Brian Blundell Boycott

The morphological types of ganglion cells of the domestic cat's retina.

1. Three distinct morphological types of cat retinal ganglion cells have been identified and categorized as α, β and γ. Alpha ganglion cells have dendritic field diameters from 180 to 1000 μm; β, about 25 to 300 μm; γ, 180 to 800 μm, possibly more.

Morphology and mosaic of on- and off-beta cells in the cat retina and some functional considerations

The beta type of ganglion cell can be subdivided in Golgi-stained whole mounts of the cat retina according to the branching level of the dendritic tree in the inner plexiform layer. The dendritic branching level of on-beta cells is nearer to the cell body; that of off-beta cells is about 10 μm further outwards. After horseradish peroxidase (HRP) injection into the lateral geniculate nucleus all beta cells were labelled. In this way it is shown that about 55% of all ganglion cells, irrespective of retinal topography, are beta cells. The spatial distribution of on- and off-beta cells was studied from the HRP-labelled material. On-beta cells form a lattice with regular inter-cell spacings ; off-beta cells are also regularly arrayed. The two lattices are superimposed independently of each other. Beta cells are commonly assumed to be associated with the resolution of fine detail in the cat visual system. The mosaic of beta cells imposes some constraints and permits some predictions to be made with respect to the cat’s visual discrimination.

Morphological Classification of Bipolar Cells of the Primate Retina

Bipolar cells were studied in Golgi‐Colonnier‐stained whole mounts of macaque monkey retinae. A piece of retina, at 6–7 mm eccentricity, was particularly well stained for the analysis of the different bipolar cell types. Many midget bipolar cells were encountered and the dichotomy into flat and invaginating midget bipolars was confirmed. Six types of diffuse cone bipolar cell are distinguished. They differ in their dendritic branching pattern, in the number of cones contacted–usually between five and ten–and in the shape and branching level of their axons. The size, shape and stratification of the axons were found to be the most reliable distinguishing features for classifying diffuse cone bipolar cells. The stratification of the axons in the inner plexiform layer (IPL), whether closer to the amacrine or ganglion cells, was used to name diffuse cone bipolar cells in the order DB1 to DB6. Blue cone and rod bipolar cells were confirmed as distinct types. Axon terminals of diffuse cone bipolars were found to tile their sublamina of the IPL in a territorial manner. From this the density of each type could be estimated, and it is shown that a single cone is likely to be in contact with as many as 15 individual diffuse bipolar cells, as well as two midget bipolars. The diffuse bipolar cells observed contact all the cone pedicles in their dendritic fields. It is, therefore, unlikely that they carry a chromatic signal into the inner retina. The presence of many midget bipolar cells, which make contact with one cone pedicle only, suggests that midget bipolars provide chromatic input to ganglion cells in peripheral retina as well as in the fovea. The data show that the P‐ and M‐cell pathways of the primate visual system are, to a significant extent, already anatomically discrete at the photoreceptor synapse.

Morphology and Topography of on- and off-Alpha Cells in the Cat Retina

Neurofibrillar staining methods were found to stain all alpha cells of the cat retina completely, that is the perikaryon, the axon and the dendritic branches. The dendrites of the alpha cells in vertical sections were found to be unistratified and to occupy two narrow strata in the outer half of the inner plexiform layer. This difference in branching level could also be observed in whole-mount preparations and it has been demonstrated in the preceding paper (Peichl & Wässle 1981) that it corresponds to the physiological on‒off dichotomy. Thus the topographical distribution of on- and off-alpha cells could be studied. They were found to occur in about equal numbers. Both on- and off-alpha cell perikarya form a regular lattice and both lattices are superimposed independently. The dendritic branches of neighbouring alpha cells overlap and each retinal point is covered by the dendritic field of at least one on- and one off-alpha cell. The dendritic trees of on-alpha cells seem to have more small branches and are on the average smaller than those of off-alpha cells. The density of alpha cells was found to peak in the central area whence it continuously decreased towards the retinal periphery.

Retinal ganglion cell density and cortical magnification factor in the primate.

The question of whether the large area occupied by the primate fovea in the visual cortex (V1) is the result of a selective amplification of the central visual field, or whether it merely reflects the ganglion cell density of the retina, has been a subject of debate for many years. Measurements of the ganglion cell densities are made difficult by lateral displacements of cells around the fovea and the occurrence of amacrine cells in the ganglion cell layer. We have now identified and counted these amacrine cells by GABA immunocytochemistry and by retrograde degeneration of ganglion cells. By reconstructing the fovea from vertical and horizontal serial sections, we were able to measure the densities of cones, cone pedicles and ganglion cells within the same retina. We found 3-4 ganglion cells for every foveal cone. This ratio decreased to one ganglion cell per cone at an eccentricity of 15-20 deg (3-4 mm) and in peripheral retina there are more cones than ganglion cells. The ganglion cell density changes by a factor of 1000-4000 between peripheral and central retina. A comparable gradient has been reported for the representation of the peripheral and central visual field in V1. We suggest that ganglion cell density can fully account for the cortical magnification factor and there is no need to postulate a selective amplification of the foveal representation.

The functional organization of the brain of the cuttlefish Sepia officinalis

The functional organization of the brain of Sepia has been investigated by electrical stimulation. As a result several new divisions of the brain have been made. The pedal ganglion has been shown to consist of four parts: (1) the anterior chromatophore lobes innervating the skin and muscles of the anterior part of the head and arm s; (2) the anterior pedal lobe innervating the arms and tentacles; (3) the posterior pedal lobe innervating the funnel, collar and retractor muscles of the head; (4) the lateral pedal lobes innervating the muscles of the eyes and tissues of the orbits. The palliovisceral (or visceral) ganglion, apart from the magnocellular lobe demonstrated by Young (1939), is shown here to consist of (1) a central palliovisceral lobe innervating the mantle, funnel and viscera ; (2) a pair of lobes innervating the muscles of the fins; (3) a pair of posterior chromatophore lobes innervating the muscles of the chromatophores and skin of the mantle, fin and back of the head; (4) a pair of vasomotor lobes. Because of these new divisions the three main groupings of the suboesophageal neural tissue are now referred to as the anterior, middle and posterior suboesophageal masses corresponding to the old brachial, pedal and palliovisceral divisions. The suboesophageal centres are classified as lower motor centres and intermediate motor centres, depending on the kind of response they give to electrical stimulation and their peripheral connexions. In the supraoesophageal lobes, higher motor centres and silent areas are recognized. The silent areas include the vertical, superior frontal, subvertical, precommissural and dorsal basal lobes. Of the higher motor centres the anterior basal lobe is primarily concerned with the positioning of the head, arms and eyes, particularly during movements involving changes in direction while swimming. Such manoeuvres are brought about by the anterior basal lobe control over the fins and position of the funnel. The posterior basal lobe is here shown to consist of six main divisions: (1) the sub vertical lobe; (2) the dorsal basal lobes; (3) the precommissural lobe; (4) the medial basal lobe; (5) the lateral basal lobe; (6) the interbasal lobe. The medial, lateral and interbasal lobes are higher motor centres. The lateral and medial basal lobes control movements of the chromatophores and skin; the medial basal lobe controls swimming, breathing, fin movements and various visceral functions. The interbasal lobe controls the movements of the tentacles. The optic nerves and the optic lobes, at their periphery, are electrically inexcitable. Electrical stimulation of the centre of the optic lobes evokes all the responses that can be obtained from the other higher m otor centres. The results are discussed in term s of Sanders & Young’s (1940) physiological classification of the brain. A further category intermediate motor centre is recognized. Summary lists of the responses of each lobe are given on pages 516, 520, 525.

Alpha Ganglion Cells in Mammalian Retinae

Retinae from species of six orders of mammals (table 1) were processed by an on-the-slide neurofibrillar staining method to establish whether alpha-type ganglion cells are generally present in placental mammals. Alpha cells of the domestic cat, where they were first defined as a type, are used as a standard of reference. Alpha cells were found in all the twenty species examined; characteristically they have the largest somata and large dendritic fields with a typical branching pattern. In keeping with the common morphology there are inner and outer stratifying subpopulations and therefore a presumptive ‘on-centre’ and ‘off-centre’ responsiveness to light. Depending on the species, alpha cells form between 1 and 4% of the ganglion-cell population and their dendritic fields cover the retina three to four times. The morphology of alpha ganglion cells, and many of their quantitative features, are conserved in mammals coming from different habitats and having a wide variety of behaviours. Because it is known from the cat that alpha ganglion cells have brisk-transient or Y receptive fields it is possible that all placental mammals possess this physiological system.

Cone Connections of the Horizontal Cells of the Rhesus Monkey's Retina

The presence in the rhesus monkey’s retina of a second morphological type of horizontal cell (H2), described by Kolb et al. (1980), is confirmed. Both types of cell are here further described. Their cone connections are quantified and compared with those of mammals and other vertebrates. The dendrites and axons of the H2 type of cell contact only cones as do the dendrites of the H1 cell (originally described by Polyak (1941)) which has an axon contacting only rods. The dendrites of foveal H2 cells contact between 11 and 14 cones; those of H1 contact 7. The number of cones that each type of cell contacts increases with increasing distance from the fovea, so that, by 5-6 mm eccentricity, H2-type cells synapse with between 20 and 30 cones, and the H1 cells with 12-15. The qualitatively estimated coverage factors of each are 3 or 4; every cone synapses with more than one of both types. Neither type of horizontal cell makes chromatically specific connections that are anatomically recognizable, unlike the situation in some teleostean and turtle retinae. Individual horizontal cells, particularly those connected to foveal cones, may have different ratios of chromatic input. At equivalent eccentricities, up to about 6 mm from the fovea, the dendritic fields of H2 horizontal cells are about twice the size of H1 cells and contact about twice the number of cones. These relative differences are closely similar to those of the cat’s horizontal cells and it is suggested that they are a basic feature of most placental mammals. The organization of foveal cone fibres within Henle’s layer is described. The distribution of primate cone telodendria, gap junctions and synapses in the outer plexiform layer are briefly reviewed and compared with those of other vertebrate retinae.

Synaptic Connexions Made by Horizontal Cells within the Outer Plexiform Layer of the Retina of the Cat and the Rabbit

Two ultrastructurally distinctive types of horizontal cells are described in the retinae of the cat and the rabbit. Evidence is presented that they have different synaptic connexions in the outer plexiform layer. The majority of the presynaptic structures identified in the outer plexiform layer of the rabbit (as defined on page 320) belong to a neurofilamentous type of horizontal cell. It is suggested that the cat may be the same. No synapses have been identified on to, or from, the second, predominantly neurotubular, type of horizontal cell. No chemical synapses on to, or between, horizontal cells have been found. Thus input of this kind to both types of horizontal cells is as yet only known to be from the photoreceptors. All positively identified postsynaptic processes were the dendrites or perikarya of bipolar cells. Other cell types that are possibly pre- or postsynaptic in the outer plexiform layer are discussed.

Topography of Horizontal Cells in the Retina of the Domestic Cat

Neurofibrillar methods stain a class of horizontal cells in the cat retina which are shown to be identical with the A-type horizontal cell of Golgistaining. Thus all of the A-type cells of a single retina can be observed. On this basis the changes in density and dendritic field size of A-type horizontal cells with respect to retinal eccentricity were measured. The decrease in density from centre to periphery is balanced by a corresponding increase in size of the dendritic field. Consequently each retinal pointindependent of retinal position — is covered by the dendritic fields of three or four A-type horizontal cells. The nuclei and nucleoli of B-type horizontal cells could also be recognized in neurofibrillar-stained material and thus their distribution was determined. The density ratio B-type: A-type is 2.8 + 0.4 and does not vary much from the centre to the periphery of the retina. Each retinal point is also covered by four B-type horizontal cells. Thus a single cone can contact a maximum of eight horizontal cells. The rate of density decrease from centre to periphery is closely similar in cones and horizontal cells but greater in ganglion cells.