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Anat Histol Embryol. 2021;00:1–11. wileyonlinelibrary.com/journal/ahe
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1© 2021 Wiley-VCH GmbH
1 | INTRODUCTION
The complex anatomical composition of the brain makes it s physical
exploration difficult, and it requires introduction of a high definitive
diagnostic technique. Computed tomography (CT) is characterized
by a high resolution and discrimination of the soft tissue ( Abdel
Maksoud, 2020; Blanco et al., 2015; Morrow et al., 2000; Zafra et al.,
2012), but it does not transcend to soft tissue discrimination and
differentiation given by magnetic resonance imaging (MRI) (Abdel
Maksoud, 2020, 2021; Hagag & Tawfiek, 2018; Thrall, 2013). So,
MRI is a preferable diagnostic imaging technique used for evaluation
and diagnosis of the brain tissue due to its excellent soft tissue con-
trast (Abedellaah et al., 2015; Schmidt et al., 2019).
MRI is commonly used in human medicine for the study of
normal brain anatomy (Alkan et al., 2009; Fillmore et al., 2015;
Goncalves- Ferreira et al., 2001; Ismail et al., 2017) and also for eval-
uation of the neurological disorders of the central nervous system
(Arnold & Matthews, 2002; Gordon & Dennis 1995; Junge et al.,
2017; Snellman et al., 1999). In addition, there is increased attention
in human brain mapping for relating the functions of the underlying
Received: 19 June 2021
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Accepted: 18 September 2021
DOI : 10.1111/a he.12744
ORIGINAL ARTICLE
Morphological characteristics of the forebrain in the donkey
(Equus asinus): A compared atlas of magnetic resonance imaging
and cross- sectional anatomy
Mohamed K. M. Abdel Maksoud1 | Fatma M. Halfaya2 | HebatAllah H. Mahmoud1 |
Azza A. H. Ibrahim1
1Anatomy and Embryology Department,
Faculty of Veterinary Medicine, Beni- Suef
University, Beni- Suef, Egypt
2Surgery, Anesthesiology and Radiology
Depar tment, Faculty of Veterinary
Medicine, Beni- Suef University, Beni- Suef,
Egypt
Correspondence
Mohamed Kamal Merai Abdel Maksoud,
Anatomy and Embryology Department,
Faculty of Veterinary Medicine, Beni- Suef
University, Beni- Suef 62511, Egypt.
Email: mkamalvet@gmail.com
Abstract
The brain is the most essential part of the central nervous system which regulates
and coordinates all body activities. Based on its phylogenetic development from the
neural tube, the brain is divided into rhombencephalon (hindbrain), mesencephalon
(midbrain) and prosencephalon (forebrain). The present study is achieved to describe
the morphological characteristics of the normal forebrain in the donkey using the
matched magnetic resonance imaging (MRI) and cross- sectional anatomy. Ten cadav-
eric heads of healthy adult donkeys of both sexes were used. Two heads were ex-
amined using a 1.5 Tesla MRI scanner, and the brains of the other heads were gently
extracted; six brains were sectioned into transverse, dorsal and sagittal slices, and
two brains were grossly inspected. MR images were selected in correlation to their
closely corresponding gross sections. Both cross- sectional anatomy and MRI scans
showed extensive gyration of the neocortex. The forebrain structures appeared with
variable intensities on three sequences, Flair, T1- weighted and T2- weighted MRI, ena-
bling comprehensive evaluation of the relevant neuroanatomical structures. The pre-
sent study provided a precise neuroanatomical atlas of the forebrain in the donkey
which could help in the quick and efficient interpretation of clinical diseases of the
forebrain, localization of the forebrain functions and evolutionary neurobiology.
KEYWORDS
cross- sectional anatomy, donkey, forebrain, magnetic resonance imaging, morphology
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A BDEL MAKSOU D Et AL.
brain structures using functional image studies (Amunt s et al., 2007;
Devlin & Poldrack, 2007). In veterinar y practices, MRI is currently
used for the evaluation of the brain in small animals (Hudson et al.,
1995; Martin- Vaquero et al., 2011; Mogicato et al., 2011b; Mogicato
et al., 2011a). The application of MRI in large animal medicine is lim-
ited by procedural problems of obtaining MR images (Jef fery et al.,
1992). However, these procedures have been developed and MRI
becomes readily available to be used in the study of the brain in
horse (Arencibia et al., 2001; Chaffin et al., 1997; Kimberlin et al.,
2017; Schmidt et al., 2019), camel (Abedellaah et al., 2015; Arencibia
et al., 2005) and domestic ruminant s (Schmidt et al., 2009, 2012;
Tsuka & Taura, 1999; Tzuka et al., 2008; Wemheuer et al., 200 4).
Identification and segmentation of MR images was a challeng-
ing problem due to the absence of an anatomical model that fully
describes each structure (Greeshma, 2019). So, it is necessary to
understand the normal cross- sectional anatomy of the brain for
accurate interpretation of MRI. To the authors’ knowledge, little
attention is paid to combine cross- sectional anatomy and MRI for
the description of the normal brain especially in the donkey. The
objective of this study is to describe the morphological characteris-
tics of the normal forebrain in the donkey using the matched cross-
sectional anatomy and MRI.
2 | MATERIALS AND METHODS
2.1 | Animals
The study was conducted on ten adult healthy donkeys (8- 15years
old) of both sexes. The donkeys were sedated with 2mg/kg xylazine
HCl 2% (Xyla- Ject, ADWIA Co., SAE, Egypt) injected intramuscularly.
Euthanasia was performed using 50mg of sodium pentobarbital per
kg of bodyweight intravenous (I/V). No neurological disorders were
detected at previous clinical examination. The heads were severed
at the atlanto- axial joint immediately after euthanasia. The heads
were rinsed using tap water and stored at 4ᵒC. All procedures related
to the used animals in this study were approved by the Institutional
Animal Care and Use Committee of Beni- Suef University, Egypt
(2020- BSUV- 57, adopted on 20 February 2020).
2.2 | Magnetic resonance imaging study
Two heads were subjected to MRI within one hour from euthanasia.
Using a standard human knee coil, the heads were positioned with
their dorsal aspects facing the examination t able. Flair, T1- and T2-
weighted spin- echo sequences were obtained in transverse, dorsal
and sagit tal planes using a 1.5 Tesla magnet (Philips Intera, Holland).
The acquisitions parameters are given in Table 1. The total scan time
was about 3 hours for the two examined heads. 3D sequences of
the serial slices were automatically reconstructed, and MR images
in each plane were manually segmented using graphical software
(eFilm Workstation™, Merge Healthcare, Washington, USA).
2.3 | Anatomical study
The common carotid arteries of the eight heads were thoroughly
washed usi ng normal saline so lution to be injected with 10% formal in
solution, and then, the specimens were kept in 10% formalin solution
for one week (Adam et al., 2016). The frontal, temporal, inter- parietal
and occipital bones were carefully removed using an electric band
saw. The brain was carefully extracted from the skull and dura mater
using blunt scissors. Two brains were grossly inspected for identifi-
cation of the normal anatomical structures of the forebrain. The last
six brains were sectioned in 1- cm thick slices using a sharp knife into
TABLE 1 Acquisition parameters for obtaining Flair, T1- and T2- weighted MRI images
MRI sequences
TR
(msec)
TE
(msec)
FOV
(mm)
RFOV
(%)
Slice
thickness
(mm)
Interslice
space (mm) Matrix size
Acq. Tm
(min:s)
No. of
sections
Flair
Transverse 11000 140 25 × 25 81 5 1 192 × 14 8 21:21 20
Sagittal 11000 140 25 × 25 81 5 1 192 × 148 21:27 18
Dorsal 11000 140 25 × 25 81 5 1 192 × 148 21:15 20
T1- weighted
Transverse 540 150 21 × 21 71 5 1 212 × 17 21:18 20
Sagittal 486 150 24 × 24 93 5 1 220 × 177 21:26 18
Dorsal 540 150 25 × 25 81 5 1 228 × 182 21:14
T2- weighted
Transverse 4073 100 24 × 24 81 5 1 26 8 × 250 21:20 20
Sagittal 3646 100 23 × 23 94 5 1 328 × 258 21:24 18
Dorsal 4079 10 0 26 × 26 81 5 1 288 × 218 21:12 20
Abbreviations: Acq Tm, acquisition time; FOV, field of view; RFO, rectangular field of view (%);TE, echo delay time; TR, repetition time.
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ABDEL MA KSOUD Et AL .
transverse (2 brains), dorsal (2 brains) and sagittal (2 brains) slices.
The anatomical sections were serially numbered, and their anatomi-
cal structures were inspected and identified.
2.4 | Matching of the MR images with the
anatomical sections
The cross- anatomical sections and their closely corresponding MR
images were matched in three planes; five in transverse (Figures
1- 5), two in sagittal (Figures 6- 7) and t wo in dorsal (Figures 8- 9). MR
images were interpreted, and the signal intensities of each structure
were detected in the applied sequences: Flair, T1- and T2- weighted
MRI. These planes were obtained in correspondence to reference
lines along with the whole brain in the right lower corners of the
transverse images and the left upper corners of the sagittal and dor-
sal ones.
FIGURE 1 Transverse images of the brain at the level of the
rostral piriform lobe. (a) Transverse anatomical section and (b)
T1- weighted magnetic resonance image: an— accumbens nucleus,
dg— diagonal gyrus, cg— cingulate gyrus, ci— cingulum, cn— caudate
nucleus (head), cs— coronal sulcus, ds— diagonal sulcus, ec— external
capsule, esg— ectosylvian gyrus, ess— ectosylvian sulcus, cc— corpus
callosum, gs— genual sulcus, is— insula, lf— cerebral longitudinal
fissure, ln— lentiform nucleus, log— lateral olfactory gyrus, lot—
lateral olfactory tract, lrs— lateral rhinal sulcus, lv— lateral ventricle,
mot— medial olfactory tract, on— optic ner ve, pog— postcruciate
gyrus, rc— rostral commissure, rcc— radiation of corpus callosum,
rpl— rostal piriform lobe, sc— semi- oval centre, scf— subcallosal
fasciculus, sf— sylvian fissure, sg— sylvian gyrus, sp— septum
pellucidum, ssg— suprasylvian gyrus, sss— suprasylvian sulcus
(a)
(b)
FIGURE 2 Transverse images of the brain at the level of the
optic chiasma. (a) Transverse anatomical section and (b) T2-
weighted magnetic resonance image: as— ansate sulcus, cc—
corpus callosum, cg— cingulate gyrus, ci— cingulum, cl— claustrum,
cn— caudate nucleus (body), cpv— choroid plexus of the lateral
ventricle, dg— diagonal gyrus, ec— external capsule, ers— endorhinal
sulcus, esg— ectosylvian gyrus, ess— ectosylvian sulcus, ic— internal
capsule, is— insula, lf— cerebral longitudinal fissure, lml— lateral
medullary lamina, lrs— lateral rhinal sulcus, lv— lateral ventricle,
mg— marginal gyrus, ms— marginal sulcus, oc— optic chiasma, ou—
olfactory tubercle, pl— pallidum, ps— rostral perforate substance,
pt— putamen, rc— rostral commissure, rcc— radiation of corpus
callosum, sa— striate artery, sc— semi- oval centre, scc— supracallosal
sulcus, scg— supracallosal gyrus, scf— subcallosal fasciculus, sf—
sylvian fissure, sg— sylvian gyrus, sm— supracommissural part of
the hippocampus, sn— septal nuclei, sp— septum pellucidum, ss—
splenial sulcus, ssg— suprasylvian gyrus, sss— suprasylvian sulcus,
ts— terminal stria
(a)
(b)
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A BDEL MAKSOU D Et AL.
The anatomical terms used in this study complied with Schaller
(2007) and Nomina Anatomica Veterinaria (2017).
3 | RESULTS
The forebrain of the donkey included the diencephalon and telen-
cephalon; the latter consisted of the two cerebral hemispheres and
their commissural fibres.
3.1 | Cerebral hemispheres
The two cerebral hemispheres of the donkey were separated by
a cerebral longitudinal fissure (Figures 1- 5, 8, 9; lf). Based on its
FIGURE 3 Transverse images of the brain at the level of the
tuber cinereum. (a) Transverse anatomical section and (b) T1-
weighted magnetic resonance image: as— ansate sulcus, bf— body
of fornix, cc— corpus callosum, cg— cingulate gyrus, ci— cingulum,
cl— claustrum, cn— caudate nucleus (body), cof— column of fornix,
cpl— caudal piriform lobe, dg— diagonal gyrus, ec— external capsule,
esg— ectosylvian gyrus, ess— ectosylvian sulcus, ic— internal
capsule, if— infundibulum, is— insula, lf— cerebral longitudinal
fissure, lrs— lateral rhinal sulcus, lv— lateral ventricle, mg— marginal
gyrus, ms— marginal sulcus, ot— optic tract, pl— pallidum, ptg—
pituitary gland, pt— putamen, rcc— radiation of corpus callosum,
sc— semi- oval centre, scf— subcallosal fasciculus, sf— sylvian fissure,
sfo— subfornical organ, sg— sylvian gyrus, sm— supracommissural
part of the hippocampus, sp— septum pellucidum, ss— splenial
sulcus, ssg— suprasylvian gyrus, sss— suprasylvian sulcus, tc— tuber
cinereum, tv— third ventricle
(a)
(b)
FIGURE 4 Transverse images of the brain at the level of the
mamillar y body. (a) Transverse anatomical section and (b) Flair
magnetic resonance image: ab— amygdaloid body, cc— corpus
callosum, cf— commissure of fornix, cg— cingulate gyrus, ci—
cingulum, cn— caudate nucleus (tail), cpl— caudal piriform lobe,
cpt— choroid plexus of the third ventricle, crc— cerebral crus, esg—
ectosylvian gyrus, ess— ectosylvian sulcus, et— external thalamic
medullary lamina, gi— genu of internal capsule, gt— grey terminal
lamina, hp— hippocampus proper, ht— habenular thalamic stria,
ia— inter- thalamic adhesion, it— internal thalamic medullary lamina,
iv— interventricular foramen, lf— cerebral longitudinal fissure, lg—
lateral geniculate body, lrs— lateral rhinal sulcus, ltn— lateral thalamic
nuclei, lv— lateral ventricle, mb— mamillary body, mg— marginal
gyrus, ms— marginal sulcus, mt— mamillo- thamic tract, og— oblique
gyrus, os— oblique sulcus, ot— optic tract, phg— parahippocampal
gyrus, pv— paraventricular thalamic nuclei, rcc— radiation of corpus
callosum, rtn— rostral thalamic nuclei, scc— supracallosal sulcus,
scf— subcallosal fasciculus, scg— supracallosal gyrus, sf— sylvian
fissure, sg— sylvian gyrus, sp— septum pellucidum, ss— splenial
sulcus, ssg— suprasylvian gyrus, sss— suprasylvian sulcus, tr—
thalamic reticular nucleus, ts— terminal stria, tv— third ventricle,
zl— zonal layer of thalamus
(a)
(b)
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ABDEL MA KSOUD Et AL .
structural components, each hemisphere presented white and grey
matter; both matter and the cerebrospinal fluid within the cerebral
hemisphere could be depicted with variable signal intensities on
different MRI sequences (Flair, T1- and T2- weighted) as shown in
Table 2. Morphologically, the hemispheres consisted of the dorsal
and basal surfaces; the latter sur face was subdivided into medial and
lateral parts. The lateral part of the basal sur face was related to the
corpus striatum, while the medial one was related to the rhinenceph-
alon. The dorsal surface of the hemispheres was referred to as the
cerebral cortex (neocortex).
FIGURE 5 Transverse images of the brain at the level of
cerebral crus. (a) Transverse anatomical section and (b) T1-
weighted magnetic resonance image: ah— Amon's horn, av—
alveus of hippocampus, dtg— dentate gyrus, cc— corpus callosum,
cf— commissure of fornix, cg— cingulate gyrus, cgm— central grey
mater, ci— cingulum, cpl— caudal piriform lobe, crc— cerebral crus,
emg— ectomarginal gyrus, ems— ectomarginal sulcus, fh— fimbria
of hippocampus, hb— habenula, hc— habenular commissure,
hn— habenular nucleus, hp— hippocampus proper, lf— cerebral
longitudinal fissure, lv— lateral ventricle, ma— mesoencephalic
aqueduct, mg— marginal gyrus, ms— marginal sulcus, phg—
parahippocampal gyrus, pn— pulvinar nuclei, rcc— radiation of
corpus callosum, rn— red nucleus, sbn— substantia nigra, scf—
subcallosal fasciculus, sf— sylvian fissure, sg— sylvian gyrus,
sh— hippocampal sulcus, ss— splenial sulcus, ssg— suprasylvian
gyrus, sss— suprasylvian sulcus, te— thalamic tenia, tlv— temporal
horn of the lateral ventricle
(a)
(b)
FIGURE 6 Mid- sagittal images of the brain at the level of the
inter- thalamic adhesion. (a) Transverse anatomical section and (b)
T2- weighted magnetic resonance image: as— ansate sulcus, bcc—
body of corpus callosum, bf— body of fornix, cb— cerebellum, ci—
cingulum, cpt— choroid plexus of the third ventricle, crc— cerebral
crus, ens— endomarginal sulcus, fv— fourth ventricle, gcc— genu of
corpus callosum, gs— genual sulcus, ia— inter- thalamic adhesion,
ma— mesencephalic aqueduct, ss— splenial sulcus, pg— prorean
gyrus, mrs— medial rhinal sulcus, mb— mamillary body, mot— medial
olfactory tract, mst— mesencephalic tectum, oc— optic chiasma, on—
optic ner ve, png— pineal gland, po— pons, rc— rostral commissure,
rpl— rostral pirifrm lobe, sb— subcallosal area, spc— splenium of
corpus callosum, sm— supracommissural part of the hippocampus,
sn— septal nuclei, ss— suprasplenial sulcus, tc— tuber cinereum, tcc—
rostrum of corpus callosum, tv— third ventricle
(a)
(b)
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A BDEL MAKSOU D Et AL.
3.1.1 | Rhinencephalon
The rhinencephalon of the donkey was divided into three parts:
basal, septal and limbic.
The basal part of the rhinencephalon
The rhinencephalon began rostrally by the olfactory bulb which was
found rostroventral to the frontal pole of each hemisphere (Figure 7;
ob). This bulb joined caudally with the hemisphere through short
white fibre bundles, the olfactor y peduncle (Figure 7: op), which was
demarcated ventrally from the olfactory bulb by the limiting sulcus of
the olfactory bulb (Figure 7; lso), and bounded medially and laterally
by the medial (Figures 6, 7; mrs) and lateral rhinal sulci (Figures 1- 4;
lrs) respectively. The olfactory peduncle divided caudally into medial
(Figures 1 , 6; mot) and lateral olf actory tra cts (Figure 1; lot). T he latter
tract was bounded laterally by the lateral olfactory gyrus (Figure 1;
log). Both medial and lateral olfactory tracts housed a triangular grey
mass, the rostral piriform lobe (Figures 1, 6, 7; rpl). Caudal to this lobe
was the olfactory tubercle (Figure 2; ou) which was bounded laterally
by the endorhinal sulcus (Figure 2; ers). Another large lobe, caudal pi-
riform lobe could be depicted (Figures 3- 5; cpl). The rostral perforate
substance (Figure 2; ps) was the caudolateral part of the olfactor y
tubercle and perforated by the striate arteries (Figure 2; sa).
The septal part of the rhinencephalon
The septal part of the rhinencephalon was located on the medial
aspect of each cerebral hemisphere and included the diagonal gyrus,
septum pellucidum, subcallosal area and septal nuclei. The diagonal
gyrus (Figures 1- 3; dg) was separated from the insula (Figure 1; is)
by the diagonal sulcus (Figure 1; ds). The septum pellucidum was a
thin layer of white mass connecting the corpus callosum with the
fornix (Figures 1- 4, 8, 9; sp). The subcallosal area was a small grey
substance found rostroventral to the rostrum of the corpus callo-
sum (Figure 6; sb). The septal nuclei appeared as a longitudinal grey
structure at the medioventral border of each hemisphere at the level
of the rostral commissure (Figures 2, 6; sn).
The limbic part of the rhinencephalon
The limbic part of the rhinencephalon included rostral commissure,
hippocampus, fornix, amygdaloid body and terminal stria. The rostral
commissure appeared as an inverted U- shape ventral to the septum
pellucidum on transverse images (Figures 1, 2; rc) and a bridge of
white matter rostroventral to the inter- thalamic adhesion on sagittal
images (Figures 6, 7; rc).
In relation to the rostral commissure, the hippocampus could
be divided morphologically into two parts: supracommissural and
retrocommissural. The supracommissural part of the hippocampus
appeared as a thin layer of grey matter dorsal to the corpus callo-
sum (Figures 2, 3, 6- 9; sm) and continued dorsally with the supracal-
losal gyrus (Figures 2, 4, 7; scg) which separated from the cingulate
gyrus (Figures 1- 5, 8, 9; cg) by the supracallosal sulcus (Figures 2, 4;
scc). The latter sulcus continued rostral to the genu of the corpus
callosum as a genicular gyrus (Figure 7; gg). In addition, the retro-
commissural part or hippocampus proper appeared as an elongated
convex grey structure located within the medial and caudal parts
of the lateral ventricle (Figures 4, 5, 8; hp). The internal surface of
the hippocampus was covered by a thin layer of white matter, the
alveus (Figures 5, 7; av), which continued medially into the commis-
sure of the hippocampus (commissure of fornix) (Figures 4, 5, 7; cf)
and converged to form the fimbria of the hippocampus (Figures 5,
7; fh). Between the dorsal and ventral ends of the fimbria, the hip-
pocampus convoluted around himself forming a spiral- like structure
FIGURE 7 Parasagittal images of the brain at the level of
the lateral ventricle. (a) Transverse anatomical section and (b)
T2- weighted magnetic resonance image: ah— Amon's horn, an—
accumbens nucleus, av— alveus of hippocampus, bcc— body of
corpus callosum, cb— cerebellum, cca— caudal calliculus, cf—
commissure of fornix, ci— cingulum, cn— caudate nucleus, crc—
cerebral crus, crs— cruciate sulcus, eng— endomarginal gyrus, esg—
ectosylvian gyrus, fg— fasciolar gyrus, fh— fimbria of hippocampus,
gcc— genu of corpus callosum, gg— genicular gyrus, lv— lateral
ventricle, lso— limiting sulcus of the olfactory bulb, mb— mamillary
body, mdt— medullary stria of thalamus, mrs— medial rhinal sulcus,
mt— mamillo- thalamic tract, ob— olfactory bulb, oc— optic chiasma,
on— optic nerve, op— olfactory pudencle, pcg— precruciate gyrus,
pg— prorean gyrus, po— pons, prs— prorean sulcus, pt a— pretectum
area, rc— rostral commissure, rca— rostral calliculus, rpl— rostral
piriform lobe, spc— splenium of corpus callosum, scg— supracallosal
gyrus, scs— supracallosal sulcus, sm— supracommissural part of
the hippocampus, stn— subthalamic nucleus, tc— tuber cinereum,
tcc— rostrum of corpus callosum, th— thalamus, zn— uncertain zone
(a)
(b)
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ABDEL MA KSOUD Et AL .
(Ammon's horn) (Figures 5, 7, 9; ah). Ventrally, the hippocampus was
demarcated from the caudal piriform lobe by the hippocampal sul-
cus (Figure 5; sh) which separated between the parahippocampal
gyrus (Figures 4, 5, 9; phg) and the dentate gyrus (Figure 5; dtg). The
latter gyrus continued dorsally and caudally under the splenium of
the corpus callosum as a fasciolar gyrus (Figure 7; fg).
The forni x was white matter fi bres located with in the midline of the
brain and extended from the septum pellucidum to the thalamus. The
FIGURE 8 Dorsal images of the brain at the level of the septum pellucidum. (a) Transverse anatomical section and (b) T2- weighted
magnetic resonance image: bf— body of fornix, ds— diagonal sulcus, cc— corpus callosum, cg— cingulate gyrus, ci— cingulum, cn— caudate
nucleus, cof— column of fornix, cpv— choroid plexus of lateral ventricle, c s— coronal sulcus, emg— ectomarginal gyrus, ens— endomarginal
sulcus, ess— ectosylvian sulcus, gs— genual sulcus, hp— hippocampus proper, lf— cerebral longitudinal fissure, lv— lateral ventricle, mg—
marginal gyrus, ocg— occipital gyrus, pcg— precruciate gyrus, rcc— radiation of corpus callosum, scf— subcallosal fasciculus, sf— sylvian fissure,
sm— supracommissural part of the hippocampus, sp— septum pellucidum, ss— splenial sulcus, ssg— suprasylvian gyrus, th— thalamus
(a) (b)
FIGURE 9 Dorsal images of the brain at the level of the mesencephalic aqueduct. (a) Transverse anatomical section and (b) T1- weighted
magnetic resonance image: ah— Amon's horn, bf— body of fornix, ds— diagonal sulcus, cc— corpus callosum, cg— cingulate gyrus, ci— cingulum,
cl— claustrum, clc— central lobule of cerebellum, cn— caudate nucleus, ec— external capsule, gs— genual sulcus, ic— internal capsule, iv—
interventricular foramen, lf— cerebral longitudinal fissure, lg— lateral geniculate body, lv— lateral ventricle, ma— mesencephalic aqueduct,
mgb— medial geniculate body, pcg— precruciate gyrus, pg— prorean g yrus, phg— parahippocampal gyrus, pl— pallidum, prs— prorean sulcus,
pt— putamen, rca— rostral colliculus, rcc— radiation of corpus callosum, rt— reticular thalmic nucleus, scf— subcallosal fasciculus, sf— sylvian
fissure, sm— supracommissural part of the hippocampus, sp— septum pellucidum, th— thalamus, tlv— temporal horn of the lateral ventricle,
tv— third ventricle
(a) (b)
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A BDEL MAKSOU D Et AL.
body of this fornix was found just ventral to the septum pellucidum
(Figures 3 , 6, 8, 9; bf), and its f ibres extended caudally for ming commis-
sure of the fornix which joined the two hippocampi (Figures 4, 5, 7; cf).
Ventrally, the fibres of the body of the fornix diverged bilaterally form-
ing the columns of the fornix (Figures 3, 8; cof ). A small white matter
structure, subfornical organ, was visualized between the t wo columns
of the fornix within the cavity of the third ventricle (Figure 3; sfo).
The amygdaloid body appeared as a grey complex within the
caudal part of the piriform lobe (Figure 4; ab). Slender white fibre
bundles, the terminal stria, surrounded the caudate nucleus and the
thalamus (Figures 2, 4; ts).
3.1.2 | Corpus striatum
The corpus striatum was a large body composed of grey basal nuclei
separated by white fibres including the caudate nucleus, accumbens
nucleus, lentiform nucleus and claustrum. The caudate nucleus was
a large grey substance bulged into the rostrolateral part of the lateral
ventricle and composed of the head (Figures 1, 2; cn), body (Figure 3;
cn) and tail (Figure 4; cn). The accumbens nucleus was found ventro-
medial to the caudate and lentiform nuclei (Figures 1, 7; an). The len-
tiform nucleus was separated from the caudate nucleus by a sheet
of white matter, the internal capsule (Figures 2, 3, 9; ic), and it was
divided into a medial part, the putamen (Figures 2, 3, 9; pt) and a
lateral one, the pallidum (Figures 2, 3, 9; pl). Both putamen and pal-
lidum were separated by the lateral medullary lamina (Figure 2; lml).
The claustrum was an elongated grey lamina separated between the
putamen and insula (Figures 2, 3, 9; cl). Furthermore, the fibres of
the external capsule separated the claustrum from the putamen me-
dially and the insula laterally (Figures 1- 3, 9; ec).
3.1.3 | Neocortex
The neocortex of the donkey showed a mantle- like appearance
which enveloped the underlying brain stem. This cortex had many
gyri and sulci. Each g yrus composed of grey matter from the outside
and white matter from the inside. The prorean gyrus (Figures 6, 7, 9;
pg) and its corresponding sulcus (Figures 7, 9; prs) were positioned
at the most rostroventral part of the frontal lobe of the hemisphere.
The sylvian gyrus (Figures 1- 5; sg), ec tosylvian sulcus (Figures 1- 4,
8; ess) and its corresponding gyrus (Figures 1- 4, 7; esg) were located
dorsolateral to the sylvian fissure (Figures 1- 5, 8, 9; sf). Ventromedial
to the sylvian gyrus was the oblique g yrus (Figure 4; og) and its
sulcus (Figure 4; os). The suprasylvian sulcus (Figures 1- 5; sss) and
its gyrus (Figures 1- 5; ssg) were found dorsomedial to the ectosyl-
vian sulcus. On the caudodorsal aspect of each hemisphere, we de-
picted the marginal sulcus (Figures 2- 5; ms), and its gyrus (Figures
2- 5; mg), ec tomarginal sulcus (Figure 5; ems), and its gyrus (Figure 5;
emg), and endomarginal sulcus (Figures 6, 8; ens) and its correspond-
ing gyrus (Figure 7; eng). The coronal sulcus could be visualized on
the rostrodorsal aspect of each hemisphere (Figures 1, 8; cs) which
continued rostromedially with the ansate sulcus (Figures 2, 3, 6; as).
Rostromedial to the latter sulcus was the cruciate sulcus (Figure 7;
crs) which separated the precruciate gyrus (Figures 7- 9; pcg) from
the postcruciate gyrus (Figure 1; pog).
3.1.4 | The white matter of the cerebral hemisphere
The white matter of the cerebral hemisphere of the donkey formed
a great mass of the deep part of the cerebral hemisphere. It formed a
large semi- oval centre (Figures 1- 3; sc) dorsal to the corpus callosum
and lateral ventricles and sent fibres between the basal nuclei in-
cluding internal and external capsules, and lateral medullary lamina.
In addition, large elongated fibre bundles, subcallosal fasciculus, ex-
tended between the corpus callosum and caudate nucleus (Figures
1- 5, 8, 9; scf). A thin layer of white matter extended into the cin-
gulate gyrus as a cingulum dorsal to the corpus callosum (Figures
1- 9; ci). The latter corpus was located at the bottom of the cerebral
longitudinal fissure and consisted of genu (Figures 6, 7; gcc), rostrum
(Figures 6, 7; tcc), splenium (Figures 6, 7; spc) and body (Figures 6,
7; bcc), as well as, it ex tended rostrodorsally towards the semi- oval
centre by the radiation of the corpus callosum (Figures 1- 5, 8, 9; rcc).
3.2 | Diencephalon
The diencephalon of the donkey included epithalamus, thalamus,
metathalamus, subthalamus and hypothalamus. The basic structures
of the diencephalon either white or grey mat ter, as well as the CSF,
appeared with variable intensities on different MRI sequences (Flair,
T1- and T2- weighted) as shown in Table 2.
The epithalamus was the most caudodorsal part of the dien-
cephalon comprising of the habenula and pineal gland. The latter
gland was a small grey substance projecting into the lateral ventri-
cle (Figure 6; png). This gland was anchored to the thalamus by two
white fibre bands, the habenula (Figure 5; hb). The latter was related
dorsally to the thalamic tenia (Figure 5; te) and extended rostrally as
TABLE 2 The appearance of forebrain tissue (white and grey matter) and cerebrospinal fluid (CSF) of the donkey on three sequences of
magnetic resonance imaging (MRI), Flair, T1- and T2- weighted
Tissue Flair T1 T2
A- Brain tissues
Grey matter Low signal intensity High signal intensity Intermediate signal intensit y
White matter Low signal intensity Intermediate signal intensity Low signal intensity
B- cerebrospinal fluid High signal intensity Low signal intensity High signal intensity
|
9
ABDEL MA KSOUD Et AL .
habenular thalamic stria (Figure 4; ht) which enlarged caudally due
to the formation of the habenular nucleus (Figure 5; hn). The lat ter
nucleus interconnected by crossed white fibres, the habenular com-
missure (Figure 5; hc).
The thalamus was the most rostral part of the diencephalon and
related rostrally to the caudal part of the caudate nucleus (Figures 7-
9; th). The two thalami were connected at the midline of the brain by
the inter- thalamic adhesion (Figures 4, 6; ia). Each thalamus was cov-
ered by a thin layer of white fibres, the zonal layer of the thalamus
(Figure 4; zl), and comprised of nuclear masses separated by thin lay-
ers of white fibres including the rostral thalamic nuclei (Figure 4; r tn),
the paraventricular thalamic nuclei (Figure 4; pv) and pulvinar nu-
cleus (Figure 5; pn). Moreover, the rostral thalamic nuclei were sep-
arated from the lateral thalamic nuclei (Figure 4; ltn) by a thin layer
of white fibres, the internal thalamic medullary lamina (Figure 4; it).
Another layer of white fibres, the external thalamic medullary lamina
(Figure 4; et), separated between the lateral thalamic nuclei and the
thalamic reticular nucleus (Figure 4; tr).
The subthalamus was found ventral to the thalamus between the
latter and the midbrain including the subthalamic nucleus and uncer-
tain zone. The latter zone was a thin layer of white matter (Figure 7;
zn) found ventral to the mamillo- thalamic tract (Figures 4, 7; mt). The
subthalamic nucleus was a small grey matter located ventral to the
uncertain zone (Figure 7; stn).
The metathalamus was represented by t wo small grey bodies: a lat-
eral geniculate body (Figures 4, 9; lg) and a medial one (Figure 9; mgb).
The hypothalamus was the ventral part of the diencephalon
extending from the optic chiasma rostrally to the mamillary body
caudally. The optic chiasma was the most rostral part of the hypo-
thalamus (Figures 2, 6, 7; oc). From this chiasma, the right and lef t
optic tracts diverged caudodorsally bet ween the cerebral crura and
the caudal piriform lobes (Figures 3, 4; ot). The tuber cinereum was
a small grey matter found between the optic chiasma and the ma-
millary body (Figures 3, 6, 7; tc). The latter body was an oval white
structure (Figures 4, 6, 7; mb) connected with the thalamus dorsally
through the mamillo- thalamic tract (Figures 4, 7; mt). The roof of the
third ventricle was closed by a plate of grey matter, the grey terminal
lamina (Figure 4; gt). The pituitary gland was a flattened hypointense
structure (Figure 3; ptg) connected to the hypothalamus by a small
stalk, the infundibulum (Figure 3; if).
4 | DISCUSSION
The current study provided a detailed gross anatomical descrip-
tion of the normal forebrain in the donkey using compared cross-
sectional anatomy with their matched MR images which could assist
as an alternative atlas for identification and diagnosis of the central
nervous system disorders. Moreover, the annotated data might help
in establishing a func tional neurological atlas using MRI.
The neocortex varies greatly in size between the mammalian spe-
cies, and it is highlighted evolutionarily to be associated with intel-
ligence and emotional behaviour (Dunbar, 1998; Innocenti & Kaas,
1995; Kaas, 1995). The neocortex of primates which have large- sized
brains tends to expand relative to other neuroanatomical structures
(Finlay & Darlington, 1995). Both gross sections and MR scans of
the donkey forebrain showed extensive gyration of the neocortex.
This pattern of gyration was charac teristic for ungulates and associ-
ated evolutionarily with the increased body weight (Hofman, 1985).
Moreover, the brain of the ungulates was more gyrencephalic than
other mammals of the same bodyweight (Pillay & Manger, 2007).
Furthermore, specific sulci were developed with special senses next
to the allometric expansion of the neocortex (Hofman, 1985). As ex-
amples of this development, the sensory information from the limbs
and trunk is processed in the cortical area of the ectosylvian sulcus,
from the tongue in the suprasylvian sulcus, from the nostrils in the
coronal sulcus and from the lips in the diagonal sulcus (Adrian, 1943;
Takeuchi & Sugita, 2001; Woolsey & Fairman, 1946). However, the
great variability of the gyral and sulcal pattern in the same species
should be considered during mapping and localization of the brain
functions (Amunts et al., 2007; Pakozdy et al., 2015). In addition, the
insular cor tex under investigation was hidden in the sylvian fissure
and oblique sulcus, and it could not be determined on the outer sur-
face, which thought to be due to large extension of the temporal lobe
of the forebrain (Russo et al., 2008; Schmidt et al., 2019).
The transverse, dorsal and sagittal MR images in the current
study were acquired at 5mm slice thickness with 1mm interslice
space to provide an excellent spatial resolution and reduce partial
volume artefacts. Moreover, these images at this slice thickness in
the present study allowed a neuroanatomical reference for the clini-
cal animal practices which require a thicker slice thickness (Mogicato
et al., 2011b). The scanning time used in this study was prolonged;
however, under clinical conditions, a shorter scanning time is recom-
mended to reduce the cost and period of general anaesthesia and
associated risks. Using 3D reconstructed slices allowed a generation
of high signal intensity images and visualization of the entire brain
volume, while the MR planes were manually segmented for accurate
matching with their corresponding cross- sectional slices. Other fac-
tors could affect the resolution of the obtained MR images including
contrast and signal intensity, magnetic field streng th, the receiver
coil and optimized sequence parameters (Schmidt et al., 2012).
T1- and T2- weighted are the commonly used MRI sequences
in the clinical veterinary practices. Fluid attenuation inversion re-
covery (Flair) is an increasingly used MRI sequence in human med-
icine for it s potential visualization of the brain lesions (Rydberg
et al., 1994; Tanaka et al., 20 00), as well as reduction in artefacts
of blood flow and cerebrospinal fluid (Alkan et al., 20 09; Herlihy
et al., 2001). However, recent repor ts used this MRI sequence to
visualize feline brain (Gomes et al., 2009; Magicato et al., 2011b).
Nevertheless, before its use in the clinical animal practices, it
should be shown whether this sequence clarifies some anatom-
ical structures that were not previously depicted in the other
MRI sequences (Gomes et al., 2009; Magicato et al., 2011b). The
compared sequences of MRI, Flair, T1- and T2- weighted used in
this study provided a thorough evaluation of the neuroanatomical
structures and CSF circulating in the brain ventricles; the grey and
10
|
A BDEL MAKSOU D Et AL.
white matter were clearly identified using T1- and T2- weighted MR
images with superior T1- weighted ones, while the CSF was best
delineated using Flair MRI. So, further clinical investigations of the
neuroanatomical lesions in veterinary practices using Flair MRI are
recommended.
Although the labelled MR images provided an excellent con-
trast of the most super ficial nuclei and clinically relevant anatomical
structures of the telencephalon and diencephalon, however, some
structures remained invisible especially the deep nuclei. These re-
sults shared similarities to those of Hudson et al. (1995), Gomes
et al. (2009) and Mogicato et al. (2011a,2011b). However, a study
reported using a contrast- enhanced MRI at 7 Tesla to clarify the
brainstem structures that were not previously visualized at 1.5 Tesla
MRI (Kang et al., 2009). Meanwhile, using this higher operating MRI
unit remained impractical regarding the currently available MRI units
in the clinical veterinary practices.
5 | CONCLUSION
The forebrain of the donkey is characterized by extensive gyration
of the neocortex. The current study provided a detailed neuroana-
tomical atlas of the forebrain in the donkey using variable MRI se-
quences to be a reference for diagnosis and interpretation of the
clinical diseases, localization of the forebrain functions and evolu-
tionary studies.
ACKNOWLEDGEMENT
The authors would like to thank all radiology team, Eman Scan
Radiology Center, Beni- Suef Governorate, for performing MRI
scanning.
CONFLICT OF INTEREST
The authors have no conflic t of interest in the current form of the
manuscript.
DATA AVAIL ABILI TY STATEMENT
The data that support the findings of this study are available from
the corresponding author upon reasonable request.
ORCID
Mohamed K . M. Abdel Maksoud https://orcid.
org/0000-0002-6723-9337
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How to cite this article: Abdel Maksoud, M. K. M., Halfaya, F.
M., Mahmoud, H. H., & Ibrahim, A. A . H. (2021).
Morphological characteristics of the forebrain in the donkey
(Equus asinus): A compared atlas of magnetic resonance
imaging and cross- sectional anatomy. Anatomia, Histologia,
Embryologia, 00, 1– 11. htt ps://doi.org /10.1111/ahe.12744
