Paper - A phylogenetic consideration of the optic tectum

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Huber GC. and Crosby EC. A phylogenetic consideration of the optic tectum. (1933) Proc Natl Acad Sci U S A. 19(1): 15-22. PMID 16587730

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A Phylogenetic Consideration Of The Optic Tectum

By G. Cart Huber and Elizabeth C. Crosby

Laboratory Of Comparative Neurology, Department Of Anatomy, University Of Michigan

Read before the Academy, Tuesday, November 15, 1932

It is not unusual in the consideration of the optic tectum to regard it as dominated on the afferent side by the optic tract. It cannot be denied that there exists a direct relation between the size of the eye and the development of certain layers of the optic tectum, but it is equally true that the tectum is a sensory correlation center and to a very considerable degree its size, and more particularly its lamination, evidences the relative variety and complexity of. the non-optic afferent impulses reaching it from the brain stem and diencephalic region. But its function as a sensory correlation center is only one phase of its activity, since afferent impulses correlated through the interrelation of its neurons, are affected through efferent paths arising from certain of its neurons so that it becomes not only an important afferent correlation center but also an equally important efferent center, containing the upper neuron of the final common path.

On casual examination of the optic tectum of different vertebrate orders there would appear to be a wide variety of patterns, the apparent number of layers varying from two or three in certain urodele amphibians to approximately fifteen in reptiles and birds. In an endeavor to elucidate the structure of the optic tectum, one method of approach, adopted and developed particularly by the Spanish school, was to designate by number, numerically arranged from within out, cell and fiber layers. The application of this system of numbering to the tecta of different orders of vertebrates led to the use of the same numbers to designate widely divergent functional fields.. According to the above indicated system of numbering there were described in the optic tectum of reptiles fourteen distinct layers. In recent studies, Huber and Crosby, with use of abundant reptilian material, containing series cut in several critical planes and prepared to reveal cell structure and arrangement, medullated and nonmedullated nerve fibers, were able to group these various layers into six strata, on the basis not only of morphology but of morphology and function, and they regard these six strata as presenting a fundamental pattern, present potentially or with full expression or again with slight regression in all vertebrate tecta. These strata we have named:

1. Stratum opticum.
2. Stratum fibrosum et griseum superficiale. 3. Stratum griseum centrale.
3. Stratum album centrale.
4. Stratum griseum periventriculare.
5. Stratum fibrosum periventriculare.

Following a functional pattern these layers are enumerated from the periphery toward the ventricle, contrary to the older numerical designation which was from the ventricle outward.

The stratum opticum, as its name implies, is composed of the main bundles of the optic tract fibers which enter the optic tectum along almost its entire ventral circumference and pass dorsalward. Certain of these optic fibers synapse with the dendrites of tectal cells close to the stratum of optic fibers, while others penetrate to various levels of the underlying stratum and there come into synaptic relation with the dendrites of cell bodies situated in all of the deeper cell layers. The stratum fibrosum et griseum superficiale, as its name implies, consists essentially of alternate fibrous and cellular layers of which the former represent in part regions of synapse and in part pathways of afferent fibers, while the cellular layers are composed of neurons receptive to incoming impulses. The incoming impulses, other than the optic, are tactile, pain and temperature impulses from the spinal cord by way of spino-tectal paths, tactile, pain and temperature impulses from the head by way of trigemino-tectal paths from the cutaneous centers of the medulla oblongata, and auditory impulses from the cochlear centers of the bulb in part at least by way of the nucleus isthmi. These receive important additions from impulses carried by certain commissural systems and by fiber bundles from the diencephalon particularly the dorsal thalamus, and from the pretectal and subtectal centers. These connections indicate that the stratum fibrosum et griseum superficiale is a main receptive area of the optic tectum and that within its confines occurs a correlation of optic and non-optic exteroceptive impulses, in which correlation, however, neurons of deeper strata participate. The degree of layer differentiation in the stratum fibrosum et griseum superficiale correlates directly with the volume and the relative importance of the non-optic impulses in the various vertebrate orders. Within the stratum griseum centrale lie the cell bodies of neurons, the neuraxes of which constitute efferent paths. Such neurons send their major dendrites toward the periphery of the tectum, where they come in part into direct synaptic relation with incoming optic and non-optic fibers, and in part receive impulses after these have been subjected to recombinations inthe stratum fibrosum et griseum superficiale. Certain secondary ascending fibers appear to terminate directly within this stratum. The neuraxes of the neurons of the stratum griseum centrale, with certain exceptions, reach the stratum album centrale, composed of the major efferent pathways from the tectum to lower centers Collaterals turn into the stratum fibrosum et griseum superficiale for reinforcement, as do neuraxes of other neurons of the stratum. Internal to this stratum is found another cellular layer, the stratum griseum periventriculare, which varies greatly in thickness and layer differentiation in the various reptiles, and presents still wider variation in the different vertebrate orders. This stratum consists of neurons possessing long dendrites which extend toward the periphery and shorter dendrites which are directed toward the ventricle. The longer dendrites form synaptic relations which are comparable to those of the stratum griseum centrale, while the shorter dendrites receive impulses from the periventricular system of fibers. This periventricular system, which phylogenetically considered is a very old system, and is present with varying degree of expression in all vertebrate orders, is highly developed in reptiles. It is composed of fiber fascicles, many of which are unmedullated, which arise from the preoptic and hypothalamic regions (thus presumably from olfacto-visceral centers) from dorsal thalamic centers (largely somatic) and from midline tegmental gray, and in entering the tectum course between the ependymal layer and the stratum griseum periventriculare. These are reinforced by important connections from the inferior colliculus, which constitute an acustico-optic system. These acustico-optic fibers and the periventricular system together constitute the major part of the stratum fibrosum periventriculare, in which stratum they come into synaptic relations with the short dendrites of the neurons of the stratum griseum periventriculare. ‘Therefore, it is evident that the neurons of the stratum griseum periventriculare correlate a great variety of impulses, serving as efferent centers since many of their neuraxes enter the stratum album centrale, which has been characterized as composed of the chief efferent pathways.

This pattern as found in reptiles expresses structurally a functional differentiation, as is evident by a comparison of the reptilian optic tectum with that of amphibians on the one hand and with mammals on the other. As presented in the literature (Herrick), the urodele tectum consists essentially of an inner cellular layer and an outer fibrous layer of which the more peripheral portion is composed of optic tract fibers, representing a fundamentally primitive stage both in phylogeny and in ontogeny. The dendrites of the neurons of the central gray extend toward the periphery, where they come into synaptic relation with optic and other incoming paths. The neuraxes, which often have dendritic origin, leave the tectum just superficial to the cell layer, between it and the incoming paths. In higher amphibians, as in the frog, there is to be poted a step of further differentiation in that certain neurons of the central gray have migrated toward the periphery to form somewhat indistinctly delimited layers among the fiber ' bundles. Thus there is here evidenced the beginning of a stratum fibrosum et griseum superficiale and a stratum griseum centrale, a development which can be correlated with the greater development and particularly with the greater specificity of the afferent tectal pathways resulting in a relatively greater size and functional significance of the optic tectum. Moreover, the efferent pathways in the optic tectum of the frog arise and course as they do in the reptiles among and internal to a part of the cells giving origin to them, so there is a morphological differentiation into a stratum griseum centrale, a stratum album centrale and a strateum griseum periventriculare, for the more centrally placed neurons of the cellular layer are concerned particularly with the entering periventricular system thus constituting the functional beginning of a periventricular gray stratum.

The contrasting of the tectal development as noted in the urodele with that as described for frog and reptiles serves to illustrate the great advance in morphologic differentiation in the latter forms. The high degree of morphologic differentiation can be correlated directly with the great increase in the. functional significance of the optic tectum of reptiles, constituting this area, with the closely associated dorsal thalamus, the greatest sensory correlation center of the reptilian brain, amply documented by the richness and variety of fibers constituting its efferent paths. The most obvious morphologic change noted on comparison of the lower amphibian and the frog and reptilian tecta, is the separation of the central gray layer of the lower amphibians into a stratum griseum centrale and a stratum griseum periventriculare with the interposition of a stratum album centrale in frogs and reptiles. This is explainable in part on the supposition that further migration of cells toward the incoming pathways in response to neurobiotactic influences has occurred, thus submerging the layer of efferent fibers, in part added to by the actual turning in of neuraxes, as evidence by the looping of these in the form of shepherd’s crooks, so clearly seen in chrome-silver preparations. The degree to which this more central position of neuraxes has been attained varies as we pass from the frogs and more generalized to the more specialized reptilian forms, for in the turtle a considerable portion of the efferent fiber paths still course in the stratum griseum centrale, while in certain of the lizards, in the main, they are more deeply concentrated in the stratum album centrale. The presence in reptiles of a well differentiated stratum fibrosum periventriculare is to be correlated with the high degree of differentiation of the periventricular system in these forms, representative of a high degree of correlation of the optic tectum with the midline mesencephalic and diencephalic centers and the mesencephalic auditory centers, in the main a system of ventro-dorsal correlation.

In the bird there is to be noted a further amplification of the pattern observed in reptiles, expressed largely in the increase of the number of layers or zones within the stratum fibrosum et griseum superficiale, which constitutes a major layer for the reception of impulses. Morphologically considered the acme of development as regards relative size and differentiation is reached in the reptilian and the avian tecta. It is worthy of note that almost the same degree of tectal differentiation is attained in certain of the bony fishes, where again the optic tectum constitutes a dominant sensory correlation center.

On comparison of the mammalian optic tectum with the reptilian optic tectum, the former on casual examination appears as less highly differentiated, and the degree of differentiation in mammals decreases as one passes from the lower to the higher mammalian forms. Eight layers were enumerated by Tsai in a relatively recent contribution on the optic tract and the optic tectum of the opossum, and this enumeration did not include a periventricular fibrous layer. The layers thus indicated are homologized easily with the strata described for reptiles. The observer’s innermost cell layer corresponds to our stratum griseum periventriculare, the overlying fiber layer to the stratum album centrale, the following cell layer to the stratum griseum centrale and the succeeding fiber and cell layers, exclusive of the superficial optic stratum, and his stratum zonale, with the associated gray, are components of our stratum fibrosum et griseum superficiale. As one progresses from marsupial to rodents and carnivores and to the higher primates the six fundamental strata are still represented, but the relative development and differentiation of the several strata varies as one passes from lower to higher forms. The differences in development are exhibited more particularly in the differentiation of the two receptive layers, the stratum fibrosum et griseum superficiale and the stratum griseum periventriculare with its associated stratum fibrosum periventriculare.

In human the description of the optic tectum is based largely on Weigert preparations. The following layers are very generally recognized and are here enumerated from without inward: 1, a stratum zonale; 2, a stratum griseum or cinereum; 3, a stratum opticum; 4, a stratum lemnisci, containing cells as well as fibers; 5, a stratum profundum, likewise containing gray and white, and, internal to this layer, the scattered cells of the mesencephalic root of the fifth nerve with periventricular gray. The most obvious difference between the primate and the reptilian tectum consists in the relative position of the stratum opticum and this difference is only relative, for while in many reptiles the optic tract lies close to the periphery in others, as in the turtle, it is separated from the surface by a zone containing here and there a few cells on its inner surface, forming thus a potential stratum zonale. In mammals, as seen in the opossum and on up through primates, the stratum opticum, which belongs to the afferent systems of the tectum, lies relatively deeper within the main receptive layer so that certain of the afferent fibers, largely cortico-tectal and thus new in mammals, and the receptive gray lie superficial to the optic stratum, constituting the stratum zonale and the stratum cinereum of mammals. The stratum lemnisci of mammals, with its gray and fiber components is a direct representative of the main portion of the stratum fibrosum et griseum superficiale. The stratum profundum with its outer layer of gray and its inner layer of white constitutes respectively the stratum griseum centrale and the stratum album ‘centrale. The stratum griseum periventriculare and its associated stratum fibrosum periventriculare are present certainly in higher mammals, the former being constituted in man by other cells and the cells of origin of the mesencephalic root of the fifth nerve, and the latter, as far as evidence exists at present, being limited to relatively few scattered fibers. Therefore, it is evident that the postulated six fundamental tectal strata are present in mammals including man although somewhat modified in accordance with functional changes. The foregoing account emphasizes two aspects of tectal phylogeny. One of these concerns its development according to a fundamental pattern; the other is concerned with the variation in correspondence with its réle as a correlation center and its relationship to the serisory correlations of the brain as a whole. The raison d’étre of this fundamental pattern as well as of its variation is to be sought in its dual activity, on the one hand serving as a sensory correlation center and on the other hand as a discharge center for efferent impulses. Stratification, simple or complex, is a morphologic expression of the subdivision into afferent and efferent centers. The main efferent (but also correlative) center and fiber tracts occupy the more central portion and thus separate a superficial receptive correlation layer from a deep or periventricular layer, primarily receptive and correlative but also efferent in function. The trend of development as one passes from amphibians to reptiles and birds is toward an increase in the richness and complexity of the afferent sensory impulses; optic, tactile, pain and temperature impulses from the body and the head and correlated somatic sensory impulses from the dorsal thalamus of the same and opposite side, together with rich intertectal, pretectal and subpretectal connections, so that the tectum with the intimately related dorsal thalamic centers become the main sensory correlation center of the brain, overshadowing in richness of correlation and degree of morphologic differentiation the developing cortex in these forms. The alternating layers of gray and white within the receptive area undoubtedly permit a localization of impulses within this area. The ventrodorsal correlation systems, as represented in the periventricular fibers, and the acustico-optic fibers, carrying in auditory impulses from the inferior colliculus, were described as coming into relation with the neurons of the periventricular gray. These neurons, through the spread of their dendrites into the stratum fibrosum et griseum superficiale, serve to correlate within themselves optic, tactile, pain and temperature impulses, with auditory impulses and with the impulses brought in through the periventricular system, which in part as least are olfacto-visceral in character. Since the periventricular layer and fiber paths which influence it are large in the reptilian tectum, they must be regarded as of distinct significance in any consideration of it as a sensory correlation center. The high development and differentiation of both of these receptive layers in reptiles and in birds is morphologic evidence that in these forms the tectum has reached the peak of its development as a sensory correlation center. The efferent paths in the reptilian and avian tectum are also well developed, discharge being made to diencephalic, tegmental, cerebellar and bulbar centers, with few if any tecto-spinal paths. Of particular interest are the tecto-thalamic connections, for the dorsal thalamus receives at best few lemnisci fibers and is dependent for its development upon the various sensory impulses which reach it by way of bulbo-tectal and tecto-thalamic paths, the development of the dorsal thalamus going hand in hand with the development of the tectum in these forms.

In the mammalian brain the highest sensory correlation centers are found in the cerebral cortex, which, with the exception of the olfactory cortical areas, interrelate impulses brought into the cortex from tbe dorsal thalamus, consequently in all mammals there are to be found thalamocortical paths, which increase in number and complexity as one passes from lower to higher forms. This increase in the dominance of the sensory centers of the cerebral cortex is associated with a gradual decrease of the optic tectum as a dominant sensory correlation center. In causal relation to its decreasing importance as the major sensory correlation center are to be emphasized changes in its fiber relations. An increasingly greater number of optic tract fibers terminate in the metathalamic lateral geniculate nucleus, so that in man, at least, the optic tectum has chiefly such direct optic tract fibers as mediate light reflexes. However, visual impulses reach the optic tectum after a synapse in the dorsal nucleus of the lateral geniculate body, through the peduncle of the lateral geniculate. And further, the ascending sensory pathways in crescendo from lower to higher mammals in the main skirt the tectal region in order to reach their major nuclei of termination in the dorsal thalamus, contributing in their course small bundles and in certain cases collaterals only to the main receptive stratum of the optic tectum. With the gradual loss of its function as a necessary relay station in the path of ascending sensory impulses to the dorsal thalamus there is noted a gradual decrease of tecto-thalamic and thalamo-tectal fibers, the ouly clearly recognized exponent of these systems in man being found in the peduncle of the lateral geniculate and certain commissural systems. This decrease in the afferent systems to the tectum is evidenced structurally by a relative reduction in the differentiation and size of a part of the outer receptive layer, the stratum lemnisci. There isa shifting inward of the optic tract so that the stratum fibrosum et griseum superficiale, represented in amphibians and highly developed as a single stratum in the reptilian and avian optic tecta, is differentiated in mammals into a superficial portion to which in man the name stratum zonale and stratum cinereum are generally applied, and a deeper porticn commonly known as the stratum lemnisci. Consequent to a decrease in the afferent systems there is noted a decrease in the tecto-thalamic paths.

The efferent paths to motor centers carry progressively longer fibers in passing from lower to higher forms, so that in man tectospinal paths have been traced to at least the middle of the spinal cord. Thus in this sense the efferent systems of the optic tectum are more efficient in higher mammals and in man than in the lower mammals. The marked reduction of the stratum periventriculare fibrosum in higher mammals and man appears to be associated in part at least with the reduction of the periventricular fiber system.

It must be evident from what has preceded that the optic tectum affords a classic example of the interrelation of structure and function. Its rise to a position of functional dominance finds its expression in a high degree of morphologic differentiation; its decline from a dominant position is associated with a decrease both in relative size and in morphologic differentiation.

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