The human accessory optic system

The accessory optic system (AOS) has been extensively studied among vertebrates, including primates. It has never clearly been identified in man, and it has not been considered functionally important by clinicians. Because of a lack of a suitable neuroanatomical tract-tracing technique, anatomical demonstration of a retinofugal pathway to the human AOS had previously not been feasible. A modified osmium impregnation method has been shown to permit the tracing of degenerated fibers in man even after long survival periods. This technique employs p-phenylene diamine (PPD) as a marker of myelin and products of axonal degeneration. We applied the PPD method in the examination of one monkey brain (Cynomolgus) and two human autopsy brains with previous visual system lesions. The lateral, dorsal, and medial terminal accessory optic nuclei and the interstitial nucleus of the superior fasciculus, posterior fibers (LTN, DTN, MTN, and inSEp) in the monkey and the LTN, the DTN, and the inSEp in the human all showed degenerated axons and preterminal axonal profiles indicative of direct retinal input. The ventral midbrain tegmentum including the MTN area was not available for study in either of the human brains. The accessory optic projections in both the monkey and human brains proved to be bilateral but primarily crossed. The human visual system thus shares similarities with the simian, in the location and number of the AOS fiber bundles and terminal nuclei and in the organization of the retinofugal projections to these nuclei.     

The accessory optic system of the ferret.

The accessory optic system of the ferret has been studied both by silver degeneration staining and by autoradiography after intraocular 3H leucine injections. There is no anterior accessory optic tract but a posterior tract containing only crossed fibres leaves the brachium of the superior colliculus and ends in the two nuclei, the medial and lateral terminal nuclei, lying either side of the cerebral peduncle. Both suprachiasmatic nuclei receive retinal fibres visible only on autoradiographs; most fibres end in the contralateral nucleus. No other area in the hypothalamus appears to receive retinal fibres demonstrated by these methods.     

The accessory optic system of the monocularly deprived cat

Single-unit extracellular recordings were made in the lateral (LTN) and dorsal (DTN) terminal nuclei of the accessory optic system (AOS) of 10 monocularly deprived cats. The separate effects of monocular deprivation (MD) observed in each hemisphere are outlined below. Unlike many units in normal animals, LTN and DTN cells in the hemisphere contralateral to the non-deprived (open) eye, were no longer activated through visual stimulation of the ipsilateral (deprived) eye. In both nuclei, cells were driven effectively only by stimuli presented via the contralateral eye. The distribution of preferred directions was considerably altered in the LTN but not in the DTN. Almost every LTN unit encountered in MD cats preferred downward stimulus motion, in contrast to normal animals where equal numbers of LTN cells show preferences for upward and downward movement (J. Neurophysiol., 51 (1984) 276-293). DTN units showed the usual preference for horizontal motion toward the recorded hemisphere. Velocity preferences were slower on average in the DTN, and unaffected in the LTN. In the hemisphere contralateral to the deprived eye, the ocular dominance distribution of LTN and DTN cells showed a distinct shift in favor of the contralateral (deprived) eye. This effect was not as complete as that observed in the other hemisphere. Cells in both nuclei displayed a small influence from the ipsilateral (exposed) eye in some animals, but this input was much less than that observed in normally reared cats. Average velocity preferences among DTN units were slower than normal, and slower relative to the DTN population in the opposite hemisphere. No pronounced changes were observed in LTN velocity tuning. The distributions of preferred directions for both nuclei were similar to those obtained in the other hemisphere: DTN cells were found to prefer horizontal motion, while most LTN units were activated best by stimuli moving vertically and down within their receptive fields.     

Gliogenesis in the embryonic avian optic tectum: neuronal-glial interactions influence astroglial phenotype maturation

We have analyzed the development of neuroglial cells in the chick optic tectum under 3 sets of developmental conditions to assess the role of heterotypic cell-cell interactions in gliogenesis. Immunochemical and biochemical methods were employed to measure and localize the expression of the glial markers glutamine synthetase, glial fibrillary acidic protein, S-100 protein, carbonic anhydrase-C and myelin basic protein as functions of development in situ and in aggregation and monolayer cultures of dissociated embryonic tissue. The results showed that certain astroglial cells can be recognized as early as day 9 of development in situ. Oligodendroglial development manifests several days later and the full range of glial subtypes are not evident until nearly the time of hatching. Culture of 7-day embryonic tectum cells either in aggregates or in monolayer cultures failed to yield definitive oligodendroglia. Fibrous astroglia, as defined by glutamine synthetase and glial fibrillary acidic protein, developed well in both culturing systems. However, as previously noted in the embryonic neural retina system, glutamine synthetase expression was marked dependent on neuronal-glial associations.     

Pretectal complex and accessory optic system of primates

In the present report, conflicting results regarding the pretectal complex and accessory optic system of primates are discussed. Subsequently data are presented and used in an attempt to clarify some of the issues. The retinal projections to the pretectal complex and accessory optic system of the tree shrew and squirrel monkey were examined using anterograde autoradiographic methods. These data demonstrate that, following intraocular injections of 3H-proline or 3H-fucose in the tree shrew, silver grains are apparent bilaterally over the pretectal olivary nucleus and the anterior and posterior pretectal nuclei and contralaterally over the nucleus of the optic tract. Following intraocular injections of the 3H-tracer in squirrel monkeys, dense transported label is observed bilaterally over the pretectal olivary nucleus and the nucleus of the optic tract with sparse label over the posterior and medial pretectal nuclei. In both the tree shrew and squirrel monkey, a differential retinal projection is observed, chiefly contralaterally, to all accessory optic terminal nuclei (i.e., the dorsal, lateral and medial terminal nuclei).     

Anuran accessory optic system: evidence for a dual organization

The accessory optic system of Rana pipiens consists of lateral and medial fascicles of the basal optic root (BOR1, BORm) and a single terminal nucleus, nBOR. The present study provides new evidence that these two fascicles differ not only in their trajectories but in fiber spectra and innervation patterns as well. BOR1 contains a substantially higher percentage of large, myelinated axons than does BORm, and the mean diameter of axons in BOR1 is greater than that of BORm. BOR1 innervates the entire terminal field of nBOR, while BORm innervates only the central and mediodorsal portions of nBOR. The ventrolateral portion of nBOR is uniquely innervated by BOR1 and contains several types of neurons not found in the central and medial regions of nBOR which are innervated by both fascicles. Cytoarchitectural analysis of nBOR with Golgi techniques has revealed a number of similarities between the anuran nBOR and the mammalian medial terminal nucleus (MTN) with regard to cellular morphology, dendritic geometry, and retinofugal arborization patterns. In frog, nBOR appears comparable to the ventral subdivision of the mammalian MTN, while the peri-nBOR region, which contains neurons postsynaptic to nBOR, may represent a more primordial version of the mammalian dorsal MTN.     

Displaced ganglion cells and the accessory optic system of pigeon

The central projection and retinal distribution of displaced ganglion cells (DGC's) are described for the pigeon. Discrete, localized injections of horseradish peroxidase (HRP) into the nucleus of the basal optic root (nBOR) complex labeled as many as 4,800 DGC's in the contralateral retina. The greatest densities of DGC's were observed in the more peripheral regions of the middle and inferior temporal regions of the retina, with lowest densities occurring in the inferior nasal, red field, and foveal areas. Large HRP injections of the tectal lobes, which did not include the pretectal, accessory optic (nBOR), hypothalamic, or thalamic visual nuclei, labeled only ganglion cells within the ganglion cell layer. An HRP injection centered within the nucleus lentiformis mesencephali, also including portions of the optic tectum and optic tract, labeled only ganglion cells within the ganglion cell layer of the contralateral retina. DGC's thus appear to be the primary, if not exclusive, source of retinal afferents to the nBOR complex in pigeon. The observed retinal distribution of DGC's indicates that the areas of retina with the greatest density of cells in the receptor layer, inner nuclear layer, and ganglion cell layer are relatively devoid of DGC's. Since the nBOR complex projects directly upon the vestibulocerebellum and oculomotor nuclei, DGC's would thus appear to be involved in neural circuits that mediate oculomotor reflexes and visuomotor behavior.     

The accessory optic system of rodents: a whole-mount HRP study

The three-dimensional fiber pathways of the accessory optic system in three species of rodents (rat, golden hamster, guinea pig) were examined on whole-mounted preparations of the diencephalon and the midbrain, without sectioning, by anterograde labeling of retinal axons with horseradish peroxidase (HRP). HRP histochemical studies on the serial coronal sections were also done. In this study, only the accessory optic system on the side contralateral to the eye injection of HRP was clearly detected. The rat accessory optic system consisted of the inferior fasciculus, the superior fasciculus, the medial terminal nucleus, the lateral terminal nucleus, and the dorsal terminal nucleus. After the inferior fasciculus arrived at the ventromedial border of the cerebral peduncle, some fibers from the inferior fasciculus ran caudally to the medial terminal nucleus. The remaining fibers from the inferior fasciculus further proceeded dorsocaudally on the surface of the cerebral peduncle and left the inferior fasciculus at various levels of the cerebral peduncle to be mixed up with the fibers from the superior faciculus. The golden hamster accessory optic system also consisted of the inferior fasciculus, the superior fasciculus, the medial terminal nucleus, the lateral terminal nucleus, and the dorsal terminal nucleus. However, all fibers of the inferior fasciculus ran caudally on the lateral surface of the hypothalamus or along the ventromedial border of the cerebral peduncle to terminate at the medial terminal nucleus. The guinea pig accessory optic system and rat accessory optic system were similar, but the posterior fibers of the superior fasciculus decreased in number, and the dorsal terminal nucleus and the posterior portion of the lateral terminal nucleus were not observed in the guinea pig accessory optic system.     

Ganglion cells of the cat accessory optic system: Morphology and retinal topography

The ganglion cells of the cat's retina form classes that are distinct in their cell morphology, retinal distribution, central projections, and functional properties. By means of the retrograde transport of horseradish peroxidase injected into the accessory optic nuclei of the cat midbrain, we have characterized the retinal ganglion cells projecting to these nuclei. The retinal projection is virtually completely crossed to the medial terminal nucleus and to the lateral terminal nucleus. This appears to be true for the dorsal terminal nucleus as well, although difficulties of the technique limit our findings for this region. No differences were found in either the spatial distribution, or the somal size distribution, or the morphological characteristics of the ganglion cells projecting to these three nuclei. In spatial distribution, these cells are concentrated in the area centralis and visual streak and show no evidence of a nasotemporal divison. Morphologically, they have small to medium-sized somas and delicate, sparsely branching dendrites. They do not appear to belong to any of the morphological cell types thus far identified.     

Macaque accessory optic system: I. Definition of the medial terminal nucleus

The organization of the accessory optic system (AOS) has been studied in the macaque monkey following intravitreal injections of tritiated amino acids in one eye. Retinal projections to the dorsal (DTN) and the lateral (LTN) terminal nuclei are identical to those previously described in other primate species. We observed an additional group of retinorecipient cells of the AOS, located between the cerebral peduncle and the substantia nigra, which we define as the interstitial nucleus of the superior fasiculus, medial fibers. In this report, we focus our attention on the medial terminal nucleus (MTN). Although a ventral division of this nucleus (MTNv) was not observed in the macaque, the retina projects to a group of cells in the midbrain reticular formation (MRF), which we argue to be homologous to the dorsal division of the MTN (MTNd). To provide evidence in support of this homology, the retinal projection to the MTNv and MTNd was also examined in 21 additional species from 11 orders of mammals including carnivores, marsupials, lagomorphs, rodents, bats, insectivores, tree shrews, hyraxes, pholidotes, edentates, and five additional species of primates. Whereas the retina projects to both ventral and dorsal divisions in all species studied, in haplorhine primates only the projection to the MTNd is conserved. The relative topological position of the MTNd in the MRF, dorsomedial to the substantia nigra and ventrolateral to the red nucleus, remains constant throughout the mammals. The trajectory of fiber paths innervating the MTNd is also similar in all species. In addition, the MTNd has comparable afferent and efferent connections with retina, pretectum, and vestibular nuclei in all species thus far studied. These results support the unequivocal conclusion that the MTNd is an unvarying feature of the mammalian AOS.     

Retinal ganglion cells projecting to the rabbit accessory optic system

Recent evidence from extracellular recording studies indicates that the medial terminal nucleus (MTN) of the rabbit accessory optic system receives inputs from a particular functional class of retinal ganglion cells—specifically, the on-type direction-selective cells. These ganglion cells have been selectively labeled by the retrograde transport of horseradish peroxidase (HRP) injected into the MTN. The number of labeled cells, their distribution over the retina, and their soma areas were determined. In one animal in which the HRP injection completely filled the nucleus, two thousand ganglion cells were labeled. This number agrees with previous estimates of the number of retinal axons terminating in the MTN. Unlike results in avians, none of the ganglion cells was displaced—i.e., they were not Dogiel cells. The density of labeled cells was highest in the visual streak and, overall, the distribution of labeled cells corresponded to the physiologically determined distribution of on-type direction-selective cells. Cells labeled by the HRP injection were among the 20% largest cells in the retina. This result, in conjunction with conclusions from other studies, leads to the prediction that on-type direction-selective cells can be characterized morphologically as cells with large cell bodies and a very extensive dendritic spread in which the dendrites ramify in the vitreal sublamina of the inner plexiform layer.     

The accessory optic system and the retino-hypothalamic system. A review.

The introduction of new techniques in neuroanatomy has helped to clarify a number of important issues on the nature of the accessory optic and retino-hypothalamic system. In this study, an effort was made, to collect all data obtainable, and to arrange them on the basis of some common parameter, so that the various results may be directly compared. These data were then interpreted on specific issues, although only limited coverage has been given to functional aspects, as described in older publications. The absence of a universally accepted concept of the function of both systems to date suggests the need for a thorough analysis of both contemporary and older literature dealing with a characterization of the structural components of the accessory optic and the retino-hypothalamic systems. On the basis of these anatomical studies it is concluded that the accessory optic system (AOS) is much more complex than formerly believed. Its development in various vertebrae classes is quite different. Among the mammals, the AOS is very well established in rodents but in primates and man its anatomical and functional role seems markedly reduced. In the rodents it consists of both superficially and deeply arranged axons which are in close topical relation to the cerebral peduncles. The axons not only supply the classic accessory otpic terminal nuclei but also the subthalamic nucleus and the substantia nigra. The secondary projections have not yet been established. The retino-hypothalamic system (RHS) mainly but not exclusively supplies the suprachismatic nucleus (sc). Crossed as well as uncrossed retinal fibres project to the ventro-lateral and to the posterior part of this nucleus. The cells within the sc combine both secretory and neuronal properties. The possible functions exerted are discussed. Both, the AOS and the RHS, are so closely related within the suprachiasmatic area that most methods fail in correlating experimental results with either system. The numerous problems which still remain to be clarified are also discussed.     

Development of the meninges of the human embryonic optic nerve

From 8 to 14 weeks post-conception the human embryonic optic nerve is surrounded by loosely packed layers of connective tissue. From 8 weeks onwards the innermost layers of this sheath consist of fibroblast-like cells whereas the cells of the middle and outer layers, although similar in appearance, contain increasing amounts of glycogen, until by 14 weeks very large amounts of glycogen are present in these cells. A collagen-rich dural layer first appears at 15 weeks post-conception. This layer contains few cells. The outer-most cells have the appearance of fibroblasts and are joined to each other by long sheet-like processes. Cell in the middle of the dura are glycogen-containing cells, apparently actively engaged in collagen production. These cells are similar to those found in the adjacent arachnoid. By 18 weeks of age the meninges are well-differentiated. The endothelial cells of all capillaries found in the meninges from 8 weeks post-conception, including dural capillaries, are sealed by zonulae occludentes. At 15 and 18 weeks a few fenestrated capillaries were observed at the junction of the dura and the surrounding loose connective tissue. Peripheral nerves are closely related to the meninges from 8 weeks post-conception and peripheral nerve bundles are present in the dura from 15 weeks. At 18 weeks the first signs of myelination were observed in these bundles.     

The accessory optic system and temporal correlates of visuomotor orientation

Surgical transection of the basal optic root in Rana pipiens leads to substantial increases in prey-orientation latencies for stimuli presented in the contralateral visual field. In general, the greater the reduction in retinal innervation of nBOR, the greater the postoperative increase in prey-orientation latencies. The results support Herrick's earlier suggestion that the accessory optic system may be substantially involved in early activation and temporal modulation of visuomotor behaviors mediated via mesencephalic circuits.     

Optokinetic nystagmus and the accessory optic system of pigeon and turtle.

Optokinetic nystagmus (OKN) response functions were obtained in pigeon (Columba livia) and turtle (Chrysemys picta) before and after electrolytic lesions of the accessory optic nuclei (AON). Postlesion retinal input to the AON was evaluated using standard autoradiographic techniques. Bilateral destruction of AON in both pigeon and turtle did not abolish OKN, but was correlated instead with a reduction in OKN frequencies at high pattern velocities. A difference was observed between species with respect to the effects of partial lesions. Incomplete destruction of AON produced no observable change in OKN response functions in pigeon, but correlated with reduced OKN response functions in turtle. These results suggest that the AON mediate a portion of OKN in both pigeon and turtle, particularly at high pattern velocities, but are not essential for its occurrence.