256 Br J Ophthalmol 2005;89:256 Br J Ophthalmol: first published as 10.1136/bjo.2004.059105 on 17 February 2005. Downloaded from

Cover illustration...... The lonely eye

lthough the dinosaurs are gone, the organ to be a solar dosimeter useful extant vertebrates provide clues to for photoperiod recognition for circa- Athe development of photorecep- dian and seasonal rhythms, but there tion among the clades that probably may be more to this murky organ than preceded and then radiated into the first meets the eye. The parietal eye in dinosaurs. The ancient order Rhyncho- reptiles, including Sphendon, is not lat- cephalia, which includes Sphenodon as its erally symmetrical which, in and of only family, with two surviving species, itself, is unusual in the world of bilateral had its heyday between 200 million and symmetrical organisms such as verte- 100 million years ago. While this order brates. Development of the reptilian is reptilian, these creatures were not third eye is actually believed to be as a lizards, but their own order. pair of diencephalic evaginations with Approximately 100 million years ago Figure 1 Developing eye of Sphenodon. Note the more rostral and left sided portion as other members of Rhynchocephalia early lens formation and retinal pigment becoming the parietal eye and the more were succumbing to extinction, epithelium in front of photoreceptors as described in text. caudal and right sided portion becoming Gondwanaland was breaking apart and the pineal sac. In animals that have lost New Zealand and its islands were in the figure above (Ung CY-J, Molteno the parietal eye, including mammals, breaking free from Australia, thereby ACB, An enigmatic eye: the histology of the pineal sac is retained and condensed isolating this last member of the tuatara pineal complex. Clin Exp into the form of the pineal gland. In Rhynochocephalia, Sphenodon, presumably Ophthalmol 2004;32:614–18). The retina reptiles, the pineal synthesises melato- without competition. The tuatara sur- is upside down with the retinal pigment nin and probably other hormones. In vives virtually unchanged, as a fossil humans, the pineal synthesises melato- relict and provides us with a glimpse of epithelium interposed between any incoming light and the photoreceptors! nin and many other neuroendocrine vertebrate evolution from perhaps as regulatory compounds. Melatonin influ- long as 200 million years ago. Sphenodon, and other reptiles, have everted photoreceptors with outer seg- ences vertebrate thermoregulation and, In the early Jurassic (approximately importantly, the circadian rhythm by 200 million years ago) tetrapods were ments containing stacks of discs very similar to those of the lateral eyes acting as a somnifacient. radiating into lizards, turtles, crocodiles, The third eye did not spring de novo dinosaurs, and eventually birds and (Eakin RM, The Third Eye. UC Press, in the early reptiles or even the early mammals. Sphenodon was in an order 1973). tetrapods as there is a homologous of early reptiles and provides us with a Why should the photoreceptors be everted in the third eye but not in the photosensitive organ in frogs, and even

window into those beginnings. http://bjo.bmj.com/ some fishes suggesting that this central The tuatara has a third eye, as do lateral eyes? As explained by Eakin in dorsal third eye is much older than some other reptiles. But this adaptation The Third Eye, it all relates to embryol- reptiles and probably belongs to our has been lost in the radiation into later ogy. In vertebrates, all eyes begin as watery beginnings as chordates. The orders such as crocodiles, birds, and evaginations of the diencephalon to lamprey, a cyclostome, is a primitive mammals, although remnants of this create optic vesicles, and the lateral eyes organ can be found in most of these. The proceed to invaginate forming optic fish that has the asymmetrical pineal third eye, then, represents evolution’s cups. But the third eye never invagi- complex mentioned above suggesting earlier approach to photoreception. nates and is lined with the ciliated that the structure is probably older on September 25, 2021 by guest. Protected copyright. In the tuatara, as in the other reptiles epithelium that becomes the photo- than the Devonian period leading with the organ, the third eye is a dorsal receptors with the ciliated portion of perhaps as far back as the protochor- midline structure just ventral to a the cells extending inward towards the dates. But, since the pineal complex parietal plug which is homologous to, centre of the vesicle or cyst. The most seems to be in decline even among and resembles, a cornea. Immediately distal (and most dorsal) portion of the the reptiles and in subsequent radia- ventral to the parietal plug is a lens that evagination of the third eye condenses tions, it may be going the way of the is surprising similar, at least on a to become a lens leaving the cyst lined appendix and, hence, is a very lonely eye histological basis, to those of the lateral with everted cells. The portion of the indeed. eyes. The vitreous cavity analogue is developing third eye that condenses into ventral to the lens and dorsal to a a lens, then, is homologous to a portion I R Schwab pigment epithelial layer. Ventral to the of the retina in the lateral eye. University of California, Davis, Sacramento, pigment epithelial cells are the primitive Furthermore, the ciliated cells that line CA, USA; [email protected] ciliated photoreceptors which are this cyst in the third eye differentiate G R O’Connor everted (our photoreceptors are inverted into pigment epithelium and everted Professor Emeritus of Ophthalmology, with the photopigment on the distal end photoreceptors. It is as if some stimulus University of California, San Francisco, CA, USA of the retinal cells). Ganglion cell layers is missing, and a complete ‘‘normal’’ are distal to the photoreceptors, much vertebrate eye never forms. Cover photograph of ‘‘Henry’’ from South- more like the retina of an octopus rather If the development of the third eye land Museum New Zealand and photograph than that of a vertebrate (see essay BJO seems mysterious, the function is even on this page by Casey Y-J Ung, MD, MBBS July 2003). These structures can be seen more obscure. Most observers believe (Qld).

www.bjophthalmol.com