Choroid Rete Mirabile Research Articles

Active Blood Acidification Greatly Enhances Oxygen Supply to the Teleost Retina

Most ray-finned fishes possess a unique system for retinal oxygen delivery, where intracellular acidification of red blood cells (RBCs) in the retinal capillaries induces oxygen offloading from pH-sensitive hemoglobin. A countercurrent vascular network, the choroid rete mirabile, posterior to the retina augments this “oxygen-secretory” mechanism and confers retinal PO2 values that can exceed 1300 mmHg in some species. We hypothesized that the choroid rete mirabile exerts an active role in intracellular RBC acidification to facilitate retinal oxygen secretion. We show the presence and enzymatic activities of extracellular carbonic anhydrase (CA) and vacuolar-type H+-ATPase (VHA) in the lumen of the choroid rete mirabile. These data are consistent with a pathway, where VHA secretes H+ into the choroid rete mirabile lumen, which combines with HCO3– to form CO2 (catalyzed by extracellular CA) that rapidly diffuses into the RBC facilitating hemoglobin oxygen offloading. Next, we validated the model in vivo by injecting an extracellular CA inhibitor (C18) into the dorsal aorta of anesthetized rainbow trout with a PO2 electrode implanted into the retina. Here, the inhibition of extracellular CA resulted in a rapid reduction in retinal PO2 from 517 to 226 mmHg within minutes. These data strongly support the proposed model for RBC acidification in the choroid rete mirabile. Further, in vivo data show that this mechanism primarily augments oxygen diffusion to the inner retinal segments involved in signal-processing and that the evolution of this pathway was tightly associated with the morphological expansion of this part of the retina. Together, these data suggest that the evolutionary origin of retinal oxygen secretion in the early history of the ray-finned fishes was associated with a greatly enhanced capacity for visual processing, potentially permitting improved visual prey detection and the colonization of novel environments.

PO2 Profiles in the Retina of the Hemoglobin‐less Icefishes

The retina of vertebrates has one of the highest O2 demands and requires a constant O2 supply. Four general types of retinal circulations have been described for O2 delivery in extant vertebrates: 1) sole reliance on the choriocapillaris; 2) capillaries penetrating the retina; 3) capillarization of the inner side of the retina; and 4) O2 secretion. Oxygen secretion is based on acid secretion into the blood resulting in a potent unloading of O2 from so‐called Root effect hemoglobins (Hb), which is augmented by venous to arterial O2 diffusion in a vascular rete lining the back side of the retina. This choroid rete mirabile (CRM) allows O2 delivery at super‐atmospheric pressure in the avascular retina of some fishes that have the thickest retinae and some of the largest eyes (relative to body size) of all extant vertebrates. The suborder Notothenioidei, which consists of Antarctic and sub‐Antarctic fishes, provides a model system to unravel how the interactions between Hb function and retinal vascularity evolved to produce modern fish eyes. While several phyletically basal notothenioids have been shown to display similar ocular arrangements as in other Perciform species containing a CRM, more phyletically derived notothenioids have highly reduced CRM or have lost it completely. Of particular interest are the species of the family Channichthyidae, icefishes, that are unique among adult vertebrates in possessing pale white blood containing only few vestigial immature erythrocytes and no Hb. Without Hb, O2 secretion is not functional, and icefishes have been demonstrated to possess heavily increased pre‐retinal capillarization most probably to maintain retinal oxygenation and preserve large eyes and thick retinae. However, whether available O2 at different retinal levels actually follows the degree of vascularization has not been tested.Using thin O2 sensors, we measured profiles of partial pressure of O2 (PO2) in the retina of six species of icefishes, two species of related, but red‐blooded dragonfishes (Bathydraconidae), and four species of more distantly related notothens (Nototheniidae). Arterial PO2 was statistically significantly higher in icefishes than in notothens [t‐test; p = 0.0066 (n = 3); PaO2 = 16.64 ± 3.84 kPa in Chaenocephalus aceratus; PaO2 = 4.42 ± 1.40 kPa in Notothenia coriiceps]. In general, pre‐retinal PO2 was high in icefishes (19.20 ± 6.35 kPa in C. aceratus), approaching the theoretical O2 solubility limit without O2 secretion. The PO2 level decreased towards the outer portion of the retina, but with a small peak on the choroid side of the retina, possibly due to a vestigial choriocapillaris. In notothens displaying Root effect, pre‐retinal PO2 was slightly lower (12.07 ± 5.12 kPa in N. coriiceps) but increased to a super‐atmospheric level on the outer portion of the retina (52.25 ± 32.46 kPa in N. coriiceps).Our results demonstrate that retinal PO2 is dictated by vascularization in the Hb‐deprived icefishes, leading to a unique reversal in the retinal oxygen profile.Support or Funding InformationUS National Science Foundation grant PLR‐1444167Carlsberg FoundationVelux FoundationsThis abstract is from the Experimental Biology 2019 Meeting. There is no full text article associated with this abstract published in The FASEB Journal.

Brain and sense organ anatomy and histology of the Falkland Islands mullet, Eleginops maclovinus (Eleginopidae), the sister group of the Antarctic notothenioid fishes (Perciformes: Notothenioidei)

The perciform notothenioid fish Eleginops maclovinus, representing the monotypic family Eleginopidae, has a non-Antarctic distribution in the Falkland Islands and southern South America. It is the sister group of the five families and 103 species of Antarctic notothenioids that dominate the cold shelf waters of Antarctica. Eleginops is the ideal subject for documenting the ancestral morphology of nervous and sensory systems that have not had historical exposure to the unusual Antarctic thermal and light regimes, and for comparing these systems with those of the phyletically derived Antarctic species. We present a detailed description of the brain and cranial nerves of Eleginops and ask how does the neural and sensory morphology of this non-Antarctic notothenioid differ from that seen in the phyletically derived Antarctic notothenioids? The brain of Eleginops is similar to those of visually oriented temperate and tropical perciforms. The tectum is smaller but it has well-developed olfactory and mechanoreceptive lateral line areas and a large, caudally projecting corpus cerebellum. Eye diameter is about twofold smaller in Eleginops than in many Antarctic species. Eleginops has a duplex (rod and cone) retina with single and occasional twin cones conspicuous centrally. Ocular vascular structures include a large choroid rete mirabile and a small lentiform body; a falciform process and hyaloid arteries are absent. The olfactory rosette is oval with 50-55 lamellae, a large number for notothenioids. The inconspicuous bony canals of the cephalic lateral line system are simple with membranous secondary branches that lack neuromasts. In Antarctic species, the corpus cerebellum is the most variable brain region, ranging in size from large and caudally projecting to small and round. "Stalked" brains showing reduction in the size of the telencephalon, tectum, and corpus cerebellum are present in the deep-living artedidraconid Dolloidraco longedorsalis and in most of the deep-living members of the Bathydraconini. Eye diameter is generally larger in Antarctic species but there is a phylogenetic loss of cellularity in the retina, including cone photoreceptors. Some deep-living Antarctic species have lost most of their cones. Mechanosensation is expanded in some species, most notably the nototheniid Pleuragramma antarcticum, the artedidraconid genera Dolloidraco and Pogonophryne, and the deep living members of the bathydraconid tribe Bathydraconini. Reduction in retinal cellularity, expansion of mechanoreception, and stalking are the most noteworthy departures from the morphology seen in Eleginops. These features reflect a modest depth or deep-sea effect, and they are not uniquely "Antarctic" attributes. Thus, at the level of organ system morphology, perciform brain and sensory systems are suitable for conditions on the Antarctic shelf, with only minor alterations in structure in directions exhibited by other fish groups inhabiting deep water. Notothenioids retain a relative balance among their array of senses that reflects their heritage as inshore perciforms.

Brain and sense organ anatomy and histology of two species of phyletically basal non‐Antarctic thornfishes of the Antarctic suborder Notothenioidei (Perciformes: Bovichtidae)

The predominantly non-Antarctic family Bovichtidae is phyletically basal within the perciform suborder Notothenioidei, the dominant component of the Antarctic fish fauna. In this article we focus on the South Atlantic bovichtids Bovichtus diacanthus, the klipfish from tide pools at Tristan da Cunha, and Cottoperca gobio, the frogmouth from the Patagonian shelf and Falkland Islands. We document the anatomy and histology of the brains, olfactory apparatus, retina, and cephalic lateral line system. We also use the microvascular casting agent Microfil to examine ocular vascular structures. We provide detailed drawings of the brains and cranial nerves of both species. Typical of perciforms, the brains of both species have a well-developed tectum and telencephalon and robust thalamic nuclei. The telencephalon of C. gobio is prominently lobed, with the dorsomedial nucleus more conspicuous than in any other notothenioid. The corpus cerebelli is relatively small and upright and, unlike other notothenioids, has prominent transverse sulci on the dorsal and caudal surfaces. Areas for lateral line mechanoreception (eminentia granularis and crista cerebellaris) are also conspicuous but olfactory, gustatory, and somatosensory areas are less prominent. The anterior lateral line nerve complex is larger than the posterior lateral line nerve in B. diacanthus, and in their cephalic lateral line systems both species possess branched membranous tubules (which do not contain neuromasts) with small pores. These are especially complex in B. diacanthus where they become increasingly branched and more highly pored in progressively larger specimens. Superficial neuromasts are sparse. Both species have duplex (cone and rod) retinae that are 1.25-fold thicker and have nearly 5-fold more photoreceptors and than those of most Antarctic notothenioids. Convergence ratios are also high for bovichtids. Bovichtus diacanthus has a yellow intraocular filter in the dorsal aspect of the cornea. Both species are unique among notothenioids in possessing all three vascular structures present in the generalized teleostean eye: the choroid rete mirabile, the lentiform body (also a rete), and the falciform process. When comparing the phyletically derived Antarctic clade exemplified by the families Artedidraconidae, Bathydraconidae, and Channichthyidae to the phyletically basal bovichtids, we observe phyletic regression and reduction in some regions of the brain and in some sensory modalities that are well displayed in bovichtids. In the phyletically derived families the brain is less cellular and nuclei are smaller and less prominent. In some species reduction in the size of the telencephalon, tectum, and corpus cerebelli imparts a "stalked" appearance to the brain with the neural axis visible between the reduced lobes. There is also a phyletic reduction in the number of ocular vascular structures from three in bovichtids to one or none in artedidraconids, bathydraconids, and channichthyids. There are no morphological features of bovichtid brains and sense organs that presage the divergence of the phyletically derived members of the clade in the Antarctic marine environment with its cold and deep continental shelves. We conclude that this environment does not require sensory or neural morphology or capabilities beyond those provided by the basic perciform body plan.

Ion Levels in the Gastrointestinal Tract Content and Plasma of Four Teleosts with Different Feeding Habits

The teleost pseudobranch, a reduced mandibular gill arch, morphologically closely resembles a gill hemibranch. It consists of several filaments bearing numerous lamellae. The vascular system of the pseudobranch also matches that of a gill, with afferent and efferent filamental arteries and the lamellar blood space. Despite the pseudobranch’s gill-like appearance, however, a gas exchange function is excluded in many teleosts by overlying opercular epithelium, effectively eliminating diffusional exchange with the external medium. The physiological function of the pseudobranch is still unknown, though its conspicuously close association with the ocular choroid rete mirabile, a structure supporting elevated oxygen partial pressures in the eye, suggests a role related to the process of oxygen secretion into the eyes of teleosts. In this paper we present new stereological data on the pseudobranch of rainbow trout (average weight: 478 ± 114 g, x ± SD, n = 12). The total Cavalieri volume of the pseudobranch was 46.4 μl (97 μl kg−1), consisting of lamellae 49%, connective tissue 43.8%, large blood vessels 4.5%, filamental cartilage 2.3%, and central venous sinus 1.3%. Lamellae were comprised of pillar and pseudobranchial cells 81%, blood space 12.3%, and lacunar tissue 6.4%. The inner surface of the blood space in the lamellae was 12.2 cm2 (25.5 cm2 kg−1), and its volume was 2.81 μl (5.88 μl kg−1). The results demonstrate the pseudobranch’s potential for physiological functions requiring a high surface area or surface-to-volume ratio, i.e. ion transfer, gas exchange and other regulatory processes. More detailed analysis of the function of the pseudobranch, however, has to remain subject of future morphological and physiological studies.

X-ray microtomography of 410 million-year-old optic capsules from placoderm fishes

The structure of two small ossified optic capsules from mid-Palaeozoic placoderm fishes has been revealed in fine detail, by the use of X-ray microtomography analysis and 3D visualisation software. These two specimens are 410 million-year-old; they were collected from an Early Devonian (Lochkovian) limestone in central New South Wales, and are the oldest known optic capsules from jawed fishes. The capsules show attachment areas for seven extrinsic eye muscles, rather than the six until recently deemed universal for gnathostomes. The analysis also revealed structures within the ossified cartilage which covered the medial surface of the eyeball, including nerve tracts, vascular canals, and possibly a choroid rete mirabile.

A difference in optomotor behaviour of two Antarctic nototheniid fishes is correlated with the presence of a choroid rete mirabile and Root effect

The hypothesis that fish vision is influenced by the presence of a choroid rete mirabile (an oxygen-concentrating apparatus in the eye) and the Root effect was tested using the optomotor response in two nototheniid species from Antarctica. Pagothenia borchgrevinki, an active cryopelagic zooplanktivore, does not exhibit a major Root effect and the rete is absent. In contrast, the sluggish, benthic nototheniid, Trematomus bernacchii, possesses both a rete and a significant Root effect. Whole-eye ocular PO2 was higher in T. bernacchii (18.6 kPa) than in P. borchgrevinki (18.1 kPa) and the optomotor response of T. bernacchii was positively influenced by subtended angle on a moving background whereas P. borchgrevinki did not respond to any subtended angle (0–600 min of arc). The optomotor response of T. bernacchii may therefore have been facilitated by elevated ocular PO2 due to the presence of the choroid rete and the Root effect.

The effect of strenuous exercise and beta-adrenergic blockade on the visual performance of juvenile rainbow trout, Oncorhynchus mykiss.

It is hypothesised that the visual performance of rainbow trout, Oncorhynchus mykiss, will be impaired by strenuous exercise as a result of metabolic stress (blood lactacidosis) that activates the Root effect and limits the oxygen-carrying capacity of blood flowing to the eye. The ability to resolve high contrast objects on a moving background, as a measure of visual performance, was quantified pre- and post-exercise using the optomotor response. Strenuous exercise induced a metabolic acidosis (8.0 mmol l(-1) blood lactate) and a significant red cell swelling response but no change in the optomotor response threshold (120 min of arc) was observed. Beta-adrenergic blockade (propranolol) abolished post-exercise red cell swelling but optomotor response thresholds were still maintained at 120 min of arc despite a significant blood lactate load (7.8 mmol l(-1)). The choroid rete mirabile of the trout is extremely well developed (rete area:eye area = 0.39) and may maintain visual performance by ensuring a relatively direct supply of oxygen to the central regions of the avascular retina. Exercised fish under beta-adrenergic blockade exhibited an enhanced optomotor response at 240-300 min of arc. Assuming that these responses reflect "tunnel vision", adrenergic regulation of red cell function may preserve a high ocular PO(2) gradient that satisfies the oxygen demand of peripheral retinal cells.

Correlates of choroid rete development with the metabolic potential of various tropical reef fish and the effect of strenuous exercise on visual performance

It is hypothesised that the transport of oxygen to the retinal cells of fish with Root effect haemoglobins (Hb) is impaired by strenuous exercise due to a proton load that drastically reduces arterial haemoglobin–oxygen affinity. Routinely active reef fishes have enhanced oxygen transport and anaerobic (i.e. blood lactate loading) potentials relative to inactive species. Surprisingly, the development of the choroid rete mirabile (employed as an oxygen concentrating apparatus in the eye) is directly correlated with post-exercise lactate loads rather than with the magnitude of the Root effect and suggests that an increased development is adaptive for fish with high anaerobic potentials. The hypothesis that visual performance is reduced by strenuous exercise was tested in Lutjanus carponotatus using the optomotor response. Moderate blood lactate loads (2 mmol l −1 blood lactate) and red cell swelling responses were induced by exercise, but the optomotor response threshold (180 min of arc) was maintained. A moderate metabolic disturbance does not therefore appear to be a liability for the visual performance of a tropical fish in possession of Root effect haemoglobins.

Necrosis of trout retina (Oncorhynchus mykiss) after sublethal exposure to nitrite

Rainbow trout exposed to sublethal concentrations of nitrite accumulate this substance to different degrees. The result is a formation of methemoglobin in amounts ranging from 6 to 100% of total hemoglobin. In contrast to tolerant specimens (low nitrite accumulation), the eyes of most of the intolerant trout were severely affected. Alterations ranged from necroses of single retinal neurons to complete destruction of the retina. Since severe direct or hypoxic damages to other organs have not been observed, the striking reaction of the retina may be attributable to its high oxygen demand. The impaired function of the choroidal rete mirabile is believed to lead to a reduced oxygen supply or to acidification of the ocular fluids.

Root effect hemoglobins in marine fish

1. 1. The Root effect was evaluated in hemolysates from 26 species of bony fish and 20 species of cartilaginous fish found on the Brazilian southeastern coast. 2. 2. Teleost Root shifts, with a single exception, are correlated with the presence of the choroid rete mirabile but not with its counterpart in the swimbladder. 3. 3. Five ray species displayed weak and moderate Root effects despite the absence of choroid and swimbladder rete. 4. 4. The presence and intensity of the Root effect is probably primarily related to the high oxygen demand of the retina and with the importance of visual perception in fish. 5. 5. In marine teleosts the magnitude of the Root effect seems to be associated with the presence and size of both the choroid rete and the pseudobranch. 6. 6. An antioxidant protection of the fish eyes can be advocated for the pseudobranch.

Unilateral exophthalmos in Sebastes spp.: histopathologic lesions

Abstract. A spontaneous unilateral exophthalmos occurring in five species of otherwise healthy rockfish, Sebastes spp., was investigated. All eyes from nine unilaterally exophthalmic and seven non‐exophthalmic rockfish were examined grossly and histologically. In all affected fish the exophthalmos was due to enlargement of the globes resulting from the formation of choroidal cysts filled with a clear, watery fluid and surrounded by dense, aberrant connective tissue. Cyst formation led to gross distortion and disorganization of the choroid. Distorted remnants of the choroidal rete mirabile contained markedly fewer erythrocytes, a homogeneous proteinaceous material and a mild inflammatory cell infiltrate. Thickened scleral cartilage with disoriented chondrocytes was also present in exophthalmic eyes. Some of the affected eyes showed pigmentary abnormalities with clumps of heavily pigmented cells present in the retina and choroid. Retinal degeneration and detachment was also evident in some of the affected eyes.

Choroidal rete mirabile function and resistance to retinal oxygen toxicity in fish

Previous studies have suggested that resistance to O 2 toxicity in teleost fish retina is directly related to choroidal rete mirabile function and to the chronically elevated P O 2 at the retina. We tested this hypothesis in several species of fish with varying degrees of rete development. The effect of hyperbaric oxygen on O 2 consumption, Na +-, K +-ATPase activity and the ERG was recorded. Hyperbaric oxygen had no effect on the ERG of either the flounder, which has a large rate and elevated P O 2 , or the eel, which has no rete. Exposure to hyperbaric oxygen for 6 hr attenuated by 50% the ERG of the goosefish which has a small rete (retinal P O 2 = 90 mmHg). Hyperbaric oxygen abolished the b-wave of the dogfish ERG and attenuated the skate b-wave by 80%. Elasmobranchs have no rete and low retinal P O 2 . Hyperbaric oxygen had no effect on O 2 consumption and ATPase activity in any species studied. The ERG data supported the hypothesis that resistance to oxygen toxicity by the teleost retina is an adaptation to a chronically elevated P O 2 generated by the choroidal rete.

A hemeprotein implicated in oxygen transport into the eye of fish

1. 1. Following occlusion of the circulation to the eye of bluefish a ferric hemeprotein (or proteins) appears in the blood plasma of the ophthalmic blood vessels. 2. 2. This protein may play a role in the establishment of elevated oxygen pressures by the choroid rete mirabile. 3. 3. A hemeprotein (or proteins) is occasionally found in the systemic blood plasma of Amia calva. It combines reversibly with oxygen and with carbon monoxide. Ligand binding is co-operative, suggesting that the protein has two or more interacting subunits. 4. 4. Ferrous bluefish and Amia hemeproteins exhibit hemochromogen spectra, indicating that the distal ligand position of the heme is occupied by a nitrogenous (or sulfurous) ligand.

Short circuiting the ocular oxygen concentrating mechanism in the teleost Salmo gairdneri using carbonic anhydrase inhibitors.

Ocular oxygen concentration by the process of counter current multiplication in rainbow trout (Salmo gairdneri) was rapidly suppressed after intraperitoneal injections of the carbonic anhydrase inhibitor CL-11,366. The rapidity with which this drug acted suggested a short circuiting of the choroidal rete mirabile. A comparison was made between the time after injection of inhibitor at which oxygen concentrating ability was lost to the time after injection of inhibitor at which its presence in red blood cells, choroidal rete, pseudobranch, and retinal tissue was first noted. A scheme for the possible role of carbonic anhydrase from each of these tissues in the process of ocular oxygen concentration is given.