurons – a good strategy because complex processing of color information is best provided by elaborate synaptic circuitry. As such, the chromatic opponency within a single parietal-eye photoreceptor represents a very primitive, simple form of color vision compared to, say, what goes on in the lateral-eye retina.

Incidentally, the parietal eye, like the two lateral eyes (and the pineal gland), develops as a protrusion of the diencephalon of the brain during embryogenesis, again pointing its homology to these other structures.