Accessory optic system of rhesus monkey

EXPERIMENTAL

NEUROLOGY

Accessory

63, 163-176 (1979)

Optic System of Rhesus Monkey

HOMIN Department

of Anatomy,

Birmingham, Medicine,

LIN AND ROLAND A. GIOLLI Medical

Center,

University

of Alabama

Alabama 35294, Department of Anatomy, and Department

of Psychobiology, University Irvine, California 92717 Received

August

in Birmingham,

California College of of California,

3, 1978

The accessory optic system of the rhesus monkey (Macaca mulatta) was investigated using the silver method of de Olmos-Ingram to determine the course and distribution of its degenerating fibers following retinal evisceration. Serial Nissl sections were used to relate the axonal degeneration to the brain stem cytoarchitecture. It is found that this system consists of a dorsal and a lateral terminal nucleus together with a superior fasciculus (posterior fibers). The retinal fibers within this superior fasciculus originate primarily from the contralateral and some from ipsilateral retina. These fibers leave the superior quadrigeminal brachium to course ventrally and anteriorly over the caudolateral aspects of the medial geniculate, the inferior brachium, and the dorsolateral portion of the cerebral peduncle to terminate within the dorsal and lateral terminal nuclei.

INTRODUCTION Hayhow and co-workers (17- 19) introduced a nomenclatural scheme for the components of the mammalian accessory optic system (AOS) which has now been widely accepted. In accordance with this scheme, five major components can be identified: superior and inferior fascicles, together with dorsal (DTN), lateral (LTN), and medial (MTN) terminal nuclei. The superior fascicle is in turn composed of anterior, middle, and posterior fibers. The projection is entirely contralateral. An AOS consisting of all five components was described in marsupials (12, 18, 29), rodents (19, 30), lagomorphs (9, 14), carnivores (31), and Tupaia [tree shrews (1, IS)]. On the other hand, a reduced AOS in terms of the number of components was reported in rodents (8), carnivores (17,39), Abbreviations: LTN-dorsal,

AOS-accessory medial,

lateral

optic system; AOT-accessory

terminal

optic tract; DTN, MTN,

nucleus.

163 0014-4886/79/010163-14$02.00/O Copyright 0 1979 by Academic Press, Inc. All rights of reproduction in any form reserved.

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ungulates (25,26), insectivores [hedgehogs (1,43)], primates (1,3,4,9, 11, 15,21,28,40-43), and other mammals (2,23,36). As evident above, both a complete AOS and a reduced AOS have been reported for Carnivoru ; and the species studied in common was the cat. Although Hayhow (17), using the suppressive Nauta-Gygax method, could identify only the superior fascicle plus three terminal nuclei, Lin and Ingram (3 1) also demonstrated the inferior fascicle with the sensitive silver impregnation technique of de Olmos and Ingram (7). Similarly, the inferior fascicle was described in the golden hamster with the latter technique (30), which the Fink-Heimer and autoradiographic methods failed to reveal (8). An inferior fascicle, present in almost every infraprimate species, has not been reported for any primate. It would be significant for academic and practical purposes if such a pathway could be shown by the de Olmos-Ingram technique in the monkey as well. Such a tract would undoubtedly complicate the physiological and behavioral studies relating to the primate AOS (15, 27, 32-34, 44). Without an intricate review and discussion it suffices to say that the primates as a group undergo the greatest degree of reduction in the AOS. Even though a complete lack of AOS was mentioned in the cynomolgus monkey [a macaque (9)], Giolli (11) first demonstrated that the AOS of this species consists only of foreshortened superior fascicle (posterior fibers) together with a LTN. Subsequent studies in essence confirmed such foreshortening in Perodicticus (15), lorisid lemurs [G&go (1, 3, 28, 43) and Nyticebus (1, 15, 28)], squirrel monkeys (1,4,41), chimpanzees (40), and rhesus monkeys (21). Some of those studies showed a poorly defined DTN as well (1, 15, 40, 41, 43). The rhesus monkey is a widely used laboratory primate species in the field of neurobiological research. However, only some sketchy and conflicting information on the anatomy of its AOS can be found in the older literature [for reviews see (10, 11, 16- 18)]. For some time only a brief description of its organization has been available, based on modem neuroanatomical techniques (21). A basic and comprehensive analysis of its anatomy now appears urgently needed because of the structural and behavioral studies by the Pasiks and colleagues (33-35) and physiological investigations on this part of the primate visual system (27, 32, 44). MATERIALS

AND METHODS

Seven rhesus monkeys (Mucuca mufuttu) were used, each weighing 2.5 to 3.5 kg and of either sex. Each animal was anesthetized with sodium pentobarbital. The left eye was slit open with a sharp knife in its dorsolateral aspect just behind and parallel to the comeoscleral junction.

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The retina and other intraocular contents were eviscerated with suction. The eye was then padded with gelfoam and the eyelids were sutured together to prevent infection. The monkeys were killed after an interval of 12 or 14 days (two animals), or 1, 3, 5, or 6 months subsequent to the operation. At killing, all monkeys were given overdoses of sodium pentobarbital and their brains were perfused transcardially with saline followed by 10% cacodylate-buffered formalin (7). Each brain stem was cut on a freezing microtome at 30 pm in the frontal plane. Approximately every 10th section was then impregnated by the de Olmos-Ingram method (7) to reveal the Wallerian degeneration. Contiguous sections of 60 pm were prepared by the Nissl method (cresyl violet acetate stain). Figure 1 is a composite mapping of the patterns of axonal degeneration seen in our experimental monkeys. RESULTS According to Hayhow’s (17- 19) general classification, a mammalian AOS is composed of two fibrous (superior and inferior fascicles) and three nuclear (DTN, LTN, MTN) components. The inferior fascicle leaves the principal optic tract to run between the cerebral peduncle and lateral hypothalamus. Its fibers course caudally in this same relative position and terminate in the MTN near the emergence of the oculomotor nerve. The superior fascicle proceeds from the posterior margin of the optic tract and the adjoining portion of the superior quadrigeminal brachium. Its axons pass superficially over the medial geniculate and cerebral peduncle to end in the MTN. The posterior fibers of this tract terminate also in the DTN and LTN. Only a superior fascicle (posterior fibers only) and the DTN and LTN are found in our rhesus monkeys, as presented below. Nuclear

Components

of Rhesus Accessory Optic System

The LTN is the larger of the two terminal nuclei (Fig. 1). Caudally it is situated dorsolateral to the inferior brachium and ventromedial to the main bulk of the medial geniculate (Fig. 1, A 2.0). The superior fascicle enters this caudal portion of the LTN; this is also the case in other primates (40-43). More anteriorly the LTN lies lateral to the upper half of the cerebral peduncle (Fig. 1, A 5.5). It is slender at this locus, as it is in M. cynomolgus (1 l), and it attenuates farther rostrally. This rostra1 protrusion corresponds to the “peduncular extension” described in the squirrel monkey (42). Although not labeled, this nucleus could be clearly identified in Nissl preparations of the rhesus brain atlas (38) at stereotaxic levels A 2.5-4.0 and A 5.5.

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FIG. 1. The organization of the rhesus accessory optic system (AOS) as revealed with the de Olmos-Ingram technique subsequent to unilateral retinal evisceration. The resultant fiber degeneration is plotted on partial tracings of frontal Nissl sections which are contained in the stereotaxic atlas of Snider and Lee (38). The cross at lower edge of each drawing indicates vertical - 1 mm and 6 mm to the left of midline. The anteroposterior distance (in millimeters) from the interaural line is shown at the lower left comer. Dashed lines depict degenerating axons of passage, and dots the degeneration of pericellular and terminal fibers. Axonal decomposition within principal optic nuclei is not illustrated. The rhesus AOS is bilaterally projected. The other halves are mirror-images of the above diagrams and are therefore not shown. Abbreviations for all figures: BIC-brachium of inferior colliculus, BSC-brachium of superior colliculus, CP-cerebral peduncle, DTN-dorsal terminal nucleus of AOS, LGB-lateral geniculate body, LTN-lateral terminal nucleus of AOS, MGB-medial geniculate body, Pul-pulvinar, SC-superior colliculus, SF-superior fascicle (posterior fibers) of AOS.

The DTN lies more dorsal and posterior than the LTN (Figs. 1, 2). It is situated in the rostra1 level of the superior colliculus, approximately at AP 0, immediately caudal to the medial geniculate and the pretectum, and is sandwiched between the superior and inferior brachia. This nucleus is more difficult to delineate particularly medially where its sparse perikarya are interpersed among accessory optic axons comprising the initial portion of the superior fasciculus (Fig. 2). Its cell bodies usually do not encroach on the most lateral portion of the fascicle, however. Both LTN and DTN are composed of neurons of small to medium size which contain moderate amounts of Nissl substance. The largest cross-sectional area of each nucleus is about equal. However, because

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I cu

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the LTN is much longer anteroposteriorly, its volume is also larger. A MTN could not be identified because we could not see degenerating fibers either in the inferior fasciculus or in that portion of the superior fascicle extending beyond the LTN. According to the rhesus brain atlas (38) the area corresponding to the MTN (or its synonyms) is occupied by the substantia nigra, pars compacta. Fibrous Components

of Rhesus Accessory Optic System

The distribution of silver degeneration debris in the AOS is similar in all our monkeys, with overt differences only in its quantity. Therefore these monkeys are discussed below in a composite fashion. (i) Contralateral Distribution. The degenerating axons comprising the contralateral superior fascicle (posterior fibers only) are first seen leaving the superior brachium between caudal portions of the medial and lateral geniculate bodies. Some of its fibers terminate immediately in the DTN (Fig. 3a). Others continue ventrally and slightly anteriorly along the caudolateral aspects of the medial geniculate, the inferior brachium, and the upper lateral surface of the cerebral peduncle and finally end in the LTN. No degeneration could be traced farther medially along the ventral surface of the basis pedunculi, nor is there evidence for an inferior fasciculus or the anterior and middle fibers of the superior fasciculus. (ii) Zpsilateral Distribution. An ipsilateral, less populous counterpart of the crossed superior fasciculus (posterior fibers) could be identified in every experimental brain although the termination in the DTN and LTN is somewhat difficult to establish (Fig. 3b). However, because of the close resemblance with the contralateral system we believe these two nuclei are the logical end-stations for this uncrossed pathway also. Silver-Staining

Artifacts

There are many neurons with “cellular deposits” (20, 30) in our silver preparations (Fig. 4). They have been called “granular argyrophilic neurons” (5, 6). Whether these granules are normally occurring or artifactual is a matter of definition and irrelevant here. However, it should be pointed out that such neurons with black granules do not represent axonal degeneration but have probably resulted in misidentification of AOS termination sites in the literature. The case in question is the MTN and substantia nigra to be discussed later. We saw such argyrophilic neurons bilaterally in the substantia nigra, notably its pars compacta, and less frequently elsewhere. They are not degenerating for the following reasons. (i) They physically resemble neurons that were previously well documented (5, 6, 20, 30). (ii) They are

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bilaterally and symmetrically scattered, suggesting artifacts (20, 30). (iii) Solitary examples or patches of such neurons are seen in every brain even long after operation and without any clear sign of accompanying axonal breakdown. (iv) Never are we able to link them with the genuine degeneration present in the main or accessory optic tract. DISCUSSION Nuclear

Components

of Primate

Accessory Optic System

A lateral terminal nucleus has been identified for every mammalian species subject to scrutiny in the recent literature. For some time it was generally considered to be the only terminal nucleus of the primate accessory optic tract (AOT) and hence the term nucleus of the AOT (3,4,11, 33-35). Hendricksonet al. (21) recognized the LTN inM. mulatta although it was abbreviated as NAOT. The Pasiks (33-35) studied the nucleus of the AOT in the same species. However, judging from their texts and figures their nucleus may not coincide with our LTN. At any rate, in contrast to the recently identified dorsal terminal nucleus to be discussed below and for better phylogenetical comparison, the term LTN seems more appropriate. The AOT was shown to terminate also in the DTN in some primates (1, 15, 40, 41), which corresponds closely to the DTN of our rhesus monkeys. In the rhesus, Hendrickson et al. (21) also depicted a hitherto unreported retinal terminal site (their Fig. lD, arrow). Judging by the morphology of the brain section they sketched, this nucleus is the same as our DTN. However, it is likely that this section, lying caudal to the medial geniculate, was taken from the rostra1 superior collicular level, namely, stereotaxic AP 0 or A 0.5 rather than from the pretectal (A 1.5) as they indicated. Fibrous Components

of Primate

Accessory Optic System

Contralateral Distribution. The contralateral projection of the rhesus AOT has also been demonstrated with other procedures. Based on composite information obtained with silver and autoradiographic techniques, Hendrickson et al. (21) reached a conclusion similar to ours, except for the terminology and location as discussed above. Using electron microscopy, Pasik et al. (35) observed degenerating terminals and altered postsynaptic profiles in their nucleus of the AOT after unilateral enucleation. With Nauta technique, Giolli (11) was able to trace the AOT to the LTN (his nucleus of the AOT) in M. cynomolgus. He also noticed termination on the scattered cells in the AOT dorsal to LTN. Whether these

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cells are displaced DTN neurons remains an open question. Similarly dispersed cells were reported in the squirrel monkey (42) even though a DTN was later found in this species (1, 41). It should not be surprising, then, if a DTN is also present in the cynomolgus. Zpsilaterul Distribution. The evidence for an ipsilateral AOT was provided for some infraprimate mammalian species (8, 19, 30, 31). As for primates, based on the work quoted above, Hendrickson et al. (21) stated that the rhesus AOT was composed of “almost completely crossed fibers.” Pasik et al. (35) offered some EM evidence for this ipsilateral projection in the same species. Tigges and O’Steen (41) noted radioactivity in the ipsilateral AOS of the squirrel monkey to be “barely above background” after unilateral intraocular injection of tritiated amino acid. In a similar study on the chimpanzee the presence of an ipsilateral fascicle was mentioned without elaboration (40). Kenny et al. (27) offered evidence that in addition to the contralateral AOS the uncrossed fibers of retinal origin also participate in the regulation of intrapineal serotonin concentration in the cynomolgus. Our monkeys provided morphological support for such a pathway in the primate. Medial

Terminal

Nuclei

and Substantia

Nigra

The term tractus peduncularis transversus has commonly been used interchangeably with the posterior AOT (or posterior fibers of the superior fasciculus, to use Hayhow’s nomenclature), or applied to the fiber bundle stretching superficially under the cerebral peduncle between the LTN and MTN when the posterior AOT does not extend beyond the LTN [for reviews see (10, 11, 13, 16-19, 32)]. The MTN has therefore been called the nucleus of the transpeduncular tract and many other synonyms. Lately this tract refers only to the nonoptic pathway between the LTN and MTN in the monkey (11, 32). It is not certain if a similar tract is present in the rhesus even though this region is said to be sensitive to a visually presented moving target in four monkey species, including rhesus (44). At any rate, we observed no retinal axonal degeneration in this presumed transpeduncular tract, which agrees with other current investigations on primates. It was reported that in Nauta preparations of one siamang gibbon (a primate), after unilateral eye enucleation some degenerating retinal axons entered the cerebral peduncle, dispersed, and were lost (24). “However, there was some evidence of preterminal degeneration in relationship to the substantia nigra of both sides although this was not altogether convincing, since somewhat similar appearance was also seen in the substantia nigra of a normal animal stained by the Nauta method” (24).

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SYSTEM

The Glees method showed severe boutonal degeneration in the substantia nigra of this same experimental gibbon. In another gibbon, EM revealed typical neurofilamentous changes there (24). The authors stated that “. . . if further studies, however, show that there are no such direct projections from the retina to the substantia nigra then, the presence of degenerating boutons showing neurofilamentous changes should be regarded as a normal phenomenon and therefore be taken into account in evaluating the results obtained from degeneration experiments” (24). This is important because it is well known that EM signs of boutonal degeneration can be present in even well-perfused and well-fixed normal central nervous system materials (22). The mammalian MTN is in general situated at the medial edge of the cerebral peduncle near where the N. III rootlets emerge. It abuts against the medial aspect of the substantia nigra. In species such as rodents (8, 19, 30) it is rather extensive and arches over the mediodorsal surface of the substantia nigra. Actual intermingling of MTN and nigral neurons was reported, for instance, in the horse [(26), their Fig. 2D]. It is perhaps only natural because these two structures develop embryologically and phylogenetically from the same gray mass (10) and could work as a functional unit (10, 13). Such close relationship might partly explain the confusion demarcating the accessory optic terminations in these regions. Retinal projections to the substantia nigra were abundantly recorded in earlier literature for various mammals [for reviews see (10, 11, 13, 16- 19, 32)] but only rarely so lately (24) as discussed above. On the other hand the MTN is now commonly believed to receive visual fibers in most nonprimate species but not in any primate. One exception is the report of Sehmsdorf (37), who briefly mentioned the presence of terminal degeneration within the MTN following enucleation in both higher and lower primates. Our data do not support retinal projection to either the MTN or substantia nigra in simians. It should be pointed out that this general region is prone to silver-staining artifacts as noted under Results. As it stands now the overwhelming evidence is against a direct visual input to the MTN in primates; therefore the term medial terminal nucleus (MTN) is a misnomer. The corresponding nuclear region should perhaps be called the nucleus of the transpeduncular tract provided a tract as such can be established for that species. Comparison

between Primate and Nonprimate Accessory Optic Systems

Mammalian

A brief overall comparison without intertwined discussion between the AOS of primates and that of infraprimate species so far reported in the

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current literature points to the following generalities. (i) The MTN is usually the most prominent of the three terminal nuclei in nonprimates, with the LTN being the least conspicuous. The opposite is true with primates, having the LTN as the only obvious end-station whereas the MTN is entirely wanting. (ii) Therefore, it is not unexpected to witness in primates a simultaneous disappearance of the terminal part of the superior fascicle beyond the LTN and the entire inferior fascicle, because both are supposed to terminate within the MTN when present. (iii) Although the DTN is generally ill-defined in all mammals it has changed its relative position from under the medial geniculate (usually its caudal pole) in infraprimates to just caudal to it in primates. One notable exception to the above generalities is seen in some ungulates (excluding the horse) whose AOS is strikingly similar to that of primates in many aspects (25,26). Also, it is interesting to note the complete lack of an AOS in the dolphin (23) and bat (36), observations which if confirmed might be related to their special environmental adaptions. (iv) Even though an ipsilateral AOT so far has been positively identified for only a few mammalian forms, its existence seems independent of the phylogenetic scale. More work is needed to determine if such an uncrossed pathway is indeed a universal occurrence. REFERENCES 1. CAMPBELL, C. B. G. 1969. The visual system of insectivores and primates. Ann. N.Y. Acad. Sci. 167: 388-403. 2. CAMPBELL, C. B. G., AND W. R. HAYHOW. 1972. Primary optic pathways in the duckbill platypus, Ornithorynchus anatinus: an experimental degeneration study.J. Camp.

Neural. 145: 195-208. 3. CAMPOS-ORTEGA, J. A., AND P. F. DE V. CLEAVER. 1968. The distribution of retinal fibers in Galago crassicaudatus. Brain Res. 7: 487-489. 4. CAMPOS-ORTEGA, J. A., AND P. GLEES. 1%7. The subcortical distribution of optic fibers in the Saimiri sciureus (squirrel monkey). J. Camp. Neurol. 131: 131-142. 5. DE OLMOS, J. S. 1%9. Distribution of the granular argyrophilic neurons in normal cat and monkey brains. Anat. Rec. 163: 177-178. 6. DE OLMOS, J. S. 1%9. A cupric-silver method for impregnation of terminal axon degeneration and its further use in staining granular argyrophilic neurons. Brain Behav. Evol. 2: 213-237. 7. DE OLMOS, J. S., AND W. R. INGRAM. 1971. An improved cupric-silver method for impregnation of axonal and terminal degeneration. Brain Res. 33: 523-529. 8. EICHLER, V. B., AND R. Y. MOORE. 1974. The primary and accessory optic systems in the golden hamster, Mesocricetus auratus. Acta Anat. 89: 359-371. 9. GEERAEDTS, L. M. B., AND H. J. LAMMERS. 1%2. An experimental anatomical study of the optic system in the rabbit and the monkey. Acfa Morphol. Neerlando-Stand. 5: 193- 194. 10. GILLILAN, L. A. 1941. The connections of the basal optic root (posterior accessory optic tract) and its nucleus in various mammals. J. Camp. Neurol. 74: 367-408. 11. GIOLLI, R. A. 1963. An experimental study of the accessory optic system in the cynomolgus monkey. J. Comp. Neurol. 121: 89-108.

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12. GIOLLI, R. A. 1965. An experimental study of the accessory optic system and other optic fibers in the opossum, Didelphis virginiana. .I. Camp. Neurol. 124: 229-242. 13. GIOLLI, R. A., J. R. BRAITHWAITE, AND T. T. STREETER. 1968. Golgi study of the nucleus of the transpeduncular tract in the rabbit. J. Comp. Neurol. 133: 309-328. 14. GIOLLI, R. A., AND M. D. GUTHRIE. 1969. The primary optic projections in the rabbit. An experimental degeneration study. .I. Comp. Neural. 136: 99- 126. 15. GIOLLI, R. A., AND J. TIGGES. 1970. The primary optic pathways and nuclei of primates. Pages 29-54, in C.R. NOBACK AND W. MONTAGNA, Eds., The Primate Brain. Appleton-Century-Crofts, New York. 16. HAMASAKI, D. I., AND E. MARC. 1960. A historical review of the accessory optic tracts. Am. J. Optom. 37: 53-66. 17. HAYHOW, W. R. 1959. An experimental study of the accessory optic fiber system in the cat. J. Comp. Neurol. 113: 281-313. 18. HAYHOW, W. R. 1966. The accessory optic system in the marsupial phalanger, Trichosurus vulpecula. An experimental degeneration study. J. Comp. Neurol. 126: 653672. 19. 20.

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HAYHOW, W. R., C. WEBB, AND A. JERVIE. 1960. The accessory optic fiber system in the rat. J. Comp. Neural. 115: 187-216. HEIMER, L. 1970. Selective silver-impregnation of degenerating axoplasm. Pages 106131 in W. J. H. NAUTA AND S. 0. E. EBBESSON, Eds., Contemporary Research Methods in Neuroanatomy. Springer-Verlag, New York. HENDRICKSON, A., M. E. WILSON, AND M. J. TOYNE. 1970. The distribution of optic nerve fibers in Macaca mulatta. Brain Res. 23: 425-427. IBATA, Y., T. DESIRAJU, AND G. D. PAPPAS. 1971. Light and electron microscopic study of the projection of the medial septal nucleus to the hippocampus of the cat. Exp. Neurol. 33: 103- 122. JACOBS, M. S., P. J. MORGANE, AND W. L. MCFARLAND. 1975. Degeneration of visual pathways in the bottlenose dolphin. Brain Res. 88: 346-352. KANAGASUNTHERAM, R., AND A. KRISHNAMURTI. 1971. Eye enucleation and substantia nigra. Acta Anat. 80: 460-464. KARAMANLIDIS, A. N., AND J. MAGRAS. 1972. Retinal projections in domestic ungulates. I. The retinal projections in the sheep and the pig. Brain Res. 44: 127- 145. KARAMANLIDIS, A. N., AND J. MAGRAS. 1974. Retinal projections in domestic ungulates. II. The retinal projections in the horse and ox. Brain Res. 66: 209-226. KENNY, G. C. T., C. J. LOUIS, K. C. BRADLEY, R. McD. ANDERSON,AND N. B. WALDEN. 1973. Effect of optic chiasmotomy upon serotonin concentration in the pineal gland of the monkey. Am. J. Phys. Anthropol. 38: 399-402. LAEMLE, L. K., AND C. R. NOBACK. 1970. The visual pathways of the lorisid Iemurs (Nycticebus coucang and Galago crassicaudatus). J. Comp. Neurol. 138: 49-62. LENT, R., L. A. CAVALCANTE, AND C. E. ROCHA-MIRANDA. 1976. Retinofugal projections in the opossum. An anterograde degeneration and radioautographic study. Brain

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31. LIN, H., AND W. R. INGRAM. 1972. An anterior component of the accessory optic system of the cat, with evidence for the absence of reticuloretinal fibers. Exp. Neural. 32.

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MARC, E. 1973. Neurophysiology of the accessory optic system. Pages 103-111 in R. JUNG, Ed.. Hundbook of Sensory Physiology, VIII3, Central Visual Information. B. Springer-Verlag, New York.

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33. PASIK, P., AND T. PASIK. 1973. Extrageniculostriate vision in the monkey. V. Role of accessory optic system. J. Neurophysiol. 36: 450-457. 34. PASIK, T., AND P. PASIK. 1971. The visual world of monkeys deprived of striate cortex: effective stimulus parameters and the importance ofthe accessory optic system. Vision Res. 3: 419-435 (suppl.). 35. PASIK, T., P. PASIK, AND J. HAMORI. 1973. Nucleus of the accessory optic tract. Light and electron microscopic study in normal monkeys and after eye enucleation. Exp. Neural. 41: 612-627. 36. PENTNEY, R. P., AND J. R. COTTER. 1976. Retinofugal projections in an echolocating bat. Brain Res. 115: 479-484. 37. SEHMSDORF, J. 1969. The nuclear morphology of the accessory optic system. Anat. Rec. 163: 324. 38. SNIDER, R. S., AND J. C. LEE. 1961. A Stereotaxic Atlas of the Monkey Brain (Macaca mulatta). University of Chicago Press, Chicago. 39. THORPE, P. A., AND J. HERBERT. 1976. The accessory optic system of the ferret. .I. Comp. Neural. 170: 295-310. 40. TIGGES, J., J. Bos, AND M. TIGGES. 1977. An autoradiographic investigation of the subcortical visual system in chimpanzee. J. Comp. Neural. 172: 367-380. 41. TIGGES, J., AND W. K. O’STEEN. 1974. Termination of retinofugal fibers in squirrel monkey: a reinvestigation using autoradiographic methods. Brain Res. 79: 489495. 42. TIGGES, J., AND M. TIGGES. 1969. The accessory optic system and other optic fibers of the squirrel monkey. Folia Primat. 10: 245-262. 43. TIGGES, J., AND M. TIGGES. 1969. The accessory optic system inErinaceus (Insectivora) and Galago (primates). J. Comp. Neural. 137: 59-70. 44. WESTHEIMER, G., AND S. M. BLAIR. 1974. Unit activity in accessory optic system in alert monkeys. Invest. Ophthalmol. 13: 533-534.