Book - The brain of the tiger salamander 16

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Herrick CJ. The Brain of the Tiger Salamander (1948) The University Of Chicago Press, Chicago, Illinois.

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Chapter XVI Optic and Visual-Motor Systems

THE eyes in Amblystoma are much better developed than they are in Necturus, where they are degenerate, though functional. The retina of Triturus is more highly differentiated, and vision is evidently more efficient. In frogs this advance is carried much farther, with corresponding structural elaboration of the visual centers of the tectum opticum and thalamus.

Optic Nerve and Tracts

The optic tracts and their connections of Necturus have been described ('41a). An account of the development of the optic nerves and tracts of Amblystoma was published in the same year ('41), and subsequently ('42) a detailed analysis of the visual centers and their connections, together with commentary on related physiological problems. Some further theoretical considerations were published later ('44a). These details need not be repeated. The salient features were outlined in chapter iv, and some topics are amplified here.

In the coil stage (Harrison's stage 34), optic nerve fibers begin to grow from the ganglion cells of the retina through the optic stalk before the other retinal layers are histologically differentiated ('41, p. 477; Coghill, '16, Paper II, p. 274). In the S-reaction stage (Harrison's stages 35, 36) these fibers reach the brain; in early swimming stages (Harrison's stages 36, 37) they decussate in the chiasma ('41, p. 480); and shortly thereafter they reach the tectum (Harrison's stage 38) and the primordial basal nucleus in the peduncle. Up to this stage, rods and cones and other retinal layers are incompletely differentiated. In stages immediately preceding effective feeding reactions (about stage 44) the retina is functional, and the larva can orient itself with reference to an object moving in the field of view; and shortly thereafter well co-ordinated lurching and snapping movements efficiently capture moving prey. The first visual responses are probably activated by fibers from the tectum through the posterior commissure to the nucleus of Darkschewitsch and the fasciculus longitudinalis medialis and perhaps also by the basal optic tract, though the time of the appearance of these fibers has not been recorded. Tecto-bulbar and spinal fibers mature very soon after those of the posterior commissure, the uncrossed fibers preceding the crossed fibers. These and the tecto-peduncular fibers described below are apparently the pathways employed in the activation of the skeletal musculature of the trunk and head when they are employed in the capture of food. Early feeders (stage 46) have attained full larval status, and in subsequent stages the visual system is not radically changed except for an increase in the number of thin retinal fibers and an enormous increment of these at metamorphosis, the total number of fibers in adult Amblystoma tigrinum probably reaching about 8,000 ('41, p. 506).

Correlation of this developmental history with experimental work by others has led me to the hypothesis that in Amblystoma the thick retinal fibers, which appear first in ontogeny, activate generalized total behavior patterns and that the thin fibers are concerned with more refined analysis of visual experience. (It does not follow that this is true in mammals, in which the visual responses are under thalamo-cortical control.) What kind of mechanism is employed in this analysis is still obscure. My opinion ('41, p. 528) that endings of thin and thick fibers have separate locahzation in the tectum proved on further study to be unfounded ('42, pp. 284, 293), and there is little anatomical evidence of any other kind of visual localization here, though experimental evidence cited below indicates that retinal loci are projected locally upon the tectum.

The more important known connections of the visual system are shown in the simplified diagrams (figs. 6, 11-16, 18, 20-24, 93, 101; '36, figs. 2, 6, 7; '42, figs. 4, 5, 79). Fibers of the optic nerve are distributed to five quite separate fields in the brain stem: (1) tectum, (2) pretectal nucleus, (3) cerebral peduncle, (4) thalamus, and (5) hypothalamus, as shown schematically in figure 14. This wide distribution is in marked contrast with the tendency of the other functional systems of peripheral nerves to converge into a single primary central field. This dispersal appears to have been determined by the types of motor response to be evoked rather than by the sensory qualities of the visual excitations. These five receptive fields will now be examined.

The tectum opticum evidently is the most extensive of these fields and physiologically the dominant member (see below).
The pretectal nucleus may participate in the regulation of the intrinsic musculature of the eyeball and have other functions still unknown.
The basal optic tract is present in all classes of vertebrates from cyclostomes to man. It is evidently of major importance, though little attention has been given to it in current studies of the physiology of vision. Two possible functions have been suggested for it in Amblystoma. The more primitive of these is to act as a general activator of the ocular and somatic muscles in response to visual stimuli, manifested in such behavior as the "regarding reaction" described by Coghill (pp. 38, 78). In the second place, the structure and connections of the area ventrolateralis pedunculi, within which the basal optic fibers terminate, suggest that this neuropil may be part of the apparatus of conditioning of visual reflexes (p. 38).
Optic terminals are widely spread in the thalamus and are especially concentrated in its posterior part. This ill-defined area of neuropil receives the brachia of the superior and inferior colliculi and is regarded as the primordium of the lateral and medial geniculate bodies (p. 239; '42, p. 280). Large numbers of efferent fibers go out from this field to the peduncle and the dorsal and isthmic tegmentum. The fibers to the tegmentum take four courses. Two are superficial, the uncrossed tractus thalamo-tegmentalis rectus and a crossed path ('42, p. 224, tr.thieg.d.c.A.) which decussates in the postoptic commissure. Two other tracts take deep courses close to the gray, one of which decussates ('42, p. 224, tr.th.teg.d.c.B.) and the other descends uncrossed in dorsal tegmental fascicles of group (7). For a detailed description see the analysis of the postoptic commissures in chapter xxi. These four tracts end chiefly in the dorsal and isthmic tegmentum, two of them in the superficial neuropil and two at deeper levels. They provide pathways for visual control of local reflexes, particularly those employed in capturing food. There is no separate optic projection tract from the thalamus to the cerebral hemisphere, though visual influence may reach the hemisphere through the thalamo-frontal tract, which is a common pathway of sensory projection from the dorsal thalamus (pp. 95, 238, and fig. 19, tr.th.f.).
There is a small number of optic terminals and collaterals in the hypothalamus near the chiasma ('42, pp. 219, 233, 237) . They connect with the large cells of the preoptic nucleus, axons of which form the hypophysial tract (p. 245). This is doubtless the pathway for visual influence upon hypophysial endocrine activity. This connection is probably smaller in Ambly stoma than in some other vertebrates, and different opinions have been expressed about it. Eugen Frey's description ('38) of a large hypothalamic optic root in some amphibians was evidently based on inadequate material and faulty observation, as I have pointed out ('396, pp. 558-76; '41a, p. 498; '42, pp. 218, 233). The same is probably true of Geiringer's ('38) description of a passage of fibers from the optic nerve directly into the hypophysial tract. I have preparations that give this appearance, but more critical examination disproves it. There is some evidence that in fishes and amphibians efferent fibers go out from the preoptic nucleus through the optic nerve to the retina ('336, p. 254); but I have not been able to confirm this or the claim of some authors that efferent fibers go out to the retina from the tectum. Both these connections may exist. In the chiasma the coarser optic fibers are segregated from the finer, and most of them take deeper courses in the optic tracts — the axial bundles. As the optic tracts traverse the thalamus, they separate into medial (dorsal) and lateral (ventral) tracts, each of which contains both thick and thin fibers. In the tectum most of these fibers end by wide arborizations in a common pool of intermediate neuropil (fig. 93, layer 2).

Tectum Opticum==

In embryological development the first afferent fibers to reach the tectum are those of the optic tract. These terminate in its anterior part near the posterior commissure, and tectal structure matures in subsequent stages from this region posteriorly. In the adult the common pool of neuropil, to which reference was made above, also receives similar terminals of the spinal and bulbar lemnisci, the brachium of the superior colliculus from the thalamus, the strio-tectal and habenulo-tectal tracts, and some other fibers. This pool of neuropil is spread throughout the entire tectum, with little evidence of localization of function within it.

The optic tectum is structurally nearly homogeneous, with two exceptions: (1) a dorsal thickening on each side, which is related with the dorsal tectal commissure and probably corresponds (in some respects only) with the torus longitudinalis of fishes ('42, pp. 250, 287), and (2) the eminence of the posterior commissure at the anterior border of the tectum, likewise chiefly commissural in function. The stratification of the tectum, which is so conspicuous in the frog and many other vertebrates, is here notably absent. The only layers that are clearly evident are the deep gray and the superficial white, though there are obscure indications of the incipience of further stratification, more evident in the alba than in the grisea. For descriptive purposes I have divided the optic tectum, somewhat arbitrarily, into eight concentric layers, as shown in figures 36 and 93; for their characteristics see page 244 of 1942.

Two features of tectal structure merit special emphasis. The first is that the convergence of most of the afferent fibers into a common pool of neuropil of almost homogeneous structure suggests a totalizing or integrative function for the tectum as a whole. The second point of major interest is that the efferent fibers from the tectum are extremely diversified in structure and distribution. There are all gradations from diffusely spread fibers in the deep neuropil to welldefined long myelinated tracts like the tecto-bulbar and tecto-spinal systems. This suggests that such localization of function as exists in this tectum is determined more by what is going on in the efferent side of the arc than in the afferent side, a point which has been emphasized by Crosby and Woodburne ('38).

Five strong systems of myelinated fibers leave the tectum. These take widely divergent courses. They are as follows:

1. Commissura posterior. — These are the first to appear in the embryo. The crossed fibers are joined by uncrossed fibers from the eminence underlying the commissure, and they spread widely in the peduncle and adjoining parts of the thalamus and dorsal tegmentum. The primary connection is with the nucleus of Darkschewitsch (p. 217 and figs. 6, 18, 22) and thence to the f . longitudinalis medialis, providing innervation of the trunk musculature in response to visual stimulation.

2. Tractus tecto-peduncularis rectus et cruciatus (p. 303 and figs. 18, 22, tr.t.p.c; '42, p. 267). — These thick fibers arise from the anterior part of the tectum, descend parallel with fibers from the posterior commissure, decussate (in part) in the commissure of the tuberculum posterius, and arborize in the alba of the peduncle of both sides more ventrally than those of the posterior commissure. Their course as seen in horizontal sections is shown in figures 30-36, tr.t.p.c.l. (see also '42, p. 267, and the figures there cited). They activate the interstitial nucleus of the f. longitudinalis medialis and probably also the oculomotor nucleus and appear to be adapted to regulate mass movements of trunk, limbs, and eyes in the orientation and movements of the body with reference to objects in the visual field. These fibers are joined by similar thick fibers from the pretectal nucleus and dorsal thalamus (tr.fh.p.c. of the figures).

Superficially of the connection just described, there is a large collection of uncrossed fibers passing between the pretectal nucleus (pars intercalaris diencephali) and the peduncle. These were described in Necturus ('17, p. 264; '336, p. 110 and fig. 57) under the name "tr. thalamo-peduncularis dorsalis superficialis." These fibers are spread close to the pial surface in the wide di-mesencephalic fissure and end in large numbei-s in the neuropil of the area ventrolateralis pedunculi. Some of them also reach the hypothalamus. The condition in Amblystoma is similar, thus bringing the pretectal nucleus into intimate relation with terminals of the basal optic tract and the oculomotor nucleus.

3. Tr actus tecto-thalamicus et hypothalamicus cruciatus (fig. 12, tr.t.th.h.c.a. and p.\ see also the section on com. postoptica in chapter xxi). — The anterior and posterior divisions of this complex were described in 1942 (p. 221). The anterior tract passes from the dorsal part of the superior colliculus to the hypothalamus, decussating in the postoptic commissure. It is here termed "tr. tecto-hypothalamicus anterior" (figs. 25-36, tr.t.hy.a.; see further on p. 296). It has connections with the thalanms and hypothalamus of both sides, and some of its crossed fibers may reach the peduncle and tegmentum.

The posterior division arises chiefly from the inferior colliculus, with accessions from the ventral border of the superior colliculus. It lies parallel with the anterior division and, more posteriorly, partially decussates in the postoptic commissure and has terminals in the thalamus and hypothalamus of both sides (figs. 25-35, tr.t.th.h.c.p.). Its thicker and more myelinated fibers continue as tr. tecto-tegmentalis cruciatus into tegmental fascicles of groups (6) and (8), to end in the peduncle and tegmentum as far back as the VII nerve roots. The distribution of these fibers suggests that they are primarily concerned with mass movements and local reflexes of the musculature of the head and probably also with conditioning of these movements. What seems to be the equivalent of this tract is described as connected with the nucleus isthmi in all animals in which that nucleus is well developed; but in urodeles this tract is very large, though the nucleus isthmi is vestigial.

4. Tecto-hulbar and tectospinal tracts. — These tracts have been described and illustrated in the papers of 1936 (p. 340) and 1942 (p. 268). They are the largest of the efferent tracts, and most of their fibers are well myelinated. There are two crossed tracts (figs. 12, 27-36, tr.t.b.c.l. and ir.i.b.c.2.) and an uncrossed tract (tr.t.h.c.r.) from the tectum opticum. The posterior crossed tract itr.t.h.c.2.) decussates transversely in the vicinity of the nucleus of the IV nerve. The anterior crossed tract {tr.t.b.c.l.) takes a peculiar course, its fibers entering the ventral medial tegmental fascicles, f.v.t.{l), within which they decussate obliquely. There are about a dozen of these anastomosing fascicles extending from the commissure of the tuberculum posterius backward to the level of the IV nucleus, where these crossed fibers join those of tr.t.b.c.2. and descend to the medulla oblongata and spinal cord (figs. 6, 12).

The uncrossed tecto-bulbar fibers — tr. tecto-bulbaris rectus — were seen in my earlier studies to arise only from the posterior part of the tectum, as drawn here in figure 12 (tr.t.b.r.); but later ('42, p. 269) other fibers of this system were found to arise more anteriorly and to pass backward by several pathways to join the posterior group. The most anterior of these fibers enter dorsal tegmental fascicles of group (7) , from which they separate to join the posterior tract. Others pass spinal ward in layers 3 and 4 of the tectum, at the posterior end of which they join the other fascicles. Here they send collateral branches into the isthmic visceral-gustatory nucleus, as shown in figure 23. Below the junction of these three divisions, the tr. tecto-bulbaris rectus descends superficially in the isthmus, then turns spinalward, under the lateral recess of the ventricle, passing through the ventral border of the auricle into the medulla oblongata, where it joins the crossed tecto-bulbar tract.

5. Brachia of superior and inferior colliculi. — These are large collections of fibers passing in both directions between the tectum and the thalamus. They are widely dispersed, and most of them discharge from tectum to dorsal thalamus. Those from the superior colliculus are spread throughout the alba and form a massive tract (figs. 34, 35, 36, tr.t.th.r.). These are joined by some fibers from the inferior colliculus, and from the latter area other strands of unmyelinated fibers take separate courses, some passing forward in the dorsal part of the tectum and some at its ventral margin; most of these fibers pass from inferior to superior colliculus, but some of them continue into the thalamus, particularly ventrally, to enter the geniculate neuropil (figs. 14, 15, 16, br.col.; '42, p. 264).

C onclusion

The internal structure of the optic tectum of Amblystoma and the wide spread of its fibrous connections, both afferent and efferent, suggest that in this animal the primary function of the tectal system is visual control over movements of the body as a whole and, in particular, the orientation of the body and conjugate movements of the eyeballs with reference to objects in the visual field. Such other local visual reflexes as the animal possesses are probably organized elsewhere.

TECTO-OCULOMOTOR CONNECTIONS

The visual location of food and enemies involves the innervation of the muscles of the eyeballs, and our knowledge of the apparatus employed in the conjugate movements of the eyes is scanty. The anterior and posterior divisions of the crossed tecto-bulbar tract decussate, respectively, in the vicinity of the nuclei of the III and IV nerves (fig. 12). The anterior division {tr.t.h.c.l.) crosses in the ventral medial tegmental fascicles which span the rather long distance between the III and the IV nuclei. When these ventral fascicles — group (1) of my analysis in 1936 — were first identified as tecto-bulbar fibers, it was supposed that this anomalous arrangement was a provision for activation of the eye-muscle nuclei by collaterals from these fascicles. No evidence of this has been found, but the myelinated fibers of both tr. tecto-bulbaris cruciatus 1 and 2 are accompanied by very many shorter, unmyelinated fibers, which pass from the tectum to the III and IV nuclei of both sides. This tr. tecto-peduncularis is shown diagrammatically in figures 18, 22, and 24 (and in more detail in '42, figs. 14, tr.t.p.2., and 45, tr.t.p.c.2.). In addition to the tectopeduncular fibers in the alba, there is a deep series (tr. tecto-peduncularis profundus, '42, p. 267 and fig. 14, ir.t.p.3.), which takes tortuous courses in the neuropil of the grisea. From the anterior part of the tectum and pretectal nucleus the well-defined tr. tecto-peduncularis cruciatus and the uncrossed tr. thalamo-peduncularis dorsalis superficialis may participate in the regulation of conjugate movements of the eyes.

If pupillary constriction is controlled from the pretectal nucleus, as in mammals, there are two available pathways to the III nucleus, first, by way of the pretectal components of the two tracts last mentioned and, second, by tr. pretecto-hypothalamicus (p. 296 and fig. 15, tr.pt.hy.) and thence to the III nucleus by tr. hypothalamopeduncularis (figs. 18, 23, tr.hy.ped.).

VISUAL FUNCTIONS

Most of our experimental knowledge of visual functions of amphibians has been derived from Amblystoma, Triturus, and frogs. In these animals there is no visual cortex, and in urodeles there is no specific optic projection tract to the cerebral hemisphere. Here the intrinsic features of the stem portion of the visual apparatus can be studied, simplified by absence of the cortical connections; and yet the complications of internal structure as just summarized present baffling physiological problems. Triturus has more efficient eyes than Amblystoma, and in frogs this differentiation is much further advanced, so that the Anura offer the most promising approach for experimental analysis, and for this we need more information about the histological structure of the anuran brain than is now available.

The electrical activity of the optic tectum of the frog has been investigated by Beritoff ('43, pp. 215-40) in co-operation with Tzkipuridze, who present oscillographic records of its spontaneous activity and of the effects of various kinds of stimuli. A distinction is drawn between the quick oscillations due to excitation of the ganglion cells of the retina and slow oscillations ascribed to activity of the neuropil. Similar studies with the aid of microelectrodes may profitably be made of the properties of the layers of the tectum and other central stations of visual activity.

Attention has been called ('41, p. 521) to evidence that the retina of Triturus is more highly, differentiated histologically than that of Amblystoma. That it is functionally superior is confirmed by the experiments of Stone and Ellison ('45), who exchanged eyes of adult A. punctatum and T. viridescens. The Triturus grafts degenerated, but the Amblystoma eyes on Triturus hosts followed a course of recovery as they do in homoplastic transplantations, retinal degeneration being followed by complete regeneration. Visual acuity appeared to be higher than in normal Amblystoma but lower than in normal Triturus.

In the feeding reactions of larval Amblystoma, the location and seizure of prey can be successfully done, in the absence of eyes, with the aid of the lateral-line organs (Scharrer, '32; Detwiler, '45). The lemniscus systems may discharge lateral-line impulses into the tectum, in company with those of other sensory systems; the mesencephalic V system may participate in the reaction; and the habenulotectal tract may transmit an olfactory influence. In addition to these, there is a large thalamo-tectal connection and a small strio-tectal tract. But there is no experimental evidence about the specific functions of any of these connections.

The tectum and thalamus are connected by fibers passing in both directions (figs. 11, 12). These are precursors of the mammalian brachia of the superior and inferior colliculus. It is evident that the tectum and the dorsal thalamus may act as an integrated unit in regulating the major activities of the body in adjustment to external situations. With the emergence of the cerebral cortex in higher animals, this pattern is radically changed, and for the understanding of these changes it is essential that the pre-existing organization be adequately known. The history of the transformation of this generalized amphibian structure to those of reptiles and mammals has been sketched by Huber and Crosby ('43).

Evidence has been published that in some vertebrates the several quadrants of the retina have local representation in the optic tectum. In a series of vertebrates, including several species of amphibians, Stroer ('39, '39a, '40) described continuous fascicles of fibers from the retinal quadrants to the tectum, where they end locally in an arrangement which projects the retinal quadrants upon the tectum in reversed orientation. I have made diligent search for evidence of such an arrangement in Necturus and in young and adult Amblystoma without success ('41, '41a, '42). In Amblystoma thick and thin fibers from the different retinal quadrants are inextricably intertwined in the optic nerve. At the chiasma the thick .fibers are segregated from the thin fibers, and in the tectum the terminals of both kinds of fibers mingle and seem to be distributed nearly uniformly to all parts. There is physiological evidence that Amblystoma can visually localize objects in the field of view; and, by analogy with other animals, the presumption is strong that retinal loci are projected upon the tectum in more or less definitely circumscribed areas.

In Triturus and Amblystoma good localization of objects in the visual field is restored after transplantation of the eyes (Stone, '44; Stone and Zaur, '40; Stone and Ellison, '45), and it is preserved after rotation of the eyeball through 180°, though in the latter case motor reactions to objects in the visual field are reversed from the normal (Sperry, '43). Similar physiological results follow operations which eliminate the chiasma and connect the retina with the tectum of the same side, and also after transplanting an eye to the opposite side of the head (Sperry, '45). These observations have been repeated upon seven species of anurans, all of which have much more highly differentiated visual apparatus, with similar results. After the cutting of the optic nerve and its regeneration in the adult animal, the same results were obtained. Vision was normal in those animals whose retinas had been kept in normal position, but it was reversed about the optic axis in animals whose retinas had been rotated through 180° prior to nerve section (Sperry, '44, '45). In frogs, destruction of quadrants of the tectum of both normal and operated animals resulted in scotomas of local quadrants of the visual field in a pattern which is in agreement with the anatomical observations of Stroer ('39rt); and, in cases in which the eyeball was rotated, the scotomas were in arrangement reversed from that found when the eyes were in the normal position.

These experiments increase the probability that, in Amblystoma, retinal loci are in some way projected locally upon the tectum; but the mechanism employed in localization of visual functions can be clarified only by further experimentation. Sperry 's experiments demonstrate "the high degree to which the complex and precisely patterned neural mechanisms subserving adaptive visuomotor coordination are dependent upon inherently predetermined rather than upon functionally acquired neural adjustments."