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Historical note: The vertebrate median eye
Vision Res. Vol. 14, pp. 137-140. Pergamon Press 1974. Printed in Great Britain.
HISTORICAL NOTE: THE VERTEBRATE MEDIAN EYE JACOB G. SIVAK School of Optometry, University of Waterloo, Waterloo, Ontario, Canada (Received 1 May 1973)
INTRODUCTION The pineal complex, an outgrowth of the roof of the diencephalon, is found in almost all species of vertebrates. It has been the object of intensive and persistent study by researchers for the past 100 yr. Reviewers of the subject (for example, Duke-Elder, 1958, Gladstone and Wakely, 1940) normally attribute the earliest explanation of its function to Rent Descartes who considered the pineal gland to be the location of the "rational soul" which directed a machine-like body. The function of the pineal complex has proven to be extremely resistant to explanation. In 1958 Stebbins and Eakin stated that the pineal organ has remained an organ of uncertain function despite extensive research. Kelly (1962) noted that while pineal organs have been meticulously studied, every effort to arrive at some final physiological characterization has resulted in frustration. One of the difficulties encountered by those attempting to get at the problem, is the high degree of variation encountered from class to class, from species to species, and even within the same species. Oksche (1965) in a survey of the morphology of the pineal complex remarked that from a phylogenetic aspect, few organs have undergone such a change in form and cytological differentiation as the pineal organ. The most recent review of the subject by Wurtman, Axelrod and Kelly (1968) refers, in its opening page, to the bizarre range of morphological diversity encountered within the almost universal presence of a pineal organ in vertebrates. After a brief comparative survey of the gross anatomy of pineal organs, these authors admit that even at gross levels of examination the pineal systems display a complexity and variability that taxes their ability to formulate an adequate evolutionary hypothesis. In view of the above, very little generalization has been possible. The necessity, therefore, of extensive and time consuming probing of individual species of animals has produced a large volume of literature which is poorly interrelated. For example, Kappers (1965) in a review of the innervation of the pineal organs in vertebrates, meets with difficulty in determining from the
literature whether a parietal (parapineal) nerve is present in lizards possessing a median eye. He remarks that, not seldom, findings of different authors do not agree on this point. On the subject of pineal innervation in general, Kappers further concludes that our present knowledge of the innervation of the pineal complex is far from complete. Since the present discussion is concerned primarily with the function of the median eye, a brief survey of the gross comparative anatomy of the pineal complex follows: Many of the early pineal investigations were probably prompted by the apparent ~'eyelike" anatomy of the median eye in some lower vertebrates. Careful and exhaustive descriptions, both anatomical and developmental, were produced by such as Dendy (1907) who documented the embryonic development of the median eye of the tuatara and the New Zealand lamprey. An early description of the median eyes of some North American lizards was provided by Ritter in 1890. Others, such as Beard (1888), Spencer (1887), yon Leydig (1890), Studnicka (1905) and Francotte (1887), published extensive descriptions of European and other species possessing median eyes. An anatomically well developed median eye (also variously described in the literature as the third eye, the parietal eye, the pineal eye and the parapineal eye) with a transparent covering (depigmented skin and/or scales), with a lens, a vitreous body and a pigmented retina, is found only in the lamprey (Petromyzon), tuatara and in several lizards. The ontogenetic development of the median eye appears to be consistent among the species possessing such an organ. In every case the median eye is formed as a dorsal vesicular outgrowth of the diencephalon, the distal portion of which develops into a lens, while the proximal end develops into a retina. Contrary to the case of the lateral eyes, the retinae are not inverted, i.e. the sensory cells of the retinae are closest to the lens. In addition, the afferent pathways are of the two rather than three, neuron order. In the lamprey two median eye organs are present; a dorsal pineal eye and below it and slightly posterior a less developed parapineal eye. The pineal eye consists
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Historical Note
essentially of a lens and a well differentiated retina. It is joined by nerve fibers to the posterior commissure. The parapineal eye is joined neuronally to the habenular commissure. This paired nature of the pineal complex in the lamprey and in fossil remains supports the supposition that the median eye was originally a paired structure in the ancient vertebrates (Walls, 19671. The median eye structure in fishes is generally less developed when present, and often is completely absent. A single median eye structure, related to the parapineal eye of the lamprey, is found in certain primitive fishes. In the more modern fishes there is less median eye development. In most cases the eye-like structure has disappeared and the remaining structure is related, in an evolutionary sense, to the pineal eye of the lamprey. This structure, known as the epiphysis, is situated below the skull. In amphibians, a median eye structure is also less evident. In the tailed amphibians no eye structure exists, although an epiphysis (pineal body) is present. In anurans, or tailless amphibians, a rudimentary form of median eye does occur. The frontal organ of the frog is an example. This structure (parapineal) develops in the young and degenerates when the adult stage is reached. Ventral to the skull, a pineal body (epiphysis) exists as well. In this case, neural connections from the frontal organ join the roof of the epiphysis and together with fibers from that structure travel to the posterior commissure and subcommissure area. It is in certain species of reptiles that the median eye has reached its highest level of development. The tuatara (Sphenodon punctatum), a reptile indigenous to New Zealand, has attracted much attention both because of an evidently well developed median eye and because the tuatara is.the sole living member of the reptilian order, Rhynchocephalia. Furthermore, certain species of lizards, such as the green iguana (Iguana iguana) possess median eyes at a similar level of development (Fig. l). The reptilian median eye has been related to the parapineal (or parietal) eye of the lamprey. As in the frog, it is located above the skull, while the epiphysis Qr pineal body remains ventral to it. This organization is in contrast to the case of the lamprey where the pineal structure is the more eyelike organ and is situated above the parapineal structure. However, the sensory pathway of the pineal system is similar to that of the lamprey. At the superior end of the vertebrate subphylum, the birds and mammals, no median eye structure exists. However, the epiphysis (now called the pineal gland) exists. With evolution, the epiphysis became modified from a saccular structure to one of a solid parenchymatous character. Wurtman et al. (1968) in "The Pineal" present comprehensive reviews of recent work concerning the anatomy of the pineal gland or epiphysis, its biochemistry, pharmacology and physiology, and the effect of light in relation to biological rhythms.
STUDIES OF MEDIAN EYE FUNCTION
Early statements concerning the function of the median eye consisted primarily of speculation based on the apparent anatomical resemblance or non-resemblance of these eyes to the lateral eyes of vertebrates. Naturally, most of the evidence cited concerned the median eye of the lamprey, the tuatara, or one of the several species of lizards in which such an eye is evident. The early investigators were primarily concerned with the importance and position of the median eye in the evolutionary cycle. Thus attention was primarily focused on the question of the paired nature of median eyes in ancestral vertebrates with the intention of determining primitive vertebrate lines of evolution. In certain cases this search led to comparisons with the median eyes of invertebrates (Walls, 1942). Spencer (1887) reported having obtained no response when he focused an intense beam of light on the median eye of lizards when the lateral eyes were closed. Francotte (1887) devised an experiment to test the photoreceptive function of the median eye. He arranged six boxes in a hexagonal circle. A small opening 'was cut at the end of each box which opened into the central space and an incandescent lamp was placed in one of the boxes. A lizard, whose lateral eyes were cauterized, was placed in the central space. Francotte reported that in eight out of 10 cases the lizard ended up in the lighted box. Francotte admitted that the lizard may have been attracted by the warmth of the light. He considered the experiment inconclusive but thought that it at least permitted speculation regarding a photoreceptive ability. Dendy (1907) and Studnicka (1905) considered the median eye of the lamprey to be a functional photoreceptive organ. Dendy, in his report on the development of the median eyes of the New Zealand lamprey, noted that the pineal eye (the more developed of the two median eyes) contained the essential structural elements that one is accustomed to associate with a light perceiving organ. In common with Studnicka he found it impossible to believe that it was not functional. It exhibited, in his opinion, no sign of degeneration. Sensory cells, pigment cells, and ganglion cells are all present in a high degree of perfection and the retina is connected to the brain with a well developed nerve. However, neither of the authors considered this organ adequate for image formation. Dendy referred to the lamprey's use of the median eye as a detector of changes in light intensity from above. In a later paper (1911) Dendy noted that a high intensity light focused on the median eye of the tuatara produced no obvious response. In 1910 Nowicoff(see Gladstone and Wakely, 1940) studied the influence of light on the retinal pigment epithelium of the median eye of two species of lizards. He found that exposure to fight caused distal pigment accumulation (toward the source), the process being reversed in the dark. Similar pigment movements are
Historical Note known to occur in the lateral eyes of the lower classes of vertebrates. The disordered distribution of the median eye along a phylogenetic scale (while present in lamprey and some reptiles, it is rudimentary or absent in fish and amphibia), the conflicting reports by investigators (such as the presence, or not, of nerve tracts from the median eye to the brain), and the neuroendocrine nature of the pineal gland in higher vertebrates, often led to the conclusion that the median eye was vestigial (non-functional) or that its function was secretory. With regard to the latter, Kelly (1962) cites the example of an early study by Holmgram who ascribed the high degree of variability in the configuration of the median eye sensory cells to different stages of a regeneration cycle. Subsequent workers, according to Kelly, have misinterpreted this observation to indicate a secretory function for the median eye. Young (1935) demonstrated that illumination of the dorsal region of the head of lamprey produced movements of the animal. However, when the pineal complex (pineal and parapineal) was surgically removed this response persisted. Young further demonstrated that removal of the pineal complex of lamprey disturbs the rhythm of dermal colour changes which occur when the animal passes through alternate light and dark phases. Since the pituitary had been shown to cause the response of darkening, and since pineal removal resulted in a constant dark response, Young suggested that the paling response of the lamprey was due to the inhibition of the pituitary through the influence of the pineal complex. The major flaw in the latter part of Young's study is that surgical removal of the pineal complex is never perfect, a fact that he himself admits, and one that has contaminated many studies where pinealectomy was employed to examine the pineal gland of mammals. For example, Young relates that in every case of pineal removal, the third ventricle was ruptured causing a loss of cerebro-spinal fluid. In 1939, Clausen and Mofshin conducted a unique study in an attempt to prove that the median eye is a photoreceptor. Using a North American species of lizard (Anolis carolinensis) they demonstrated a significant difference in oxygen consumption in dark vs light conditions, with oxygen consumption as much as 30 per cent greater in the light. They showed that this difference could be broken down and attributed to three types of photoreceptors: the lateral eyes, the median eye, and dermal receptors. Their experiment involved the sequential occlusion of the dermal receptor and the surgical removal of either the lateral or median eyes. Walls (1942) restricts the function of the lamprey median eye to the recording of light intensity and, perhaps, the direction of light. When referring to the reptilian median eye, Walls suggests that the evolution of the median eye from a paired structure (as in fossil forms and from the double nature of the lamprey median eye) to a single structure in some reptiles, was due to the gradual perfectioning of the optical quality of this eye. When optical imagery was attained, fusion
139
of the two images of the paired structure was impossible owing to the lack of any accessory musculature, and thus a single median eye evolved. From this historical review, it is evident that the basic function of the median eye continued to be very much in doubt well into the 20th century. As late as 1947 Gasson, in a report on the median eye of the tuatara, regarded the ability of this eye to distinguish between light and dark as a matter of pure conjecture. Mygind (1948) assigned a position regulating function to the median eyes, a function related to the corrective movement of a lateral eye when light does not fall on the fovea (or area centralis, if no fovea exists), and to the gravitational motor reactions of the labyrinth organ. This hypothesis was based on a study of the anatomy of the median eye of the lamprey, which Mygind felt ruled out any possibility of an optical system capable of imagery. Furthermore, Mygind indicates the usefulness of a supplementary positioning organ to a neck-less animal living in a murky aquatic environment. Unfortunately for the latter suggestion, the median eye is less developed and often absent in the fishes and amphibians but becomes more evident, and apparently better developed, in many reptiles. In a study by Stebbins and Eakin (1958) the median eye of the western fence lizard (Sceloporus occidentalis) was destroyed. Later in the study aluminium foil shields were employed to cover the median eye. The results indicate that removal or shielding of the median eye leads to an increase in locomotory activity due to the increased time of exposure to sun or artificial light. In a similar experiment, Glaser (1958) used a spring balance actograph to record movements of lizards (Xanthusia vigilis). Glaser's data agree with those of Stebbins and Eakin. An increase in locomotory activity followed shielding of the median eye. Since lizards are poikilotherms the increase in activity is related to increase in time spent at higher temperature. Stebbins and Eakin concluded that the median eye seems to function as an activity inhibitor, of an endocrine nature, that regulates exposure to sunlight. That conclusion, especially the postulate of the existence of a hormone, was heavily influenced by the fact that Stebbins and Eakin were unable to identify a median eye nerve tract. However, in a subsequent report (1959) the same authors did note the existence of such a nerve tract in the western fence lizard. In the late 1950's and the early 1960's histological and electrophysiological studies finally brought a close to the era of speculation concerning the function of the median eye. Studies by Eakin and Westfall (1959), and Steyn (1960), produced electron-microscopic evidence confirming the close similarity of the sensory cells of lizard median eyes to those of lateral eye retinae. Setyn reported the predominance of cone-like cells. They are described as consisting of an inner and outer segment; the inner segments containing dense particles, mitochondria and oil droplets, while the outer segments largely contain laminated layers or stacks of cell membranes. As in the case of the rods and cones, the outer
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segments are modified cilia. However, the median eye receptor cells are never arranged with the same anterior posterior regularity seen in the lateral eye retinae. Further examination (Oskche, 1965) has demonstrated similar photoreceptor-like ceils in the amphibians and lamprey. Miller and Wolbarsht (1962) recorded the electrical activity in response to illumination from the median eye of anolis. The response consisted of a negative graded potential maintained for the duration of the stimulus, and action potentials that were of greater frequency at onset and cessation of the stimulus. D o d t and Heerd (1962) recorded from the nerve of the frog median eye (frontal organ) and found that the response varied with wavelength. Subsequent reports (Dodt and Scherer 1967, 1968; Hamasaki 1968, 1969) have indicated that the lacertilian median eye is wavelength specific and may consist of separate photopic and scotopic systems. While the morphological and electrophysiological studies cited above provide evidence for the photoreceptive nature of the median eye, very little consideration has been given to the optical capabilities of this organ. A study of transmittance and curvature of the interparietal scale, one of the two optical elements of the median eye, indicates that the possibility of optical imagery exists (Sivak, 1973).
Acknowledgements--The author wishes to acknowledge the assistance of Drs. J. R. Levene and J. D. Moreland.
REFERENCES
Beard J. (1888) The parietal eye of cylostome fishes. Q. Jl. microsc. 9ci. 29, 55-73. Clausen H. J. and Motshin B. ~193~)the pineal eye of the lizard (Anolis carolinensis), a photoreceptor as revealed by oxygen consumption studies. J. cell. comp. Physiol. 14, 29-41. Dendy A. (1907) On the parietal sense organs and associated structure in the New Zealand lamprey. Q. Jl. microsc. Sci. 51, 1-29. Dendy A. (1911) On the structure, development and morphological interpretation of the pineal and adjacent parts of the brain in the tuatara (Sphenodon punctatum). Phil. Trans. R. Soc. B. 201,227-331. Dodt E. and Heerd E. (1962) Mode of action of pineal nerve fibers in frogs. J. Neurophysiol. 25, 405-429. Dodt E. and Scherer E. (1967) The electroretinogram of the third eye. II. Symposium of the Internat. Soc. Clin. Electroretinooraphy (JSCERG), held in Efurt. 299-310.
Dodt E. and Scherer E. (1968) Photic responses from the parietal eye of the lizard (Lacerta sicule campestris). Vision Res. 8, 61-72. Duke-Elder S. (1958) System of Ophthalmology, Vol. I, The Eye in Evolution, C. V. Mosby C0., St., Louis. Eakin R. M. and Stebbins R. C. (1959) Parietal eye nerve in the fence lizard. Science., N.Y 130, 1573-1574. Eakin R. M. and Westfall J. A. (1959) Fine structure of the retina in the reptilian third eye. J. biophys, biochem. Cytol. 6, 133-134. Francotte P. (1887) Contribution ~.l'ttude du developpement de l'epiphyse et du troisi~me oeil chez les reptiles. Acad. R. Belg., Ser. 3 14, 810-840. Gasson W. {1947) The normal and parietal eyes of the tuatara. Optician. 37, 261-265. Gladstone R. J. and Wakely C. P. G. (1940) The Pineal Organ, Williams and Wilkins Co., London. Glaser R. J. (1958) Increase in locomotor activity following shielding of the parietal eye in night lizards. Science., N.Y. 128, 1577-1578. Hamasaki D. I. (1968) Properties of the parietal eye of the green iguana. Vision Res. 9, 515 523. Hamasaki D. I. (1969) Spectral sensitivity of the parietal eye of the green iguana. 14sion Res. 10, 87-154. Kappers J. A. (1965) Survey of the innervation of the epiphysis cerebri and the accessory pineal organs of vertebrates. Prog. Brain Res. 10, 87-154. Kelly D. E. (1962) Pineal organs: photoreception secretion, and development. Am. Scient. 50, 597-625. Leydig Fr. von. (1890) Das Parietalorgan. Biolog. Zbl. 9, 278-285. Miller W. H. and Walbarsht M. D. (1962) Neural activity in the parietal eye of a lizard. Science, N.Y 135, 316-317. Mygind S. H. (1949) The function of the parietal eye. Acta Psychiat. neurol, scand. 24, 607-627. Oksche A. (1965) Survey of the development and comparative morphology of the pineal organ. Proy. Brain Res. 10, 3-30. Ritter W. E. (1890) The parietal eye in some lizards from the western United States. Bull. Mus. comp. Zool. Harv. 20, 209-228. Sivak J. G. (1973) Optical properties of the interparietal scale of the green iguana (Iguana iguana). Herpetologica. 29, 254--256. Spencer W. B. (1886) The parietal eye of hattaria. Nature, Lond. 34, 33-35. Stebbins R. C. and Eakin R. M. (1958) The role of the third eye in reptilian behaviour. Am. Mus: Novit. 1870, 1-40. Steyn W. (1960) Observations on the ultrastructure of the pineal eye. J. R. Micr. Soc. 70, 47-58. Studnicka F. K. (1905) Die Parietalorgane. Lehr. der Vergl. Mikr., Jena. 5, 47-63. Walls G. L. (1967) The Vertebrate Eye and its Adaptive Radiation, Hafner Pubt. Co., New York. Wurtman R. J., Axelrod J. and Kelly D. E. (1968) The Pineal, Academic Press, New York. Young J. Z. (1935) The photoreceptors of lampreys. II. The functions of the pineal complex. J. exp. Biol. 12, 254-270.
HISTORICAL NOTE: THE VERTEBRATE MEDIAN EYE JACOB G. SIVAK School of Optometry, University of Waterloo, Waterloo, Ontario, Canada (Received 1 May 1973)
INTRODUCTION The pineal complex, an outgrowth of the roof of the diencephalon, is found in almost all species of vertebrates. It has been the object of intensive and persistent study by researchers for the past 100 yr. Reviewers of the subject (for example, Duke-Elder, 1958, Gladstone and Wakely, 1940) normally attribute the earliest explanation of its function to Rent Descartes who considered the pineal gland to be the location of the "rational soul" which directed a machine-like body. The function of the pineal complex has proven to be extremely resistant to explanation. In 1958 Stebbins and Eakin stated that the pineal organ has remained an organ of uncertain function despite extensive research. Kelly (1962) noted that while pineal organs have been meticulously studied, every effort to arrive at some final physiological characterization has resulted in frustration. One of the difficulties encountered by those attempting to get at the problem, is the high degree of variation encountered from class to class, from species to species, and even within the same species. Oksche (1965) in a survey of the morphology of the pineal complex remarked that from a phylogenetic aspect, few organs have undergone such a change in form and cytological differentiation as the pineal organ. The most recent review of the subject by Wurtman, Axelrod and Kelly (1968) refers, in its opening page, to the bizarre range of morphological diversity encountered within the almost universal presence of a pineal organ in vertebrates. After a brief comparative survey of the gross anatomy of pineal organs, these authors admit that even at gross levels of examination the pineal systems display a complexity and variability that taxes their ability to formulate an adequate evolutionary hypothesis. In view of the above, very little generalization has been possible. The necessity, therefore, of extensive and time consuming probing of individual species of animals has produced a large volume of literature which is poorly interrelated. For example, Kappers (1965) in a review of the innervation of the pineal organs in vertebrates, meets with difficulty in determining from the
literature whether a parietal (parapineal) nerve is present in lizards possessing a median eye. He remarks that, not seldom, findings of different authors do not agree on this point. On the subject of pineal innervation in general, Kappers further concludes that our present knowledge of the innervation of the pineal complex is far from complete. Since the present discussion is concerned primarily with the function of the median eye, a brief survey of the gross comparative anatomy of the pineal complex follows: Many of the early pineal investigations were probably prompted by the apparent ~'eyelike" anatomy of the median eye in some lower vertebrates. Careful and exhaustive descriptions, both anatomical and developmental, were produced by such as Dendy (1907) who documented the embryonic development of the median eye of the tuatara and the New Zealand lamprey. An early description of the median eyes of some North American lizards was provided by Ritter in 1890. Others, such as Beard (1888), Spencer (1887), yon Leydig (1890), Studnicka (1905) and Francotte (1887), published extensive descriptions of European and other species possessing median eyes. An anatomically well developed median eye (also variously described in the literature as the third eye, the parietal eye, the pineal eye and the parapineal eye) with a transparent covering (depigmented skin and/or scales), with a lens, a vitreous body and a pigmented retina, is found only in the lamprey (Petromyzon), tuatara and in several lizards. The ontogenetic development of the median eye appears to be consistent among the species possessing such an organ. In every case the median eye is formed as a dorsal vesicular outgrowth of the diencephalon, the distal portion of which develops into a lens, while the proximal end develops into a retina. Contrary to the case of the lateral eyes, the retinae are not inverted, i.e. the sensory cells of the retinae are closest to the lens. In addition, the afferent pathways are of the two rather than three, neuron order. In the lamprey two median eye organs are present; a dorsal pineal eye and below it and slightly posterior a less developed parapineal eye. The pineal eye consists
137
138
Historical Note
essentially of a lens and a well differentiated retina. It is joined by nerve fibers to the posterior commissure. The parapineal eye is joined neuronally to the habenular commissure. This paired nature of the pineal complex in the lamprey and in fossil remains supports the supposition that the median eye was originally a paired structure in the ancient vertebrates (Walls, 19671. The median eye structure in fishes is generally less developed when present, and often is completely absent. A single median eye structure, related to the parapineal eye of the lamprey, is found in certain primitive fishes. In the more modern fishes there is less median eye development. In most cases the eye-like structure has disappeared and the remaining structure is related, in an evolutionary sense, to the pineal eye of the lamprey. This structure, known as the epiphysis, is situated below the skull. In amphibians, a median eye structure is also less evident. In the tailed amphibians no eye structure exists, although an epiphysis (pineal body) is present. In anurans, or tailless amphibians, a rudimentary form of median eye does occur. The frontal organ of the frog is an example. This structure (parapineal) develops in the young and degenerates when the adult stage is reached. Ventral to the skull, a pineal body (epiphysis) exists as well. In this case, neural connections from the frontal organ join the roof of the epiphysis and together with fibers from that structure travel to the posterior commissure and subcommissure area. It is in certain species of reptiles that the median eye has reached its highest level of development. The tuatara (Sphenodon punctatum), a reptile indigenous to New Zealand, has attracted much attention both because of an evidently well developed median eye and because the tuatara is.the sole living member of the reptilian order, Rhynchocephalia. Furthermore, certain species of lizards, such as the green iguana (Iguana iguana) possess median eyes at a similar level of development (Fig. l). The reptilian median eye has been related to the parapineal (or parietal) eye of the lamprey. As in the frog, it is located above the skull, while the epiphysis Qr pineal body remains ventral to it. This organization is in contrast to the case of the lamprey where the pineal structure is the more eyelike organ and is situated above the parapineal structure. However, the sensory pathway of the pineal system is similar to that of the lamprey. At the superior end of the vertebrate subphylum, the birds and mammals, no median eye structure exists. However, the epiphysis (now called the pineal gland) exists. With evolution, the epiphysis became modified from a saccular structure to one of a solid parenchymatous character. Wurtman et al. (1968) in "The Pineal" present comprehensive reviews of recent work concerning the anatomy of the pineal gland or epiphysis, its biochemistry, pharmacology and physiology, and the effect of light in relation to biological rhythms.
STUDIES OF MEDIAN EYE FUNCTION
Early statements concerning the function of the median eye consisted primarily of speculation based on the apparent anatomical resemblance or non-resemblance of these eyes to the lateral eyes of vertebrates. Naturally, most of the evidence cited concerned the median eye of the lamprey, the tuatara, or one of the several species of lizards in which such an eye is evident. The early investigators were primarily concerned with the importance and position of the median eye in the evolutionary cycle. Thus attention was primarily focused on the question of the paired nature of median eyes in ancestral vertebrates with the intention of determining primitive vertebrate lines of evolution. In certain cases this search led to comparisons with the median eyes of invertebrates (Walls, 1942). Spencer (1887) reported having obtained no response when he focused an intense beam of light on the median eye of lizards when the lateral eyes were closed. Francotte (1887) devised an experiment to test the photoreceptive function of the median eye. He arranged six boxes in a hexagonal circle. A small opening 'was cut at the end of each box which opened into the central space and an incandescent lamp was placed in one of the boxes. A lizard, whose lateral eyes were cauterized, was placed in the central space. Francotte reported that in eight out of 10 cases the lizard ended up in the lighted box. Francotte admitted that the lizard may have been attracted by the warmth of the light. He considered the experiment inconclusive but thought that it at least permitted speculation regarding a photoreceptive ability. Dendy (1907) and Studnicka (1905) considered the median eye of the lamprey to be a functional photoreceptive organ. Dendy, in his report on the development of the median eyes of the New Zealand lamprey, noted that the pineal eye (the more developed of the two median eyes) contained the essential structural elements that one is accustomed to associate with a light perceiving organ. In common with Studnicka he found it impossible to believe that it was not functional. It exhibited, in his opinion, no sign of degeneration. Sensory cells, pigment cells, and ganglion cells are all present in a high degree of perfection and the retina is connected to the brain with a well developed nerve. However, neither of the authors considered this organ adequate for image formation. Dendy referred to the lamprey's use of the median eye as a detector of changes in light intensity from above. In a later paper (1911) Dendy noted that a high intensity light focused on the median eye of the tuatara produced no obvious response. In 1910 Nowicoff(see Gladstone and Wakely, 1940) studied the influence of light on the retinal pigment epithelium of the median eye of two species of lizards. He found that exposure to fight caused distal pigment accumulation (toward the source), the process being reversed in the dark. Similar pigment movements are
Historical Note known to occur in the lateral eyes of the lower classes of vertebrates. The disordered distribution of the median eye along a phylogenetic scale (while present in lamprey and some reptiles, it is rudimentary or absent in fish and amphibia), the conflicting reports by investigators (such as the presence, or not, of nerve tracts from the median eye to the brain), and the neuroendocrine nature of the pineal gland in higher vertebrates, often led to the conclusion that the median eye was vestigial (non-functional) or that its function was secretory. With regard to the latter, Kelly (1962) cites the example of an early study by Holmgram who ascribed the high degree of variability in the configuration of the median eye sensory cells to different stages of a regeneration cycle. Subsequent workers, according to Kelly, have misinterpreted this observation to indicate a secretory function for the median eye. Young (1935) demonstrated that illumination of the dorsal region of the head of lamprey produced movements of the animal. However, when the pineal complex (pineal and parapineal) was surgically removed this response persisted. Young further demonstrated that removal of the pineal complex of lamprey disturbs the rhythm of dermal colour changes which occur when the animal passes through alternate light and dark phases. Since the pituitary had been shown to cause the response of darkening, and since pineal removal resulted in a constant dark response, Young suggested that the paling response of the lamprey was due to the inhibition of the pituitary through the influence of the pineal complex. The major flaw in the latter part of Young's study is that surgical removal of the pineal complex is never perfect, a fact that he himself admits, and one that has contaminated many studies where pinealectomy was employed to examine the pineal gland of mammals. For example, Young relates that in every case of pineal removal, the third ventricle was ruptured causing a loss of cerebro-spinal fluid. In 1939, Clausen and Mofshin conducted a unique study in an attempt to prove that the median eye is a photoreceptor. Using a North American species of lizard (Anolis carolinensis) they demonstrated a significant difference in oxygen consumption in dark vs light conditions, with oxygen consumption as much as 30 per cent greater in the light. They showed that this difference could be broken down and attributed to three types of photoreceptors: the lateral eyes, the median eye, and dermal receptors. Their experiment involved the sequential occlusion of the dermal receptor and the surgical removal of either the lateral or median eyes. Walls (1942) restricts the function of the lamprey median eye to the recording of light intensity and, perhaps, the direction of light. When referring to the reptilian median eye, Walls suggests that the evolution of the median eye from a paired structure (as in fossil forms and from the double nature of the lamprey median eye) to a single structure in some reptiles, was due to the gradual perfectioning of the optical quality of this eye. When optical imagery was attained, fusion
139
of the two images of the paired structure was impossible owing to the lack of any accessory musculature, and thus a single median eye evolved. From this historical review, it is evident that the basic function of the median eye continued to be very much in doubt well into the 20th century. As late as 1947 Gasson, in a report on the median eye of the tuatara, regarded the ability of this eye to distinguish between light and dark as a matter of pure conjecture. Mygind (1948) assigned a position regulating function to the median eyes, a function related to the corrective movement of a lateral eye when light does not fall on the fovea (or area centralis, if no fovea exists), and to the gravitational motor reactions of the labyrinth organ. This hypothesis was based on a study of the anatomy of the median eye of the lamprey, which Mygind felt ruled out any possibility of an optical system capable of imagery. Furthermore, Mygind indicates the usefulness of a supplementary positioning organ to a neck-less animal living in a murky aquatic environment. Unfortunately for the latter suggestion, the median eye is less developed and often absent in the fishes and amphibians but becomes more evident, and apparently better developed, in many reptiles. In a study by Stebbins and Eakin (1958) the median eye of the western fence lizard (Sceloporus occidentalis) was destroyed. Later in the study aluminium foil shields were employed to cover the median eye. The results indicate that removal or shielding of the median eye leads to an increase in locomotory activity due to the increased time of exposure to sun or artificial light. In a similar experiment, Glaser (1958) used a spring balance actograph to record movements of lizards (Xanthusia vigilis). Glaser's data agree with those of Stebbins and Eakin. An increase in locomotory activity followed shielding of the median eye. Since lizards are poikilotherms the increase in activity is related to increase in time spent at higher temperature. Stebbins and Eakin concluded that the median eye seems to function as an activity inhibitor, of an endocrine nature, that regulates exposure to sunlight. That conclusion, especially the postulate of the existence of a hormone, was heavily influenced by the fact that Stebbins and Eakin were unable to identify a median eye nerve tract. However, in a subsequent report (1959) the same authors did note the existence of such a nerve tract in the western fence lizard. In the late 1950's and the early 1960's histological and electrophysiological studies finally brought a close to the era of speculation concerning the function of the median eye. Studies by Eakin and Westfall (1959), and Steyn (1960), produced electron-microscopic evidence confirming the close similarity of the sensory cells of lizard median eyes to those of lateral eye retinae. Setyn reported the predominance of cone-like cells. They are described as consisting of an inner and outer segment; the inner segments containing dense particles, mitochondria and oil droplets, while the outer segments largely contain laminated layers or stacks of cell membranes. As in the case of the rods and cones, the outer
140
Historical Note
segments are modified cilia. However, the median eye receptor cells are never arranged with the same anterior posterior regularity seen in the lateral eye retinae. Further examination (Oskche, 1965) has demonstrated similar photoreceptor-like ceils in the amphibians and lamprey. Miller and Wolbarsht (1962) recorded the electrical activity in response to illumination from the median eye of anolis. The response consisted of a negative graded potential maintained for the duration of the stimulus, and action potentials that were of greater frequency at onset and cessation of the stimulus. D o d t and Heerd (1962) recorded from the nerve of the frog median eye (frontal organ) and found that the response varied with wavelength. Subsequent reports (Dodt and Scherer 1967, 1968; Hamasaki 1968, 1969) have indicated that the lacertilian median eye is wavelength specific and may consist of separate photopic and scotopic systems. While the morphological and electrophysiological studies cited above provide evidence for the photoreceptive nature of the median eye, very little consideration has been given to the optical capabilities of this organ. A study of transmittance and curvature of the interparietal scale, one of the two optical elements of the median eye, indicates that the possibility of optical imagery exists (Sivak, 1973).
Acknowledgements--The author wishes to acknowledge the assistance of Drs. J. R. Levene and J. D. Moreland.
REFERENCES
Beard J. (1888) The parietal eye of cylostome fishes. Q. Jl. microsc. 9ci. 29, 55-73. Clausen H. J. and Motshin B. ~193~)the pineal eye of the lizard (Anolis carolinensis), a photoreceptor as revealed by oxygen consumption studies. J. cell. comp. Physiol. 14, 29-41. Dendy A. (1907) On the parietal sense organs and associated structure in the New Zealand lamprey. Q. Jl. microsc. Sci. 51, 1-29. Dendy A. (1911) On the structure, development and morphological interpretation of the pineal and adjacent parts of the brain in the tuatara (Sphenodon punctatum). Phil. Trans. R. Soc. B. 201,227-331. Dodt E. and Heerd E. (1962) Mode of action of pineal nerve fibers in frogs. J. Neurophysiol. 25, 405-429. Dodt E. and Scherer E. (1967) The electroretinogram of the third eye. II. Symposium of the Internat. Soc. Clin. Electroretinooraphy (JSCERG), held in Efurt. 299-310.
Dodt E. and Scherer E. (1968) Photic responses from the parietal eye of the lizard (Lacerta sicule campestris). Vision Res. 8, 61-72. Duke-Elder S. (1958) System of Ophthalmology, Vol. I, The Eye in Evolution, C. V. Mosby C0., St., Louis. Eakin R. M. and Stebbins R. C. (1959) Parietal eye nerve in the fence lizard. Science., N.Y 130, 1573-1574. Eakin R. M. and Westfall J. A. (1959) Fine structure of the retina in the reptilian third eye. J. biophys, biochem. Cytol. 6, 133-134. Francotte P. (1887) Contribution ~.l'ttude du developpement de l'epiphyse et du troisi~me oeil chez les reptiles. Acad. R. Belg., Ser. 3 14, 810-840. Gasson W. {1947) The normal and parietal eyes of the tuatara. Optician. 37, 261-265. Gladstone R. J. and Wakely C. P. G. (1940) The Pineal Organ, Williams and Wilkins Co., London. Glaser R. J. (1958) Increase in locomotor activity following shielding of the parietal eye in night lizards. Science., N.Y. 128, 1577-1578. Hamasaki D. I. (1968) Properties of the parietal eye of the green iguana. Vision Res. 9, 515 523. Hamasaki D. I. (1969) Spectral sensitivity of the parietal eye of the green iguana. 14sion Res. 10, 87-154. Kappers J. A. (1965) Survey of the innervation of the epiphysis cerebri and the accessory pineal organs of vertebrates. Prog. Brain Res. 10, 87-154. Kelly D. E. (1962) Pineal organs: photoreception secretion, and development. Am. Scient. 50, 597-625. Leydig Fr. von. (1890) Das Parietalorgan. Biolog. Zbl. 9, 278-285. Miller W. H. and Walbarsht M. D. (1962) Neural activity in the parietal eye of a lizard. Science, N.Y 135, 316-317. Mygind S. H. (1949) The function of the parietal eye. Acta Psychiat. neurol, scand. 24, 607-627. Oksche A. (1965) Survey of the development and comparative morphology of the pineal organ. Proy. Brain Res. 10, 3-30. Ritter W. E. (1890) The parietal eye in some lizards from the western United States. Bull. Mus. comp. Zool. Harv. 20, 209-228. Sivak J. G. (1973) Optical properties of the interparietal scale of the green iguana (Iguana iguana). Herpetologica. 29, 254--256. Spencer W. B. (1886) The parietal eye of hattaria. Nature, Lond. 34, 33-35. Stebbins R. C. and Eakin R. M. (1958) The role of the third eye in reptilian behaviour. Am. Mus: Novit. 1870, 1-40. Steyn W. (1960) Observations on the ultrastructure of the pineal eye. J. R. Micr. Soc. 70, 47-58. Studnicka F. K. (1905) Die Parietalorgane. Lehr. der Vergl. Mikr., Jena. 5, 47-63. Walls G. L. (1967) The Vertebrate Eye and its Adaptive Radiation, Hafner Pubt. Co., New York. Wurtman R. J., Axelrod J. and Kelly D. E. (1968) The Pineal, Academic Press, New York. Young J. Z. (1935) The photoreceptors of lampreys. II. The functions of the pineal complex. J. exp. Biol. 12, 254-270.