The uses of light for cephalopods living at various depths are described. Aphakic apertures are shown in the eyes of Amphitretus and bolitaenids. In cirrate octopods, the eye is an open cup without lens and the retinal rhabdoms are disorganized. The photosensitive vesicles of cephalopods are extraocular receptors present either in the mantle or on the head. In some mesopelagic forms, they serve to compare the downwelling light with that emitted by the animal's own photophores, thus allowing regulation of counterillumination. In bathypelagic species, the photosensitive vesicles are very large and may serve to ensure reproduction at great depths.

Some of the uses of the paired eyes in shallow water species are discussed. The mechanism for visual learning consists of a system for allowing many possible combinations of the output from numerous feature detectors. This begins with a set of columns in the optic lobes, followed by a tangential system. Outputs from the optic lobe lead to either attack or retreat: a third output leads to a memory system of four matrices allowing for interaction among the visual signals and between them and signals of taste or pain. These matrices allow conjunctive interaction between particular sets of signals and the setting up of memories ensuring appropriate responses. The matrices may be considered as analogous with those of the mammalian hippocampus. They include re-excitation among themselves and with the optic lobes. The tactile memory apparatus of the octopus has four similar lobes and also makes use of the four lobes of the visual system. These are therefore striking examples of adaptive networks allowing learned reactions by statistical selection among numerous channels. The anatomy, function, and generalizing powers of these networks emerged from Boycotts's early work, whose significance for computation can now be appreciated.

Behavioral and electrophysiological studies of insects demonstrate both spectrally independent and chromatically dependent behaviors and interneurons. This account describes the neuroanatomical identification of two parallel retinotopic subsystems, one supplying descending channels to spectrally independent neck and flight motor circuits, the other supplying polychromatic channels to neuropils associated with leg motor circuits in the thoracic ganglia. In the compound eye, two classes of photoreceptors contribute to each of several thousand sampling units. High-sensitivity, chromatically uniform short-axon photoreceptors (R1-R6) supply the lamina's external plexiform layer and are presynaptic to L1, L2 efferents. These project in parallel with a second system of trichromatic long-axon receptors and the L3 efferent. Both pathways supply columns of the medulla, equal in number to ommatidia. Golgi and cobalt-silver impregnation demonstrates that neurons from the medulla diverge to two deeper regions, the lobula plate and lobula, the former a thin tectum of neuropil dorsal to the more substantial lobula. Layer relationships between medulla neurons and their afferent supply suggest that the lobula plate and lobula are each supplied by one or the other, but not both, of the two parallel subsystems. Independence of the two parallel pathways is suggested by ablation of the photoreceptor layer leading to selective degeneration of the motion-sensitive lobula plate neuropil. In addition, octets of small-field neurons associated with the R1-R6/L1, L2 pathway give rise to synaptic complexes with motion-sensitive neurons of the lobula plate. A variety of behavioral and electrophysiological studies provide supporting evidence that certain insects possess parallel visual pathways comparable to the magnocellular and parvocellular subsystems of primates.

Retinae of the crab Leptograpsus which had been maintained on a 12-h light/12-h dark cycle were cultured in vitro and exposed to 1 μM okadaic acid (OKA) at 0.75 h before light onset. Control retinae were subjected to the same routine and sampled at the same times without OKA treatment. At the concentration used, OKA totally inhibits types 1 and 2A protein phosphatases, minimally inhibits type 2B, and does not affect type 2C. 1 μM OKA provoked a diminution of rhabdom diameter measured at the level of the photoreceptor nuclei in the dark, some ommatidial cartridges being stripped of rhabdomeral microvilli altogether. After 1-h illumination (225–320 lux), further reduction of rhabdom diameter was modest in control retinae but precipitate in those treated with OKA. After 2 h, control rhabdom diameters showed a further, not significant, decline, but OKA had induced a resynthesis of massive structures with the light-microscopic appearance of rhabdoms. Electron microscopy revealed that they were heterogeneous and of the following kinds: (1) a minority of rhabdoms with normally disposed but distorted microvilli; (2) rhabdoms in the throes of events that parody normal assembly; and (3) rhabdomal volumes occupied by saccular organelles or by pleats or ruffles of irregular architecture. The cytoplasm of all such receptors was packed with free and bound ribosomes and endomembranes. The sequence of events parallels that seen during light-induced degeneration of photoreceptors of the Drosophila mutant w rdgBKS222. Preliminary experiments show that a protein kinase activator SC-9 mimics many of these effects in the dark in the presence of 1 μM OKA. As a working hypothesis, it is proposed that light activates protein kinases via diacylglycerols generated by the phototransduction cascade, and that in both crab retinas challenged with OKA and retinas of rdgBKS222 activation of a nuclear regulatory protein by hyperphosphorylation provokes a runaway transcription whose selectivity and extent remain to be determined.

Primate retinal bipolar cells synapsing with two adjacent cones (2C bipolars) are further described. Their synaptic contacts are either as the central (invaginating) component of the cone triads or as basal (flat) contacts on the membrane of the cone pedicle base. Correspondingly, their axons end either in the b (inner) half or in the a (outer) half of the inner plexiform layer. The shape and size of the axon terminals of 2C bipolars are indistinguishable from those of adjacent midget bipolars. Therefore 2C bipolars, like midget bipolars, probably synapse with midget ganglion cells. Two C bipolars have not been identified as connected to foveal cones. But they are not restricted to the retinal periphery, as has previously been supposed, since they occur, mixed with midget (single cone) bipolars, throughout all parts of the retina from about 2.5 mm to atleast 10.0 mm from the fovea. It is likely that 2C bipolars are a variant of the midget bipolars; and that they contact some members of the same population of cones, instead of the midgets. This paper briefly reviews, and raises some new, problems concerning our current understanding of the synaptic connectivity patterns of the midget, 2C, and diffuse cone bipolar cells.

The major neurons and neural circuits that are involved in the transmission of color signals through the human retina to produce the color and spatially opponent P cell or midget ganglion cell responses are described. The older findings of single cone to midget bipolar connectivity is reviewed, and the single midget bipolar cell to midget ganglion cell connectivity as revealed by a recent serial section electron microscope study is described in detail. Our present knowledge concerning the discrimination of the blue-cone subtype from the other longer wavelength cones in the human at the outer plexiform layer is summarized, and our most recent findings concerning horizontal cell connectivity to the different spectral types of cones are discussed. Finally, a hypothetical pathway is proposed for color-opponent surrounds of midget ganglion cells using both horizontal cells at the outer plexiform layer and amacrine cell pathways at the inner plexiform layer.

Different techniques were used to manipulate the inhibitory interaction between the red and green photoreceptors (R and G cones) of rhesus and human primates. The response techniques that were used were the corneal electroretinogram (ERG) and psychophysical increment-threshold spectral sensitivity functions. Red-green opponency, as measured by the depth of the notch at 580 nm, is removed by intravitreal injection of bicuculline but not by strychnine. Therefore, red-green opponency is mediated by GABA and not glycine. The depth of the notch is dependent upon stimulus size. Between 30' and 15' test light diameters, this sign of red-green opponency disappears. Psychophysical increment thresholds are shown to produce the notch while decrements do not and intravitreal APB is shown to reduce the notch, evidence that red-green opponency is carried by the “ON” and not the “OFF” bipolar pathways of the retina. Red and green annuli are shown to selectively reduce red and green inhibition, as though there were selective reduction of the surround response in center-surround organized red-green receptive fields.

Dopamine exerts multiple effects on retinal horizontal cells. Dopamine, via cyclic AMP and protein kinase A, reduces the light responsiveness of horizontal cells and the electrical coupling between the cells. The gating kinetics of both gap-junctional and glutamate channels are altered as a result of phosphorylation by protein kinase A. Dopamine also causes a reversible retraction of neurites of horizontal cells maintained in culture. Diacylglycerol analogues as well as phorbol esters mimic this effect of dopamine, but not cyclic AMP analogues or Forskolin. The results suggest that dopamine causes neurite retraction by the activation of protein kinase C via diacylglycerol.

Three approaches to study the function of mammalian rod bipolar cells are described. Extracellular recordings from the intact cat eye under light- and dark-adapted conditions showed that in dark-adapted retina all light responses can be blocked by 2-amino-4-phosphonobutyrate (APB). Immunocytochemical staining with an antibody against protein kinase C (PKC) labeled rod bipolar cells in all mammalian retinae tested. When rat retinae were dissociated, PKC immunoreactivity was also found in isolated bipolar cells and could be used for their identification as rod bipolars. Patch-clamp recordings were performed from such dissociated rod bipolar cells and their responses to APB were measured. APB closed a nonselective cation channel in the cell membrane. The actions of GABA and glycine were also tested and both opened chloride channels in dissociated rod bipolar cells. These results suggest that rod bipolar cells are depolarized by a light stimulus and that GABA as well as glycine modulate their light responses.

A survey of the shapes of dopaminergic (DA) neurons in the retinas of representative vertebrates reveals that they are divisible into three groups. In teleosts and Cebus monkey, DA cells are interplexiform (IPC) neurons with an ascending process that ramifies to create an extensive arbor in the outer plexiform layer (OPL). All other vertebrates studied, including several primate species, have either DA amacrine cells or IPCs with an ascending process that either does not branch within the OPL or does so to a very limited degree. DA neurons of non-teleosts exhibit a dense plexus of fine caliber fibers which extends in the distal most sublamina of the inner plexiform layer (IPL). Teleosts lack this plexus. In all vertebrates, DA cells are distributed more or less evenly and at a low density (10–60 cells/mm2) over the retinal surface. Dendritic fields of adjacent DA neurons overlap. Most of the membrane area of the DA cell is contained within the plexus of fine fibers, which we postulate to be the major source of dopamine release. Thus, dopamine release can be modeled as occurring uniformly from a thin sheet located either in the OPL (teleosts) or in the distal IPL (most other vertebrates) or both (Cebus monkey). Assuming that net lateral spread of dopamine is zero, the fall of dopamine concentration with distance at right angles to the sheet (i.e. in the scleral-vitreal axis) will be exponential. The factors that influence the rate of fall – diffusion in extracellular space, uptake, and transport – are not yet quantified for dopamine, hence the dopamine concentration around its target cells cannot yet be assessed. This point is important in relation to the thresholds for activation of D1 and D2 dopamine receptors that are found on a variety of retinal cells.

Increasing evidence indicates that the retina takes part in the postnatal regulation of eye growth, functioning in this respect to minimize refractive error. The evidence derives both from clinical observations in man and from experiments in animals. The discovery that visual form deprivation leads to an axial overgrowth of the eye and to myopia has opened the way to many current research initiatives. Neurochemical and immunocytochemical experiments in chick and monkey suggest that definable retinal neurons participate in the regulatory pathway controlling eye growth. The most comprehensive data presently implicate dopaminergic amacrine cells. Other important issues to be addressed include the relevance of an intact connection to the central nervous system and the precise retinal mechanism by which eye growth is regulated.

Fish have large eyes, with short optic nerves that are continually flexed by compensatory eye movements during swimming. Here, I review the tissue construction of the fish optic nerve, to see how the glia and axons are adapted to withstand these mechanical stresses, which are not normally encountered by CNS tissue within the skull.

As in other lower vertebrates, the optic nerve astrocytes are highly unusual: their intermediate filaments are composed of cytokeratins (Giordano et al., 1989), not GFAP. Their processes are linked together by desmosomes, forming thin transverse lace-like partitions, placed at quasi-regular intervals longitudinally (Maggs & Scholes, 1990). This accordion-like arrangement is interpreted as providing a flexible tissue-skeleton for the optic nerve.

A new observation is that the optic axons run in coherent parallel waves. This pattern, which is complementary to that of the astroglia, reversibly accommodates limited axial stretches. The waves are equivalent to those underlying the optical banding of Fontana (1781) in peripheral nerves, but wavelength (30 μm) and amplitude (5 μm) are about an order of magnitude less, reflecting the much smaller average size of the optic axons. The pattern also occurs in mammals, and may be restricted to the visual pathway: if present elsewhere in the CNS, nerve-fiber waves are inconspicuous at best.

In fish, the astroglial partitions occur in register with the waves, suggesting that steric interactions between developing axons and glia may help to establish, or stabilize, the regular longitudinal spacing. This may have functional as well as mechanical implications, since the astrocytes form perinodal associations and their pattern is one which strongly clusters the nodes of Ranvier.

Mammalian retinae have a well-defined neuronal pathway that serves rod vision. In rabbit retina, the different populations of interneurons in the rod pathway can be selectively labeled, either separately or in combination. The rod bipolar cells show protein kinase C immunoreactivity; the rod (An) amacrine cells can be distinguished in nuclear-yellow labeled retina; the rod reciprocal (S1 & S2) amacrine cells accumulate serotonin; and the dopaminergic amacrine cells show tyrosine-hydroxylase immunoreactivity. Furthermore, intracellular dye injection of the microscopically identified interneurons enables whole-population and single-cell studies to be combined in the same tissue. Using this approach, we have been able to analyze systematically the neuronal architecture of the rod circuit across the rabbit retina and compare its organization with that of the rod circuit in central cat retina. In rabbit retina, the rod interneurons are not organized in a uniform neuronal module that is simply scaled up from central to peripheral retina. Moreover, peripheral fields in superior and inferior retina that have equivalent densities of each neuronal type show markedly different rod bipolar to An amacrine convergence ratios, with the result that many more rod photoreceptors converge on an An amacrine cell in superior retina. In rabbit retina, much of the convergence in the rod circuit occurs in the outer retina whereas, in central cat retina, it is more evenly distributed between the inner and outer retina.

A specific morphological class of ganglion cell, the alpha cell, was first defined in cat retina. Alpha cells have since been found in a wide range of mammalian retinae, including several orders of placental and marsupial mammals. Characteristically, they have the largest somata and a large dendritic field with a typical branching pattern. They occur as inner and outer stratifying subpopulations, presumably corresponding to ON-center and OFF-center receptive fields. In all species, alpha cells account for less than 10% of the ganglion cells, their somata are regularly spaced, and their dendritic fields evenly and economically cover the retina in a mosaic-like fashion. The morphology of alpha cells and many features, both of single cells and of the population, are conserved across species with different habitats and life-styles. This suggests that alpha cells are a consistent obligatory ganglion cell type in every mammalian retina and probably subserve some fundamental task(s) in visual performance.

Some general rules about the construction principles of ganglion cell classes are inferred from the alpha cells, stressing the importance of population parameters for the definition of a class. The principle, that a functionally and morphologically homogeneous population should have a regular arrangement and a complete and even coverage of the retina to perform its part in image processing at each retinal location, is especially evident across species and across ganglion cell types.