Roland A. Giolli

The accessory optic system: basic organization with an update on connectivity, neurochemistry, and function.

The accessory optic system (AOS) is formed by a series of terminal nuclei receiving direct visual information from the retina via one or more accessory optic tracts. In addition to the retinal input, derived from ganglion cells that characteristically have large receptive fields, are direction-selective, and have a preference for slow moving stimuli, there are now well-characterized afferent connections with a key pretectal nucleus (nucleus of the optic tract) and the ventral lateral geniculate nucleus. The efferent connections of the AOS are robust, targeting brainstem and other structures in support of visual-oculomotor events such as optokinetic nystagmus and visual-vestibular interaction. This chapter reviews the newer experimental findings while including older data concerning the structural and functional organization of the AOS. We then consider the ontogeny and phylogeny of the AOS and include a discussion of similarities and differences in the anatomical organization of the AOS in nonmammalian and mammalian species. This is followed by sections dealing with retinal and cerebral cortical afferents to the AOS nuclei, interneuronal connections of AOS neurons, and the efferents of the AOS nuclei. We conclude with a section on Functional Considerations dealing with the issues of the response properties of AOS neurons, lesion and metabolic studies, and the AOS and spatial cognition.

GABAergic neurons comprise a major cell type in rodent visual relay nuclei: an immunocytochemical study of pretectal and accessory optic nuclei*

SummaryThe enzyme glutamic acid decarboxylase (GAD) has been localized in sections of rodent brains (gerbil, rat) using conventional immunocytochemical techniques. Our findings demonstrate that large numbers of GAD-positive neurons and axon terminals (puncta) are present in the visual relay nuclei of the pretectum and the accessory optic system. The areas of highest density of these neurons are in the nucleus of the optic tract (NOT) of the pretectum, the dorsal and lateral terminal accessory optic nuclei (DTN, LTN), the ventral and dorsal subdivisions of the medial terminal accessory optic nucleus (MTNv, MTNd), and the interstitial nucleus of the posterior fibers of the superior fasciculus (inSFp). The findings indicate that 27% of the NOT neurons are GAD-positive and that these neurons are distributed over all of the NOT except the most superficial portion of the NOT caudally. The GAD-positive neurons of the NOT are statistically smaller (65.9 μm2) than the total population of neurons of the NOT (84.3 [j,m2) but are otherwise indistinguishable in shape from the total neuron population. The other visual relay nuclei that have been analyzed (DTN, LTN, MTNv, MTNd, inSFp) are similar in that from 21% to 31% of their neurons are GAD-positive; these neurons are smaller in diameter and are more spherical than the total populations of neurons. The data further show that a large proportion of the neurons in these visual relay nuclei are contacted by GAD-positive axon terminals. It is estimated that approximately one-half of the neurons of the NOT and the terminal accessory optic nuclei receive a strong GABAergic input and have been called “GAD-recipient neurons”. Further, the morphology of the GAD-positive neurons combined with their similar distribution to the GAD-recipient neurons suggest that many of these neurons are acting as GABAergic, local circuit neurons. On the other hand, the large number of GAD-positive neurons in the NOT and MTN (20–30%) in relation to estimates of projection neurons (75%) presents the possibility that some may in fact be projection neurons. The overall findings provide morphological evidence which supports the general conclusion that GABAergic neurons play a significant role in modulating the output of the visually related NOT and terminal accessory optic nuclei.

Projections of the medial terminal nucleus of the accessory optic system upon pretectal nuclei in the pigmented rat

SummaryThe projections of the medial terminal nucleus (MTN) of the accessory optic system (AOS) upon pretectal nuclei have been studied in pigmented rats by means of (i) the anterograde transport of 3H-leucine with the use of light autoradiography and (ii) the retrograde transport of horseradish peroxidase (HRP). Injections of 3H-leucine largely restricted to the MTN and minimally involving adjacent ventral midbrain structures, produced heavy terminal axonal labeling within the ipsilateral nucleus of the optic tract (NOT) and the dorsal terminal nucleus (DTN) of the AOS. Terminal labeling was observed in all superficial portions of the NOT, except for a small ventromedial segment in the rostral two thirds and a larger medial segment in the caudal one third of this nucleus. Thus the MTN-NOT projections we describe entirely overlap the retinal-NOT projection and partially overlap the visual cortical-NOT, as reported by others. Within the DTN, the dense terminal fields covered the entire nucleus.After postinjection survival times of 3–7 days, the pattern of axonal labeling showed that the MTNNOT projection consisted of three bundles: (i) a superficial mesencephalic bundle coursing within the superior fasciculus, posterior fibers of the AOS which enters the caudal portions of the NOT and the DTN; (ii) a deep mesencephalic bundle that traversed the midbrain tegmentum dorsolaterally, also reaching the caudal one-half of the NOT and all of the DTN; and (iii) a mesodiencephalic bundle that passed first laterally through midbrain tegmentum and then dorsally through lateral thalamus to enter the rostral one-half of the NOT.Pretectal injections of HRP that invade the NOT and DTN produced retrograde labeling of most (ca. 75%) of the neurons of the ipsilateral MTN, without labeling the adjacent substantia nigra or ventral tegmental area. This finding confirms our autoradiographic data by showing that the MTN provides the major, ventral tegmental projection to the NOT and DTN. The present finding of a MTN-NOT projection, combined with available anatomical and physiological data, suggests that the MTN may play a more significant role in visual-vestibular aspects of oculomotor control than formerly thought.

Retinogeniculostriate projections in guinea pigs: Albino and pigmented strains compared

Abstract The retinogeniculate fibers and geniculocortical projections of pigmented and albino guinea pigs were studied by anatomical degeneration methods and by electrophysiological techniques. In one experiment, an eye was enucleated from each of six pigmented and six albino animals. Six to δ days later the animals were killed and the crossed and uncrossed retinal projections to the dorsal lateral geniculate nuclei studied in serial sections prepared by the Nauta silver method. An organized uncrossed retinogeniculate projection was invariably present in the pigmented guinea pig but was not seen in the albino. There was a consistency in the pattern of the crossed retinogeniculate projections among the pigmented guinea pigs but not among the albino animals. Between ocular enucleation and histological analyses, visually evoked responses at the cerebral cortex were recorded. Indications of an input to the striate cortex via noncrossing fibers were found only in the pigmented strain. A relatively consistent pattern of input to the contralateral striate cortex was observed in the pigmented guinea pigs, while several patterns were seen in the albinos.

Cortical and subcortical afferents to the nucleus reticularis tegmenti pontis and basal pontine nuclei in the macaque monkey

Anatomical findings are presented that identify cortical and subcortical sources of afferents to the nucleus reticularis tegmenti pontis (NRTP) and basal pontine nuclei. Projections from the middle temporal visual area (MT), medial superior temporal visual area (MST), lateral intraparietal area (LIP), and areas 7a and 7b to the basal pontine nuclei were studied using 3H-leucine autoradiography. The results complemented a parallel study of retrograde neuronal labeling attributable to injecting WGA-HRP into NRTP and neighboring pontine nuclei. Small 3H-leucine injections confined to MT, MST, LIP, area 7a, or area 7b, produced multiple patches of pontine terminal label distributed as follows: (1) An injection within MT produced terminal label limited to the dorsolateral and lateral pontine nuclei. (2) Injections restricted to MST or LIP showed patches of terminal label in the dorsal, dorsolateral, lateral, and peduncular pontine nuclei. (3) Area 7a targets the dorsal, dorsolateral, lateral, peduncular, and ventral pontine nuclei, whereas area 7b projects, additionally, to the dorsomedial and paramedian pontine nuclei. Notably, no projections were seen to NRTP from any of these cortical areas. In contrast, injections made by other investigators into cortical areas anterior to the central sulcus revealed cerebrocortical afferents to NRTP, in addition to nuclei of the basal pontine gray. With our pontine WGA-HRP injections, retrograde neuronal labeling was observed over a large extent of the frontal cortex continuing onto the medial surface which included the lining of the cingulate sulcus and cingulate gyrus. Significant subcortical sources for afferents to the NRTP and basal pontine nuclei were the zona incerta, ventral mesencephalic tegmentum, dorsomedial hypothalamic area, rostral interstitial nucleus of the medial longitudinal fasciculus, red nucleus, and subthalamic nucleus. The combined anterograde and retrograde labeling data indicated that visuo-motor cortico-pontine pathways arising from parietal cortices target only the basal pontine gray, whereas the NRTP, together with select pontine nuclei, is a recipient of afferents from frontal cortical areas. The present findings implicate the existence of parallel direct and indirect cortico-pontine pathways from frontal motor-related cortices to NRTP and neighboring pontine nuclei.

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.

A Review of Axon Collateralization in the Mammalian Visual System

Axon collateralization appears to represent a prominent feature of the mammalian visual system. Both anatomical and electrophysiological evidence reveal that axon branching occurs in the retinofugal, geniculocortical and visual corticifugal projections. Most of this evidence is provided by studies on the cat, but enough data are available from investigations on the rat and monkey to permit certain interspecies differences to be recognized and evaluated. Axon branching allows individual axons to provide innervation to two or more targets and generally to transmit the same type of visual information to these targets. There is abundant evidence to suggest that two of the three functional classes of retinal ganglion cells and geniculate relay cells (namely Y and W ganglion and relay cells) utilize axon branching; however, few details regarding this subject are currently available. The third functional class of ganglion and relay cells (X ganglion and relay cells) essentially lacks axon branches. This review has three primary goals: (1) to review the pertinent anatomical and electrophysiological literature dealing with axon branching and to discuss areas in which information is meager and further investigation necessary; (2) to emphasize the need for applying recently developed techniques, such as double-labeling of neurons and electrical collision, to the study of axon collateralization, and (3) to formulate some hypotheses concerning the functional significance of axon branching.

Accessory optic system of rhesus monkey

Abstract 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 Niss 1 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.

The anatomical organization of the visual system of the rabbit

Contrary to the belief held by some (e.g., CANKOVIC, 1968) the optic chiasma of the rabbit is not complete. An uncrossed fiber component exists, which however small, must be considered. In studies utilizing the Marchi method, BROUWER (1923) has shown this component to arise from the extreme temporal margin of the retina. Furthermore, THOMPSON and co-workers (1950) have photically stimulated the eye of the rabbit and demonstrated that the temporal margin of the retina projects ipsilaterally rather than contralaterally in the brain. A similar finding has been reported in the rat utilizing both the Marchi method (LASHLEY, 1934) and electrophysiological techniques (MONTERO et al., 1968). Caudal to the optic chiasma the fibers of the uncrossed component are randomly distributed within the optic tract. As considered in appropriate sections to follow, these fibers terminate in localized segments of the lateral geniculate nuclei, pretectal nuclei and superior colliculus.

The medial terminal nucleus of the monkey: evidence for a ‘complete’ accessory optic system

The retinal projection to the medial terminal nucleus of the accessory optic system of the monkey was examined in several primate species which had received intraocular injections of [3H]proline or [3H]fucose. These data show that the medial terminal nuclei of the slow loris, marmoset monkey, and squirrel monkey all receive a sparse input from the contralateral retina.