The retina of cephalopods and its degeneration after optic nerve section

Each retinal cell of Octopus carries a rhabdomere on two opposite faces. Rhabdomeres from four cells combine to make a square rhabdome. The cells are mainly arranged with their axes in approximately either the vertical or horizontal plane as the eye is usually held in the head. Counts show that there are about twice as many retinal cell nuclei as there are rhabdomes. There are altogether about 2 x 10 7 retinal cells in each eye, with a density of about 50 000/mm 2 . The retinal cells at the centre of the retina are longer and thinner than those at the periphery. There is a strip of longer, thinner cells running horizontally along the equator. These often have less pigment in their distal ends than do the cells dorsally and ventrally, but other distributions of the pigment are seen, depending on the previous illumination. There are several types and sizes of retinal cell and not all are associated in fours to make rhabdomes. The proximal segments carry fine collateral twigs, these interdigitate and may allow mutual interaction between neighbours. The main meshes of the retinal plexus are not formed by fibres of the retinal cells but by the axons of cells in the optic lobes, presumably efferents. After severing the optic nerves to any region of the retina all the retinal cells undergo retrograde degeneration, leaving only the supporting cells intact. The retinal nerve plexus disappears almost completely, but a few fibres remain. At the boundary between a region with severed and intact nerves the plexus continues for some distance into the denervated region. After removal of all the optic lobe except a portion of its outermost (plexiform) zone the retinal receptors do not degenerate completely but are reduced in length. Their axons have not been interrupted by the operation and this is therefore a partial transneuronal retrograde degeneration.

Each optic nerve contains several bundles of axons. The axons have their surface membranes directly apposed and the bundles lie in troughs of the elongated Schwann cells. The axons have pronounced varicosities along their length. The axons enter the optic lobe and run between the granule cells to synapse in the plexiform zone. The granule cells are small neurons. Their cytoplasmic organelles include endoplasmic reticulum, ribosomes, agranular reticulum and of special interest, oval or spherical bodies with a lamellated cortex and granular medulla. The elongated varicose presynaptic bags of the optic axons contain mitochondria in the proximal region, numerous synaptic vesicles and, sometimes, neurofilaments. Below the mitochondrial zone, synaptic contacts are made with small spines invaginated into the bags. The spines probably originate from the trunks of the granule cells. Tunnel fibres that are probably trunks of the outer granule cells, run through channels in the synaptic bags.


The optic lobes provide a system for coding the visual input, for storing a record of it and for decoding to produce particular motor responses. There are at least three types of optic nerve fibre, ending at different depths in the layered dendritic systems of the plexiform zone. Here the optic nerve fibres meet the branches of at least four types of cell. (1) Centripetal cells passing excitation inwards. The dendrites of these are very long, with fields orientated more often in horizontal and vertical than in other directions. (2) Numerous amacrine cells, with cone-shaped dendritic fields but no determinable axon. (3) Centrifugal cells conducting back to the retina. (4) Commissural fibres from the opposite optic lobe, and other afferents. After section of the optic nerves the plexiform layer of the corresponding part of the optic lobe becomes reduced, but the tangential layers of dendrites remain. There is a reduction in the thickness of the layers of amacrine and other cells and a shrinkage of the whole lobe. Conversely the tangential layers can be degenerated, leaving the optic nerve fibres, by severing the arteries to the optic lobe. The centre of the optic lobe contains cells with spreading dendritic trees of many forms. Some run mainly tangentially, others are radial cones. Those towards the centre send axons to the optic tract. Small multipolar cells accompany the large neurons of the cell islands. About 2 x 10 7 optic nerve fibres visible with the light microscope enter the lobes but only 0-5 x 106, or less, leave in the optic tract, these being distributed to some ten centres in the supraoesophageal lobes. It is suggested that the variety of shapes of the dendritic trees within the optic lobes provides the elements of the coding system by which visual input is classified.


1967 ◽  
Vol 167 (1008) ◽  
pp. 252-281 ◽  

The visuo-motor system in cephalopods comprises paired eyes, paired optic lobes, paired peduncle lobes and the basal lobes. The organization of this system was investigated by observing behavioural changes immediately after surgical interference to different parts of it. Lesions were made that removed the optic and peduncle lobes and sectioned the optic nerves bilaterally, unilaterally, separately and in all the possible combinations. In all, twenty types of lesion were made: they fell into four sets. The first set wore unilateral, interfering with only one visual system (i.e. eye, optic lobe, peduncle lobe). After such lesions, locomotion was relatively unaffected. The second set of lesions bilaterally reduced the visuo-motor system. After bilateral optic nerve section loco­ motion is modified but not markedly impaired. After bilateral removal of the optic and peduncle lobes together there is marked loss of muscle tone and the preparation is unable to movo. This does not occur when either the optic or peduncle lobes are removed alone.Following removal of both optic lobes the animal is ‘ blind’ but locomotion and posture are normal. liemoval of both peduncle lobes leads to locomotor dysfunction, locomotion being ‘coarse’ and ‘uncontrolled’. There are oscillatory movements about one or more axes. This oscillation may turn into uni-directional ‘spin’ about one or more axes: this ‘spin’ is reversible in direction. Such dysfunction does not occur if the peduncle lobes are removed from an octopus with optic nerves sectioned.The third set of lesions were asymmetrical for the peduncle lobes. Some of these lesions produced ‘forced circling’ movements. This is a continual movement about the yaw and/or roll axes, whose sense is fixed: forward about the intact peduncle lobe in a tight circle, i.e. clockwise if the right peduncle lobe remains. The fourth set of lesions controlled for the possibility that asymmetries in the optic lobe system cause forced circling movement: they do not. Evidence from all four sets of data suggest that the optic lobes are the prime instigators of motor ‘commands’ following visual stimuli and that the peduncle lobes are a subordinate system that modifies these commands, on the basis of changing visual cues. A hypothesis is proposed that the peduncle lobes are important in co-ordinating commands from the two optic lobes: this ensures a unified response by the whole animal oven when the visual infor­ mation differs on the two sides of the animal.


Development ◽  
1989 ◽  
Vol 105 (4) ◽  
pp. 739-746 ◽  
Author(s):  
S. Tix ◽  
J.S. Minden ◽  
G.M. Technau

We have identified a set of larval neurones in the developing adult optic lobes of Drosophila by selectively labelling cells that have undergone only a few mitoses. A cluster of three cells is located in each of the optic lobes near the insertion site of the optic stalk. Their axons fasciculate with fibres of the larval optic nerve, the Bolwig's nerve, and then form part of the posterior optic tract. These cells are likely to be first order interneurones of the larval visual system. Unlike the Bolwig's nerve, they persist into the adult stage. The possibility of a pioneering function of the larval visual system during formation of the adult optic lobe neuropil is discussed.


2021 ◽  
Vol 22 (12) ◽  
pp. 6245
Author(s):  
Santiago Milla-Navarro ◽  
Ariadna Diaz-Tahoces ◽  
Isabel Ortuño-Lizarán ◽  
Eduardo Fernández ◽  
Nicolás Cuenca ◽  
...  

One of the causes of nervous system degeneration is an excess of glutamate released upon several diseases. Glutamate analogs, like N-methyl-DL-aspartate (NMDA) and kainic acid (KA), have been shown to induce experimental retinal neurotoxicity. Previous results have shown that NMDA/KA neurotoxicity induces significant changes in the full field electroretinogram response, a thinning on the inner retinal layers, and retinal ganglion cell death. However, not all types of retinal neurons experience the same degree of injury in response to the excitotoxic stimulus. The goal of the present work is to address the effect of intraocular injection of different doses of NMDA/KA on the structure and function of several types of retinal cells and their functionality. To globally analyze the effect of glutamate receptor activation in the retina after the intraocular injection of excitotoxic agents, a combination of histological, electrophysiological, and functional tools has been employed to assess the changes in the retinal structure and function. Retinal excitotoxicity caused by the intraocular injection of a mixture of NMDA/KA causes a harmful effect characterized by a great loss of bipolar, amacrine, and retinal ganglion cells, as well as the degeneration of the inner retina. This process leads to a loss of retinal cell functionality characterized by an impairment of light sensitivity and visual acuity, with a strong effect on the retinal OFF pathway. The structural and functional injury suffered by the retina suggests the importance of the glutamate receptors expressed by different types of retinal cells. The effect of glutamate agonists on the OFF pathway represents one of the main findings of the study, as the evaluation of the retinal lesions caused by excitotoxicity could be specifically explored using tests that evaluate the OFF pathway.


Development ◽  
1988 ◽  
Vol 102 (3) ◽  
pp. 479-488
Author(s):  
M.F. Humphrey ◽  
C.A.O. Stuermer

The tectal pathways of regenerating goldfish optic axons are abnormal but not random. The relative proportion of temporal axons is highest in rostral tectum (65%) drops in midtectum (31%) and is very low in caudal tectum (4%). By contrast, nasal axons proceed into caudal tectum and are therefore relatively evenly distributed throughout the tectum. In this study, we have tested whether temporal axons are confined to rostral tectum by the presence of nasal axons in caudal tectum or whether they have a preference for rostral tectum regardless of other axons. We similarly tested whether nasal axons would grow preferentially into caudal tectum in the absence of temporal axons. At the time of optic nerve section either the nasal or temporal half retina was removed. Either 35 or 70 days after nerve section, the regenerating optic axons were labelled with HRP and both their pathways and distribution determined in DAB-reacted tectal wholemounts. In the absence of nasal axons, the relative density of temporal axons in rostral, mid and caudal tectum was 70%, 28% and 2%, respectively. The corresponding values for nasal axons, in the absence of temporal axons, were 30%, 40% and 30%, respectively. Thus, the overall distribution of nasal and temporal axons in the half retinal regenerates was similar to that of whole retinal regenerates, demonstrating that the retinotopic preferences of the axons were not dependent upon interaxonal interactions. Thus, nasal and temporal axons obviously discriminate between rostral and caudal tectum despite pathway disorganization and the absence of axons from the opposite hemiretina. This is consistent with axonal growth being under the influence of positional markers in tectum.


1967 ◽  
Vol 2 (3) ◽  
pp. 349-358
Author(s):  
R. M. EAKIN ◽  
JANE A. WESTFALL ◽  
M. J. DENNIS

The eye of a nudibranch, Hermissenda crassicornis, was studied by light and electron microscopy. Three kinds of cells were observed: large sensory cells, each bearing at one end an array of microvilli (rhabdomere) and at the other end an axon which leaves the eye by the optic nerve; large pigmented supporting cells; and small epithelial cells, mostly corneal. There are five sensory cells, and the same number of nerve fibres in the optic nerve. The receptor cells contain an abundance of small vesicles, 600-800 Å in diameter. The lens is a spheroidal mass of osmiophilic, finely granular material. A basal lamina and a capsule of connective tissue enclose the eye. In some animals the eye is ‘infected’ with very small bodies, 4-5 µ in diameter, thought to be symbionts.


Development ◽  
1998 ◽  
Vol 125 (6) ◽  
pp. 1059-1066 ◽  
Author(s):  
D.K. Waid ◽  
S.C. McLoon

The different retinal cell types arise during vertebrate development from a common pool of progenitor cells. The mechanisms responsible for determining the fate of individual retinal cells are, as yet, poorly understood. Ganglion cells are one of the first cell types to be produced in the developing vertebrate retina and few ganglion cells are produced late in development. It is possible that, as the retina matures, the cellular environment changes such that it is not conducive to ganglion cell determination. The present study showed that older retinal cells secrete a factor that inhibits the production of ganglion cells. This was shown by culturing younger retinal cells, the test population, adjacent to various ages of older retinal cells. Increasingly older retinal cells, up to embryonic day 9, were more effective at inhibiting production of ganglion cells in the test cell population. Ganglion cell production was restored when ganglion cells were depleted from the older cell population. This suggests that ganglion cells secrete a factor that actively prevents cells from choosing the ganglion cell fate. This factor appeared to be active in medium conditioned by older retinal cells. Analysis of the conditioned medium established that the factor was heat stable and was present in the <3 kDa and >10 kDa fractions. Previous work showed that the neurogenic protein, Notch, might also be active in blocking production of ganglion cells. The present study showed that decreasing Notch expression with an antisense oligonucleotide increased the number of ganglion cells produced in a population of young retinal cells. Ganglion cell production, however, was still inhibited in cultures using antisense oligonucleotide to Notch in medium conditioned by older retinal cells. This suggests that the factor secreted by older retinal cells inhibits ganglion cell production through a different pathway than that mediated by Notch.


2020 ◽  
Vol 10 (1) ◽  
Author(s):  
Benjamin M. Davis ◽  
Li Guo ◽  
Nivedita Ravindran ◽  
Ehtesham Shamsher ◽  
Veerle Baekelandt ◽  
...  

AbstractIdentifying disease-specific patterns of retinal cell loss in pathological conditions has been highlighted by the emergence of techniques such as Detection of Apoptotic Retinal Cells and Adaptive Optics confocal Scanning Laser Ophthalmoscopy which have enabled single-cell visualisation in vivo. Cell size has previously been used to stratify Retinal Ganglion Cell (RGC) populations in histological samples of optic neuropathies, and early work in this field suggested that larger RGCs are more susceptible to early loss than smaller RGCs. More recently, however, it has been proposed that RGC soma and axon size may be dynamic and change in response to injury. To address this unresolved controversy, we applied recent advances in maximising information extraction from RGC populations in retinal whole mounts to evaluate the changes in RGC size distribution over time, using three well-established rodent models of optic nerve injury. In contrast to previous studies based on sampling approaches, we examined the whole Brn3a-positive RGC population at multiple time points over the natural history of these models. The morphology of over 4 million RGCs was thus assessed to glean novel insights from this dataset. RGC subpopulations were found to both increase and decrease in size over time, supporting the notion that RGC cell size is dynamic in response to injury. However, this study presents compelling evidence that smaller RGCs are lost more rapidly than larger RGCs despite the dynamism. Finally, using a bootstrap approach, the data strongly suggests that disease-associated changes in RGC spatial distribution and morphology could have potential as novel diagnostic indicators.


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