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European Journal of Applied Sciences – Vol. 11, No. 6

Publication Date: December 25, 2023

DOI:10.14738/aivp.116.15518

Ringvold, A. (2023). The Pecten Oculi: An Enigma in Comparative Ophthalmology. European Journal of Applied Sciences, Vol -

11(6). 81-88.

Services for Science and Education – United Kingdom

The Pecten Oculi: An Enigma in Comparative Ophthalmology

Amund Ringvold

Eye Department, University of Oslo, Oslo, Norway

ABSTRACT

Purpose: To summarize and evaluate the latest hypotheses on the function of the

pecten oculi (PO). Methods: Review of relevant literature. Results: The PO is an

organ present in all avian eyes. A similar structure, the conus papillaris (CP), is also

found in terrestrial reptiles. Several reports have claimed the PO nourishes the

avascular avian retina, but it has also been argued that the function is not primarily

nutritive but instead may be related to intraocular pH-regulation, as the avian

retina has an anaerobic metabolism. These conclusions are, at first glance,

contradictory. However, a recent report indicated how these two views may be

incorporated in a new and unifying hypothesis, with the common denominator

being that the CP/PO evolved in tandem with increasing uric acid (UA) in serum.

Discussion: According to Wingstrand and Munk, the PO leaks oxygen and nutrients

to the retina, meaning that leakage of the small and heavily soluble component UA

in serum could follow the same path. Protein-binding of the UA is not an option in

the vitreous body, as the UA could crystalize intraocularly and harm the visual

function. Two mechanisms countering this situation have been identified: 1) The

inflow of the UA to the intraocular compartments (i.e. - vitreous body and anterior

chamber) is reduced through selective barriers both in the PO and in the ciliary

body. 2) The UA solubility is increased through alkalization of the vitreous body by

the PO. Conclusion: During evolution vision was improved when the retinal vessels

were collected in the PO. Two competing hypotheses on the PO’s function have been

summarized, and it is shown how these may be incorporated in a new unifying

hypothesis.

Keywords: Avian eye, Reptile eye, Pecten oculi, Conus papillaris, Uric acid, Carbonic

anhydrase, Carbon dioxide

INTRODUCTION

Pecten is Latin for “comb”, and as such the pecten oculi(PO)is a comb-like structure protruding

into the vitreous body from the optic disc area (Figure 1). The function of the PO has been a

controversial ever since its first description some 350 years ago. Several studies, mainly

anatomical, have been published on various species, and more than 30 hypotheses concerning

its possible significance have been presented, as summarized in previous reviews [1-9].

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European Journal of Applied Sciences (EJAS) Vol. 11, Issue 6, December-2023

Figure 1: Diagram of avian bulbus oculi. L, lens; ON, optic nerve; PO, pecten oculi. Adapted from

[33], figure 492.

Figure 2: Diagram of terrestrial reptile bulbus oculi (lizard). L, lens; ON, optic nerve; CP, conus

papillaris. Adapted from [33], figure 421.

A PO-like structure, the conus papillaris (CP), is also found in some reptiles (Figure 2). Based

on macroscopic as well as light and electron microscopic studies many authors have considered

the CP analogue to the avian PO [10-11]. Brach [7] underlined that the extensively reduplicated

apical and basal plasmalemma of the PO’s capillary endothelium has no known parallel in the

animal kingdom except in the capillaries in the lizard CP, which exhibits a remarkable

histological similarity to the PO. Accordingly, observations related to the CP might have some

bearings on the more elaborate structure of the PO, even though there is no linear evolutionary

connection between reptiles and birds.

A huge body of morphological information on the PO [4, 12] has been summarized by Walls [5]:

“Briefly, the pecten is smallest, with the fewest pleats, in nocturnal birds. It is larger in

seminivorous forms, still larger and more elaborate in insectivorous birds, and largest of all in

the diurnal predators such as the hawks and eagles”. He also posed the question whether

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Ringvold, A. (2023). The Pecten Oculi: An Enigma in Comparative Ophthalmology. European Journal of Applied Sciences, Vol - 11(6). 81-88.

URL: http://dx.doi.org/10.14738/aivp.116.15518

“pecten variations really demand explanation other than the one which seems to cover the

supplemental nutritional structures of other vertebrates”.

The present survey is specifically focused on two experimentally based hypotheses on the

function of the PO [6, 13], apparently showing incompatible conclusions. A well-known

technique for verifying an organ’s function is to remove it and observe what happens. Both

Wingstrand/Munk and Brach used this method, though with different surgical procedures. The

outcome of these two studies is summarized below. Additionally, it has been concluded in a

recent paper how these and other observations may support a unifying hypothesis on the PO’s

function [14].

METHOD

CP- and PO-related literature has been collected from various digital databases (PubMed,

Medline, Ovid, Scopus, Web of Science), along with non-digitalized library collections. The PO

is present in all bird eyes, and so the various species described in the original papers will not

be further specified.

RESULTS AND DISCUSSION

Wingstrand and Munk’s Hypothesis

The bird eye has an avascular retina, with the blood vessels in the posterior bulbus being

collected in the PO. Accordingly, Wingstrand and Munk [6] suggested that retina is nourished

through trans-vitreal diffusion from the PO. Their hypothesis was given experimental support

by showing that extraocular cautery of the PO blood supply resulted in its destruction. The

outcome was visualized both histologically and by measuring the oxygen pressure in different

parts of the normal vitreous body. Two main results were reported:

a) Complete blockage of the PO-vessels resulted in the progressive degeneration of the PO

during the initial weeks, followed by a slow and incomplete revascularization.

Additionally, all eyes with a degenerative PO, developed retinal degenerative symptoms

as well, sometimes restricted to the nerve fibre layer and the ganglion-cell layer,

sometimes the entire retina.

b) The measurements of oxygen pressure (with an oxygen cathode placed in the vitreous

body of pigeons) showed that there was a fall from 100 mm Hg surrounding the PO to 5

mm Hg along the inner surface of the retina.

They concluded that “such a gradient cannot exist in a homogeneous non-consuming medium

like the vitreous body without diffusion taking place”, and so they insisted that the PO “is a

substitute for intraretinal vessels and supplies the inner layers of the retina with oxygen.”

Brach’s Hypothesis

Referring to a previous report indicating that the avian retina has largely an anaerobic

metabolism based upon glucose fermentation [15], Brach [13] argued that retinal anoxia will

not necessarily damage the inner retina, as indicated by Wingstrand and Munk. Furthermore,

he suggested that their procedure (extraocular coagulation of the PO vessels) may have

damaged the adjacent optic nerve, “resulting in descending atrophy due to damage to the optic

nerve axons”. Accordingly, he performed direct PO destruction through intraocular ablation of

the tissue employing modified bipolar electrocautery forceps. The outcome was visualized

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histologically and by measuring pH in the vitreous body of eyes with and without the PO. The

following two observations were documented:

a) The PO “was totally destroyed in 13 of 20 birds». «In none of these was general atrophy

of the inner retinal layers observed.”

b) The pH in the vitreous body was on average 7.56 in control eyes against 7.35 in eyes

without the PO (5 birds). Given this refers to a logarithmic scale (10 logarithm), the

difference is significant.

He concluded: “On the basis of my experiments, it is suggested that the function of the pecten

is not primarily nutritive.” “As the anaerobic metabolism of the avian retina liberates an acidic

waste product, it is possible that the pecten may be involved in the regulation of intraocular

pH” [13].

Comments on Wingstrand/Munk’s and Brach’s Observations

While Wingstrand and Munk claimed that an intact PO is necessary for the maintenance of a

normal retinal morphology, Brach took the opposite point of view, i.e., the retina remains

histologically normal after PO-destruction. Thus, the two studies disagree regarding

morphological results on the retina, and the discrepancy may be due to methodological

shortcomings. However, their views are less opposed concerning the findings related to the

vitreous body, as there is no obvious conflict between diffusion of oxygen from the PO to the

retina (Wingstrand and Munk) and the impact of the PO on the intraocular pH-level (Brach).

Brach’s removal of the PO caused a pH drop in the vitreous body, and he suggested that the PO

neutralizes an acidic waste product from the retina. In comparison, Wingstrand and Munk

stated that it is possible and even probable that removal of carbon dioxide from the intraocular

space is an important function of the PO, whereby they quoted Leiner along with Kauth and

Sommer [16,17], “who maintained that the high content of carbonic anhydrase in the pecten

facilitates this function”. The latter authors argued that the PO is a respiratory organ for the

inner retinal layer. Accordingly, Wingstrand and Munk’s versus Brach’s views concerning the

significance of carbonic anhydrase in the PO overlap to some degree. Thus, while Wingstrand,

Munk, and Brach provide important observations on the PO, neither of their conclusions draw

from all the currently available data in explaining the function of the PO.

Ringvold’s Hypothesis

This hypothesis is based on the two previous reports claiming that the PO is nourishing the

retina by leaking oxygen and nutrients [6] or alkalizing the vitreous body to counter the

anaerobic metabolism of the avian retina [13]. A key observation in the new hypothesis [14] is

that during the evolution of reptiles and birds there is a correlation in time between the

development of the CP/PO and increasing UA (mol w 168) concentration in blood. The PO

readily leaks fluorescein (mol w 374) into the vitreous cavity and the anterior chamber with

systemic application [18, 19], whereas the PO is essentially impermeable to fluorescein- labelled dextran which suggests that the selective permeability of its capillaries may be due to

discrimination by molecular size [7]. Blood-borne UA is partly protein-bound preventing

precipitation. However, the vitreous body contains no protein for UA binding. These facts

indicate that significant amounts of the UA could leak into the intraocular compartments as

well. Given the solubility of the UA is pH-dependent and very low in acidic environments

(Figure 3), such leakage could cause intraocular UA precipitation, threatening vision.

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Ringvold, A. (2023). The Pecten Oculi: An Enigma in Comparative Ophthalmology. European Journal of Applied Sciences, Vol - 11(6). 81-88.

URL: http://dx.doi.org/10.14738/aivp.116.15518

Figure 3: The solubility of the UA increases significantly from pH 6 towards alkalic values at

37°C. Adapted from [34], figure 5, curve (a).

Whether this scenario ever posed a threat to the visual system during evolution is unknown.

However, what we do know is that there are indeed two mechanisms minimizing the possibility

for intraocular UA precipitation, making up the core elements in the new, unifying hypothesis

of the PO’s function: 1) The access of the UA to the intraocular compartments is reduced

through selective barriers both in the PO and the ciliary body [14, 20]. 2) The PO alkalizes the

vitreous body, however, not to neutralize acidic waste products from the anaerobic retinal

metabolism, but to increase the solubility of the UA (Figure 3) [14].

CONCLUSIONS

The new hypothesis focuses on evolutionary events when the low-soluble waste product UA

was increasing in blood in parallel with the development of the CP/PO from amphibians to

reptiles/birds [14], and that the CP/PO has a key role in tackling this challenge. Thus, it is

possible to test the hypothesis by asking the following two questions: 1) Do we know of any

ammoniotelic/ureotelic species with the CP/PO? Available literature suggests not. 2) Do we

know of any mainly uricotelic species without the CP/PO? Two are apparent: Snakes and

tuatara. These species have a retina nourished directly from vessels, either inside or on its

surface, and so they are in no need of the CP/PO. This may suggest that their evolution has been

delayed or they have not reached this point in their evolutionary pathway.

It is noteworthy that the CP is not found in all reptiles, - its presence is restricted to terrestrial

species, i.e., the evolution of the CP is suggested to be linked to the terrestrial lifestyle [14].

Walls [5] tried to correlate the size and function of the CP/PO with a diurnal/nocturnal or

cone/rod perspective, and he concluded that “turning to the reptiles, we were confronted by

the paradox that neither the diurnal turtles nor the nocturnal crocodilians have preserved the

ancestral conus papillaris in a useful condition”. However, in view of the new hypothesis, this

observation is not paradoxical because both are aquatic species. It should also be added that

the PO is probably not needed to counter intraocular pH-fluctuations due to an anaerobic

retinal metabolism in the avascular avian retina [9], because an avascular retina is also known

from some mammals (rabbit, guinea pig [21]), which function successfully without the PO.