Classes Of Retinal Ganglion Cells Research Articles

Parallel Processing in the Visual Systems: The Classification of Retinal Ganglion Cells and Impact on the Neurobiology of Vision

This volume, which is one in a series onPerspective in Vision Research, is an authoritative and comprehensive text that traces the development of our knowledge of retinal ganglion cells, receptive fields, and the overall development of the visual system. Part I includes three chapters that pertain to the classification of retinal ganglion cells. The material includes studies of the conduction velocity groupings among optic nerve axons, the receptive fields of retinal ganglion cells, and the morphology of retinal ganglion cells. Part II contains two chapters on the methodology of classification, while part III contains seven chapters on the impact of ganglion cell classification. The text is detailed and mainly relevant to readers who already have some background in visual system function and anatomy. However, it has individual sections that will be informative to the casual reader with a more comprehensive appreciation of the evolutionary development in our understanding of

Taxonomy of vision

Parallel Processing in the Visual System: The Classification of Retinal Ganglion Cells and its Impact on the Neurobiology of Vision. By Jonathan Stone. Plenum: 1983. Pp.438. 55, 42.35.

The Neurobiology of Vision: Parallel Processing in the Visual System . The Classification of Retinal Ganglion Cells and Its Impact on the Neurobiology of Vision. Jonathan Stone. Plenum, New York, 1983. xvi, 438 pp., illus. $55. Perspectives in Vision Research.

The Neurobiology of Vision: <i>Parallel Processing in the Visual System</i> . The Classification of Retinal Ganglion Cells and Its Impact on the Neurobiology of Vision. Jonathan Stone. Plenum, New York, 1983. xvi, 438 pp., illus. $55. Perspectives in Vision Research.

The Neurobiology of Vision: Parallel Processing in the Visual System . The Classification of Retinal Ganglion Cells and Its Impact on the Neurobiology of Vision. Jonathan Stone. Plenum, New York, 1983. xvi, 438 pp., illus. $55. Perspectives in Vision Research.

The Neurobiology of Vision: <i>Parallel Processing in the Visual System</i> . The Classification of Retinal Ganglion Cells and Its Impact on the Neurobiology of Vision. Jonathan Stone. Plenum, New York, 1983. xvi, 438 pp., illus. $55. Perspectives in Vision Research.

Development of the retinal pathway to the pretectum of the cat

The development of retinal projections to the pretectal complex of prenatal and early postnatal cats has been examined using the anterograde transport of horseradish peroxidase and tritiated amino acids. As early as embryonic day 38, the entire dorsal pretectum is penetrated by retinal ganglion cell axons. At this stage the bilateral complement of retinal efferents appears to be dispersed uniformly within the pretectal anlage. A week later, on embryonic day 46, indistinct foci of peroxidase reaction product can be discerned within 2 of the primordial nuclei: the nucleus of the optic tract and the olivary nucleus. By embryonic day 56, five distinct bilateral fields of retinal fiber termination are apparent within the following regions: (i) the nucleus of the optic tract; (ii) the pretectal olivary nucleus; (iii) the posterior pretectal nucleus; (iv) the anterior pretectal nucleus; and (v) the medial pretectal nucleus. Four days before birth, on embryonic day 61, crossed and uncrossed retinal arbors are partially segregated within the nucleus of the optic tract and the pretectal olivary nucleus. The early postnatal retinal connection to the pretectum has an overall pattern virtually indistinguishable from that of the mature cat. The ontogeny of the retinal influx to the pretectum is similar to that of the retinocollicular projection. 61 However, the development of retinal projections to the pretectum and superior colliculus appears to lag behind those to the dorsal lateral geniculate nucleus. 49 These differences may reflect temporal and spatial gradients in the maturation of three major classes of retinal ganglion cells.

An analysis of axon caliber within the optic nerve of the cat: evidence of size groupings and regional organization

Axon size in the optic nerves of three adult cats was measured using an accurate planimetric method. A sample of the axon complement was obtained from sets of more than 125 electron micrographs taken at each nerve. In contrast to previous reports, the distribution of axon diameter, as estimated from measurements of axonal cross-sectional area was clearly bimodal. The group of finest axons had a mode at approximately 1 micrometer, and the mode of the group of intermediate size axons was approximately 2 micrometers. Fibers with diameters larger than 3.5 micrometers formed the extensive tail of the distribution. The proportions of large, intermediate, and small axons were estimated to be 5%, 45%, and 50%. These groups probably correspond to the alpha, beta, and gamma classes of retinal ganglion cells. Regional distributions of axon caliber were also bimodal and, in a few instances, even trimodal. A peripheral crescent of each nerve contained a large number of fine fibers. Mean fiber diameter within discrete regions of the optic nerve varied inversely with the density of axon packing. The thickness of the myelin sheath was highly correlated with the inner fiber diameter, hence, myelin sheath width was also distributed in a bimodal manner. These results furnish the first clear evidence that the distribution of fiber caliber within the cat's optic nerve mirrors the principal classes of retinal ganglion cells.

Retinal ganglion cell projections to individual layers of the lateral geniculate body in Galago crassicaudatus

The genus Galago provides an unique opportunity to study the relation between layers of the lateral geniculate body and classes of retinal ganglion cells. In the present experiments HRP was restricted to individual layers of the lateral geniculate body with the following results: After injections of the magnocellular layers, layers 1 and 2, labeled retinal ganglion cells ranged in size from 8 to 20 micrometers. After injections of the parvocellular layers, layers 3 and 6, labeled retinal ganglion cells ranged in size from 6 to 12 micrometers. After injections involving layers 4 and 5, which layers contain only very small, pale cells, labeled retinal ganglion cells ranged in size from 5 to 14 micrometers. Thus, the very largest ganglion cells were labeled only after injections of magnocellular layers 1 and 2, while small and medium retinal ganglion cells were labeled after HRP injections in every layers of the lateral geniculate body. Because the magnocellular layers actually contain a mixture of large, medium, and small-sized cells, we suggest that retinal ganglion cells of different size-classes project to geniculate relay cells of the corresponding size-class.

Aspartate may be an excitatory transmitter mediating visual excitation of ‘sustained’ but not ‘transient’ cells in the cat retina: Iontophoretic studies in vivo

Although the excitatory amino acids, aspartate and glutamate are present in large quantities in the layers of the mammalian retina where the bipolar and amacrine cells make contact with the retinal ganglion cells, it was not known whether these amino acids are the actual neurotransmitters which excite the retinal ganglion cells. To answer this l-aspartate, l-glutamate and the recently discovered powerful and selective antagonist for the N-methyl- d-aspartate receptor, 2-amino-5-phosphonovalerate, were applied iontophoretically to the ‘sustained’ and the ‘transient’ classes of retinal ganglion cells in the optically intact eye of anaesthetised cats. The visually-driven excitation of all ‘sustained’ cells was significantly suppressed by 2-amino-5-phosphonovalerate, whereas that of ‘transient’ cells was not. l-aspartate enhanced the visually-driven excitation and increased the spontaneous firing rare of all ‘sustained’ cells but not of ‘transient’ cells and these effects were blocked by 2-amino-5-phosphonovalerate. The results with l-glutamate were inconclusive. It is suggested that l-aspartate may be an excitatory transmitter mediating the visual response at the receptor field centre of ‘sustained’ retinal ganglion cells, but that excitation of ‘transient’ retinal ganglion cells is mediated by a different transmitter.

Spatial summation and contrast sensitivity of X and Y cells in the lateral geniculate nucleus of the macaque.

Study of parallel processing in the visual pathway1 of the cat has revealed several classes of retinal ganglion cells which are physiologically distinct and which project to various locations in the brain2,3. Two classes have been studied most extensively: X cells, which sum neural signals linearly over their receptive fields, and Y cells, in which the spatial summation is nonlinear1,4. In the cat's lateral geniculate nucleus (LGN) cells also can be classified as X or Y, a result of the parallel projection of retinal X and Y inputs to different geniculate neurones5–9. We report here our study of parallel signal processing in the LGN of the macaque monkey. We find that (1) monkey LGN cells can be classified as X or Y on the basis of spatial summation; (2) X-like cells are found in the four parvocellular and the two magnocellular laminae, whereas Y-like cells are found almost exclusively in the magnocellular laminae; and (3) the cells of the magnocellular laminae have high sensitivity and the parvocellular cells low sensitivity for homochromatic patterns. This implies that in macaque monkeys the magnocellular cells and their cortical projections may be the neural vehicle for contrast vision near threshold. The cells of the parvocellular laminae seem to be primarily concerned with wavelength discrimination and patterns of colour. As the human visual system is similar to that of the macaque in structure and behavioural performance, our findings are probably also applicable to man.

Relation of brightness to threshold for light-adapted and dark-adapted rods and cones: effects of retinal eccentricity and target size.

'Equal-brightness' functions of retinal eccentricity and target diameter were measured by a matching procedure, and compared with the corresponding threshold functions for four different adaptation conditions: light-adapted cones (LAC), dark-adapted cones (DAC), light-adapted rods (LAR) and dark-adapted rods (DAR). The separation between log brightness matches and log thresholds decreased with eccentricity and increased with target size for all adaptation conditions, but overall separation was substantially greater for the DAR condition than for the other three. A two-channel model of achromatic brightness is proposed to explain the results. The model assumes 'strong' and 'weak' channels, which contribute unequally to brightness. These channels are tentatively identified with tonic and phasic classes of retinal ganglion cells.

Localization of α-bungarotoxin binding sites to the goldfish retinotectal projection

The optic tectum of the goldfish Carassius auratus is a rich source of α-bungarotoxin (α-Btx) binding protein. In order to determine whether some fraction of these receptors is present at retinotectal synapses, we have compared the histological distribution of receptors revealed by the use of [ 125Iα-Btx radioautography to the distribution of optic nerve terminals revealed by the use of cobalt and horseradish peroxidase (HRP) techniques. The majority of α-Btx binding is concentrated in those tectal layers containing primary retinotectal synapses. The same layers contain high concentrations of acetylcholinesterase (AChE), revealed histochemically. Following enucleation of one eye, there is a loss of α-Btx binding in the contralateral tectum, observed both by radioautography and by a quantitative binding assay of α-Btx binding. Approximately 40% of the α-Btx binding sites are lost within two weeks following enucleation. By contrast, no significant change in AChE activity could be demonstrated up to 6 months enucleation. These results are discussed in light of recent studies which show that the α-Btx binding protein and the nicotinic acetylcholine receptor are probably identical in goldfish tectum. We conclude that the 3 main classes of retinal ganglion cells projecting to the goldfish tectum are nicotinic cholinergic and that little or no postdenervation hypersensitivity due to receptor proliferation occurs in tectal neurons following denervation of the retinal input.

The retinal projection to the superior colliculus in the cat: a quantitative study with HRP.

The projections of cat retinal ganglion cells to the superior colliculus (SC) were examined using the method of retrograde axonal transport of horseradish peroxidase (HRP). Several injections of HRP were made in a single SC after the visual projection to the injection sites had been established physiologically. The HRP injections resulted in a homogeneous distribution of labelled ganglion cells in whole mount preparations of the retinae of both eyes. In the eye contralateral to the injected colliculus, ganglion cells with a crossed projection were labelled in both nasal and temporal retina; in the ipsilateral eye, ganglion cells with uncrossed projection were labelled only in the temporal retina. Analysis of the counterstained retinal whole mounts indicated that at least 50% of all ganglion cells in the nasal retina and 26% in the temporal retina have crossed projection to SC, and that 24% of all ganglion cells of the temporal retina have an uncrossed projection to the SC. The morphological classes of retinal ganglion cells have different patterns of crossed/uncrossed decussation and they participate in varying proportions in the retino-tectal projection. Almost all Alpha cells in the retina send axon collaterals to the SC. Probably only about 10% of the Beta cells project to the SC and at least 80% of all Gamma cells send axons to the SC.

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.

Retinal ganglion cells and optic decussation of white cats

A suspected relation between pigment production and the physiology of visual pathways was examined in white cats with two yellow eyes, two blue eyes or one blue and one yellow. These animals had the same classes of retinal ganglion cells as ordinary pigmented cats. The conduction latencies of their optic axons were also grouped in the same pattern. The retinal distribution of ganglion cells having crossed and uncrossed axons conformed to the patterns described for ordinary pigmented cats.

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.

A specific projection of retinal displaced ganglion cells to the nucleus of the basal optic root in the chicken

The displaced ganglion cells of Dogiel are a class of retinal ganglion cells whose perikarya are located along the inner margin of the inner nuclear layer. Found in all vertebrate classes, they are particularly conspicuous in avians. Recently, Karten, Fite & Brecha (1977) found that these cells in the pigeon gave rise to a seemingly exclusive projection to the contralateral nucleus of the basal optic root, the major component of the avian accessory optic system. In the present work, the projections of displaced ganglion cells were investigated in hatchling and adult chickens. The cells were found to project to the nucleus of the basal optic root but not to the tectum. Labeled displaced ganglion cells following injections of horseradish peroxidase into the nucleus of the basal optic root were 15 × 20μm in size in both hatchlings and adults. Labeled cells tended to have a higher concentration in the peripheral than in the central retina. Cells were widely but irregularly spaced, with adjacent cells seldom closer than 100 μm. Up to 7700 displaced ganglion cells were labeled in the adult chicken. These results, together with those of Karten et al. (1977) , suggest that in birds, displaced ganglion cells may constitute a unique class of retinal ganglion cells that project exclusively to the nucleus of the basal optic root. In light of the projections of the nucleus of the basal optic root to the oculomotor complex and vestibulocerebellum, the displaced ganglion cells may be an initial link in a visual pathway involved in the control of oculomotor reflexes.

A three-group classification of rat retinal ganglion cells: histological and physiological studies

In a whole mount preparation of the hooded rat retina, stained with methylene blue, the ganglion cell density was counted over the retina. The density ranged from 6200–6500/sq.mm to 1000–1500/sq.mm. The area with a density higher than 6000/sq.mm was called the central area and was centered at about 1 mm (20°) away from the center of the optic disc, in the upper temporal quadrant. Based upon soma diameter histograms made for several locations with different eccentricites, ganglion cells were classified into three groups: large (L), medium-sized (M) and small (S). Relative frequencies of the three groups, on average, were 5, 28 and 67%, respectively. The absolute densities of S- and M-cells increase sharply towards the central area whereas the L-cells show a relatively flat distribution over the retina. The three-group classification of the retinal ganglion cells was supported by measuring their axonal conduction velocities. Single unit recordings were made from the retina and the lateral geniculate nucleus. In each case, two sites were chosen in the optic pathway for electrical stimulation: the optic chiasm and the superior colliculus in the retinal study, and the distal end of the optic nerve and the optic chiasm in the geniculate study. From differences of response latency to the two stimulating sites, conduction velocities of the optic nerve fibers were estimated. The average velocities for the L-, M- and S-axons determined by retinal recordings were 16.8, 11.4 and 6.3 m/sec and those determined by geniculate recordings 18.6, 12.0 and 5.2 m/sec.

A reclassification of retinal ganglion cells in the frog, based upon tectal endings and response properties

Tectal input from the retina was studied in the frog. Both extracellular spike activities and evoked potentials were recorded at different depths during photic stimulation of the contralateral eye. Analysis reveals that the retinal ganglion axons terminate in four distinct layers regularly distributed in depth within the superficial tectal neuropil. These layers are in close correspondence with recent histological investigations. The class ofretinalganglioncells, which terminates in a given layer, performs a distinct type of operation or can be distinguished in latency. For example the ON-OFF ganglion cells are separated into two classes with different latencies: the slow and fast ON-OFF units respectively. They also terminate in separate tectal layers.

Spatial and temporal properties of ?sustained? and ?transient? neurones in area 17 of the cat's visual cortex

Receptive field properties of cells in area 17 of the visual cortex in the cat have been studied by quantitative methods. The cortical cells were classified as ‘sustained’ or ‘transient’ according to their response to a stationary, optimal bar at the receptive field centre, this being analogous to the classification of retinal ganglion cells according to their response to a stationary, optimal spot. Evidence is presented that the ‘sustained/transient’ classification is independent of the ‘simple/complex’ classification. ‘Sustained’ cells of both ‘simple’ and ‘complex’ types had spatial frequency tuning curves with a sharp low-frequency cut, whereas ‘transient’ cells, both ‘simple’ and ‘complex’, had tuning curves with a shallow low-frequency cut, and on average were tuned to lower spatial frequencies than ‘sustained’ cells. ‘Sustained’ cells of both ‘simple’ and ‘complex’ types, had temporal frequency tuning curves with a shallow low-frequency cut, whereas ‘transient’ cells had curves with a sharp low-frequency cut, and on average were tuned to higher temporal frequencies than ‘sustained’ cells. The results indicate that ‘sustained’ and ‘transient’ cortical cells retain the spatial and temporal properties of ‘sustained’ and ‘transient’ retinal ganglion cells, respectively, and thus the two groups of neurones are organised in parallel throughout the visual system, the ‘sustained’ channel providing high spatial resolution and the ‘transient’ channel, high temporal resolution.