Introduction: Ocular diseases pose a significant health concern for donkeys. However, studies examining the microanatomy and cell populations of the donkey retina are scarce. The current study aimed to describe the vascular pattern of the donkey retina and document its cellular components. Methods: The donkey retina specimens were obtained from different retinal regions and prepared for semithin sectioning and immunohistochemistry. Results: The donkey has a paurangiotic retina in which retinal vessels are confined to a narrow area around the optic disc. Glial cells coexist with the blood vessels being very numerous in the vascular region and become scanty in the avascular ones. S-100-positive astrocytes could be observed in these avascular areas. Ganglion cells are organized in a single layer with the least population existing in the peripheral retina. Acidic fibroblast growth factor (AFGF) is immunoreactive in amacrine and ganglion cells. A subpopulation of amacrine cells reacted strongly to tyrosine hydroxylase (TH), and others reacted positively to S-100 protein. Ganglion cell nuclei exhibited a strong immunoreactivity to S-100 protein as well. Furthermore, glial fibrillary acidic protein (GFAP) is used to identify Müller cells that extend their processes across the retina from the inner to the outer limiting membrane. Conclusions: In conclusion, our findings provide novel insights into the normal retinal organization. The donkey retina shows the characteristic expression of immunohistochemical markers for the major cell types. In addition, the distribution of glial cells is comparable between the vascular and avascular regions.

1.
Purnyn
H
.
The mammalian retina: structure and blood supply
.
Neurophysiology
.
2013
;
45
(
3
):
266
76
. .
2.
Marc
RE
.
The structure of vertebrate retinas
.
Retin basis Vis
.
1999
:
3
19
.
3.
Masland
RH
.
The neuronal organization of the retina
.
Neuron
.
2012
;
76
(
2
):
266
80
. .
4.
Deeg
CA
,
Amann
B
,
Hauck
SM
,
Kaspers
B
.
Defining cytochemical markers for different cell types in the equine retina
.
Anat Histol Embryol
.
2006
;
35
(
6
):
412
5
. .
5.
Turusov
VS
.
[Protein S-100 in the histological diagnosis of tumors]
.
Arkh Patol
.
1990
;
52
(
1
):
71
8
.
6.
Wu
KH
,
Madigan
MC
,
Billson
FA
,
Penfold
PL
.
Differential expression of GFAP in early v late AMD: a quantitative analysis
.
Br J Ophthalmol
.
2003
;
87
(
9
):
1159
66
. .
7.
Dabin
I
,
Courtois
Y
.
In vitro kinetics of basic fibroblast growth factor diffusion across a reconstituted corneal endothelium
.
J Cell Physiol
.
1991
;
147
(
3
):
396
402
. .
8.
Fredj-Reygrobellet
D
,
Plouet
J
,
Delayre
T
,
Baudouin
C
,
Bourret
F
,
Lapalus
P
.
Effects of aFGF and bFGF on wound healing in rabbit corneas
.
Curr Eye Res
.
1987
;
6
(
10
):
1205
9
. .
9.
Schaepdrijver
LD
,
Simoens
P
,
Lauwers
H
,
De Geest
JP
.
Retinal vascular patterns in domestic animals
.
Res Vet Sci
.
1989
;
47
(
1
):
34
42
. .
10.
Rossel
S
,
Marshall
F
,
Peters
J
,
Pilgram
T
,
Adams
MD
,
O’Connor
D
.
Domestication of the donkey: timing, processes, and indicators
.
Proc Natl Acad Sci USA
.
2008
;
105
(
10
):
3715
20
. .
11.
Seyiti
S
,
Kelimu
A
.
Donkey industry in China: current aspects, suggestions and future challenges
.
J Equine Vet Sci
.
2021
;
102
:
103642
. .
12.
Mrema
M
.
An economic analysis of the utilisation of donkeys in Botswana: the past and the future
.
Donkeys, people and development
;
2004
; p.
164
.
13.
Wold
AG
,
Tegegne
A
,
Yami
A
.
Research needs of donkey utilisation in Ethiopia. Donkeys, people and development. A resource book in the animal tracfion network for Eastern and Southern Africa
;
2004
; p.
79
.
14.
Ali
M
,
Baber
M
,
Hussain
T
,
Awan
F
,
Nadeem
A
.
The contribution of donkeys to human health
.
Equine Vet J
.
2014
;
46
(
6
):
766
7
. .
15.
De Rose
P
,
Cannas
E
,
Reinger Cantiello
P
.
Donkey-assisted rehabilitation program for children: a pilot study
.
Ann Ist Super Sanita
.
2011
;
47
(
4
):
391
6
. .
16.
Starkey, P. and M. Starkey, Regional and world trends in donkey populations. Starkey P and Fielding D (eds).
2000
. p.
10
21
.
17.
Bradley
C
,
Grundon
R
,
Sansom
PG
.
The prevalence of uveitis in a population of donkeys in the UK
.
Equine Vet J
.
2020
;
52
(
6
):
863
7
. .
18.
Ehrenhofer
MC
,
Deeg
CA
,
Reese
S
,
Liebich
HG
,
Stangassinger
M
,
Kaspers
B
.
Normal structure and age-related changes of the equine retina
.
Vet Ophthalmol
.
2002
;
5
(
1
):
39
47
. .
19.
Schnitzer
J
.
Astrocytes in the Guinea pig, horse, and monkey retina: their occurrence coincides with the presence of blood vessels
.
Glia
.
1988
;
1
(
1
):
74
89
. .
20.
Bancroft
J
,
Steven
A
,
Turner
DJNY
,
Edinburg
M
,
Melbourne
SF
,
Tokyo
.
Theory and practice of histological techniques
.
London
:
Churchill Livingstone
;
1996
; p.
129s
.
21.
Morris
JK
.
A formaldehyde glutaraldehyde fixative of high osmolality for use in electron microscopy
.
J Cell Biol
.
1965
;
27
:
1A
149A
.
22.
Abdel-Maksoud
FM
,
Hussein
MT
,
Attaai
A
.
Seasonal variation of the intraepithelial gland in camel epididymis with special reference to autophagosome
.
Microsc Microanal
.
2019
;
25
(
4
):
1052
60
. .
23.
Attaai
AH
,
Hussein
MT
,
Aly
KH
,
Abdel-Maksoud
FM
.
Morphological, immunohistochemical, and ultrastructural studies of the donkey’s eye with special reference to the AFGF and ACE expression
.
Microsc Microanal
.
2022
:
1
14
. .
24.
Abdel-Maksoud
FM
,
Fadl
S
,
Abou-Elmagd
A
,
Saleh
AMM
.
Post-hatching developmental changes in the adrenal gland of the Japanese quail (Coturnix coturnix japonica): histological, immunohistochemical, and electron microscopic studies
.
Microsc Res Tech
.
2023
;
86
(
11
):
1461
74
. .
25.
Abdel-Maksoud
FM
,
Zayed
AE
,
Abdelhafez
EA
,
Hussein
MT
.
Seasonal variations of the epididymis in donkeys (Equus asinus) with special reference to blood epididymal barrier
.
Microsc Res Tech
.
2024
;
87
(
2
):
326
38
. .
26.
Fadl
S
,
Saleh
AMM
,
Abou-Elmagd
A
,
Abdel-Maksoud
FM
.
Prehatching development of the adrenal gland in Japanese quail (Coturnix japonica): histological, immunohistochemical, and electron microscopic studies
.
Microsc Res Tech
.
2023
. .
27.
Luo
W
.
Investigating rabbit persistent retinal neovascularization (PRNV) model leveraging artificial intelligence (AI)-assisted OCT & FA assessment
.
Invest Ophthalmol Vis Sci
.
2023
;
64
(
8
):
277
.
28.
Michaelson
IC
,
Friedenwald
JS
.
Retinal circulation in man and animals
.
Literary Licensing
;
1954
.
29.
Yu
DY
,
Cringle
SJ
.
Oxygen distribution and consumption within the retina in vascularised and avascular retinas and in animal models of retinal disease
.
Prog Retin Eye Res
.
2001
;
20
(
2
):
175
208
. .
30.
Euler
T
,
Haverkamp
S
,
Schubert
T
,
Baden
T
.
Retinal bipolar cells: elementary building blocks of vision
.
Nat Rev Neurosci
.
2014
;
15
(
8
):
507
19
. .
31.
Ehrenhofer
MC
,
Deeg
CA
,
Reese
S
,
Liebich
HG
,
Stangassinger
M
,
Kaspers
B
.
Normal structure and age-related changes of the equine retina
.
Vet Ophthalmol
.
2002
;
5
(
1
):
39
47
. .
32.
Sandmann
D
,
Boycott
BB
,
Peichl
L
.
Blue-cone horizontal cells in the retinae of horses and other equidae
.
J Neurosci
.
1996
;
16
(
10
):
3381
96
. .
33.
Balasubramanian
R
,
Gan
L
.
Development of retinal amacrine cells and their dendritic stratification
.
Curr Ophthalmol Rep
.
2014
;
2
(
3
):
100
6
. .
34.
Jeon
CJ
,
Strettoi
E
,
Masland
RH
.
The major cell populations of the mouse retina
.
J Neurosci
.
1998
;
18
(
21
):
8936
46
. .
35.
Hussein
MT
,
Attaai
A
,
Kamel
G
,
Mokhtar
DM
.
Spatiotemporal expression of sonic hedgehog signalling molecules in the embryonic mesencephalic dopaminergic neurons
.
Gene Expr Patterns
.
2021
;
42
:
119217
. .
36.
Müller
B
,
Peichl
L
.
Morphology and distribution of catecholaminergic amacrine cells in the cone-dominated tree shrew retina
.
J Comp Neurol
.
1991
;
308
(
1
):
91
102
. .
37.
Oh
SJ
,
Kim
IB
,
Lee
EJ
,
Kim
KY
,
Kim
HI
,
Chun
MH
.
Immunocytological localization of dopamine in the Guinea pig retina
.
Cell Tissue Res
.
1999
;
298
(
3
):
561
5
. .
38.
Mariani
AP
,
Hokoc
JN
.
Two types of tyrosine hydroxylase-immunoreactive amacrine cell in the rhesus monkey retina
.
J Comp Neurol
.
1988
;
276
(
1
):
81
91
. .
39.
Doyle
SE
,
Grace
MS
,
McIvor
W
,
Menaker
M
.
Circadian rhythms of dopamine in mouse retina: the role of melatonin
.
Vis Neurosci
.
2002
;
19
(
5
):
593
601
. .
40.
Besharse
JC
,
McMahon
DG
.
The retina and other light-sensitive ocular clocks
.
J Biol Rhythms
.
2016
;
31
(
3
):
223
43
. .
41.
Jackson
CR
,
Ruan
GX
,
Aseem
F
,
Abey
J
,
Gamble
K
,
Stanwood
G
, et al
.
Retinal dopamine mediates multiple dimensions of light-adapted vision
.
J Neurosci
.
2012
;
32
(
27
):
9359
68
. .
42.
Marc
RE
,
Anderson
JR
,
Jones
BW
,
Sigulinsky
CL
,
Lauritzen
JS
.
The AII amacrine cell connectome: a dense network hub
.
Front Neural Circuits
.
2014
;
8
:
104
. .
43.
Zhao
X
,
Wong
KY
,
Zhang
DQ
.
Mapping physiological inputs from multiple photoreceptor systems to dopaminergic amacrine cells in the mouse retina
.
Sci Rep
.
2017
;
7
(
1
):
7920
14
. .
44.
Kim
J-H
,
Kim
JH
,
Park
JA
,
Lee
SW
,
Kim
WJ
,
Yu
YS
, et al
.
Blood-neural barrier: intercellular communication at glio-vascular interface
.
BMB Rep
.
2006
;
39
(
4
):
339
45
. .
45.
Wincewicz
A
,
Urbaniak-Wasik
S
,
Urbaniak
A
,
Mościcka-Rylska
M
,
Woltanowska
M
,
Koda
M
, et al
.
Review on retinal gliosis illustrated with a series of massive glioses and focal nodular gliosis cases in regard to potential pitfalls of ocular reactive tumor-like lesions of this type
.
Folia Med Plovdiv
.
2018
;
60
(
1
):
30
8
. .
46.
Donato
R
.
Intracellular and extracellular roles of S100 proteins
.
Microsc Res Tech
.
2003
;
60
(
6
):
540
51
. .
47.
Karim
MM
,
Itoh
H
.
Demonstration of S-100 protein immunoreactivity in normal human retina and retinoblastoma
.
Ophthalmologica
.
1997
;
211
(
6
):
351
3
. .
48.
Molnar
ML
,
Stefansson
K
,
Molnar
GK
,
Tripathi
RC
,
Marton
LS
.
Species variations in distribution of S100 in retina. Demonstration with a monoclonal antibody and a polyclonal antiserum
.
Invest Ophthalmol Vis Sci
.
1985
;
26
(
3
):
283
8
.
49.
Du
J
,
Yi
M
,
Zhou
F
,
He
W
,
Yang
A
,
Qiu
M
, et al
.
S100B is selectively expressed by gray matter protoplasmic astrocytes and myelinating oligodendrocytes in the developing CNS
.
Mol Brain
.
2021
;
14
:
154
11
. .
50.
Vecino
E
,
Rodriguez
FD
,
Ruzafa
N
,
Pereiro
X
,
Sharma
SC
.
Glia-neuron interactions in the mammalian retina
.
Prog Retin Eye Res
.
2016
;
51
:
1
40
. .
51.
Hamon
A
,
Roger
JE
,
Yang
XJ
,
Perron
M
.
Müller glial cell-dependent regeneration of the neural retina: an overview across vertebrate model systems
.
Dev Dyn
.
2016
;
245
(
7
):
727
38
. .
52.
Dreher
Z
,
Robinson
SR
,
Distler
C
.
Müller cells in vascular and avascular retinae: a survey of seven mammals
.
J Comp Neurol
.
1992
;
323
(
1
):
59
80
. .
53.
Liu
C
,
Li
CP
,
Wang
JJ
,
Shan
K
,
Liu
X
,
Yan
B
.
RNCR3 knockdown inhibits diabetes mellitus-induced retinal reactive gliosis
.
Biochem Biophys Res Commun
.
2016
;
479
(
2
):
198
203
. .
54.
Guerin
CJ
,
Wolfshagen
RW
,
Eifrig
DE
,
Anderson
DH
.
Immunocytochemical identification of Muller’s glia as a component of human epiretinal membranes
.
Invest Ophthalmol Vis Sci
.
1990
;
31
(
8
):
1483
91
.
55.
Boycott
B
,
Wässle
HJ
.
The morphological types of ganglion cells of the domestic cat’s retina
.
J Physiol
.
1974
;
240
(
2
):
397
419
. .
56.
Wong
R
,
Hughes
AJ
.
The morphology, number, and distribution of a large population of confirmed displaced amacrine cells in the adult cat retina
.
J Comp Neurol
.
1987
;
255
(
2
):
159
77
. .
57.
Bunt
AH
,
Minckler
DS
.
Displaced ganglion cells in the retina of the monkey
.
Invest Ophthalmol Vis Sci
.
1977
;
16
(
1
):
95
8
.
58.
Bunt
AH
,
Lund
RD
,
Lund
JS
.
Retrograde axonal transport of horseradish peroxidase by ganglion cells of the albino rat retina
.
Brain Res
.
1974
;
73
(
2
):
215
28
. .
59.
Dräger
UC
,
Olsen
JF
.
Origins of crossed and uncrossed retinal projections in pigmented and albino mice
.
J Comp Neurol
.
1980
;
191
(
3
):
383
412
. .
60.
Robson
JA
,
Holländer
H
.
Displaced ganglion cells in the rabbit retina
.
Invest Ophthalmol Vis Sci
.
1984
;
25
(
12
):
1376
81
.
61.
Mastronarde
DN
.
Interactions between ganglion cells in cat retina
.
J Neurophysiol
.
1983
;
49
(
2
):
350
65
. .
62.
Hicks
D
.
Characterization and possible roles of fibroblast growth factors in retinal photoreceptor cells
.
Keio J Med
.
1996
;
45
(
3
):
140
54
. .
63.
Jacquemin
E
,
Halley
C
,
Alterio
J
,
Laurent
M
,
Courtois
Y
,
Jeanny
JC
.
Localization of acidic fibroblast growth factor (aFGF) mRNA in mouse and bovine retina by in situ hybridization
.
Neurosci Lett
.
1990
;
116
(
1–2
):
23
8
. .
64.
Noji
S
,
Matsuo
T
,
Koyama
E
,
Yamaai
T
,
Nohno
T
,
Matsuo
N
, et al
.
Expression pattern of acidic and basic fibroblast growth factor genes in adult rat eyes
.
Biochem Biophys Res Commun
.
1990
;
168
(
1
):
343
9
. .
65.
Bugra
K
,
Oliver
L
,
Jacquemin
E
,
Laurent
M
,
Courtois
Y
,
Hicks
D
.
Acidic fibroblast growth factor is expressed abundantly by photoreceptors within the developing and mature rat retina
.
Eur J Neurosci
.
1993
;
5
(
12
):
1586
95
. .
66.
Elde
R
,
Cao
YH
,
Cintra
A
,
Brelje
TC
,
Pelto-Huikko
M
,
Junttila
T
, et al
.
Prominent expression of acidic fibroblast growth factor in motor and sensory neurons
.
Neuron
.
1991
;
7
(
3
):
349
64
. .
67.
Barnstable
CJ
.
Chapter 3 Molecular aspects of development of mammalian optic cup and formation of retinal cell types
.
Prog Retin Res
.
1991
;
10
:
45
67
. .
68.
Guillonneau
X
,
Régnier-Ricard
F
,
Laplace
O
,
Jonet
L
,
Bryckaert
M
,
Courtois
Y
, et al
.
Fibroblast growth factor (FGF) soluble receptor 1 acts as a natural inhibitor of FGF2 neurotrophic activity during retinal degeneration
.
Mol Biol Cell
.
1998
;
9
(
10
):
2785
802
. .
69.
Sapieha
PS
,
Peltier
M
,
Rendahl
KG
,
Manning
WC
,
Di Polo
A
.
Fibroblast growth factor-2 gene delivery stimulates axon growth by adult retinal ganglion cells after acute optic nerve injury
.
Mol Cell Neurosci
.
2003
;
24
(
3
):
656
72
. .
70.
Dono
R
,
Texido
G
,
Dussel
R
,
Ehmke
H
,
Zeller
R
.
Impaired cerebral cortex development and blood pressure regulation in FGF-2-deficient mice
.
EMBO J
.
1998
;
17
(
15
):
4213
25
. .
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