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The Morphology of the Brain Base Arteries in the
Sparrowhawk (Accipiter nisus)
Ozudogru, Z., Balkaya, H. and Ozdemir, D.
Ataturk University, Faculty of Veterinary Medicine, Department of Anatomy, Erzurum, Turkey.
* Corresponding Author: Hulya Balkaya, Ataturk University, Faculty of Veterinary Medicine, Department of Anatomy, Erzurum, Turkey.
Tel: +90-442-2317193. E-mail: balkayaibrahim@hotmail.com
AB S T RAC T
This study was aimed at determining the vascular structure of the brain base arteries in the sparrowhawk.
For this purpose, ten hawks were used. Latex injection method was applied to the materials. After careful
dissection, the brain base arteries were investigated. The right and left internal carotid arteries were present
in all of the samples. The cerebral carotid arteries were located in the sphenoid bone. The right and left
cerebral carotid arteries formed an intercarotid anastomosis, placed ventro-caudal to the hypophysis. This
anastomosis was a side-to-side anastomosis in a ‘X’ shape. Both the right and left caudal branches of cerebral
carotid artery developed the basilar artery. The rostral branch was a continuity of the cerebral carotid artery
latero-rostrally in the way of the ventral surface of the cerebral hemisphere. The rostral branch gave off the
caudal cerebral artery, the dorsal tectal mesencephalic artery, the middle cerebral artery, the cerebroethmoidal
artery, the rostral cerebral artery and the ethmoidal artery, during its course. It was hoped that our study will
increase knowldege regarding the structural data on exotic birds since the literature relating to this species
specific vascular anatomy in wild birds is lacking.
Keywords: Brain base arteries; Intercarotid anastomose; Morphology; Sparrowhawk.
INTRODUCTION
Quail hunting with sparrowhawks is commonly used in
northeastern Turkey. In the avian taxonomy, the sparrowhawk
is known as Accipiter nisus. It is a small bird of prey from
the family Accipitridae. Throughout the world there are 50
different species of the genus Accipiter. The sparrowhawk is a
major predator of small birds, especially sparrows (1).
The fundamental structure of the central nervous system
of birds corresponds to that of the other vertebrates. The fully
developed avian brain is divided into the following regions,
from rostral to caudal: the forebrain, the midbrain and the
hind brain (2). Degeneration of cerebral circulation causes
nervous disorders (3). Arterial blood is supplied to the brain
by paired carotid arteries which run medially in the neck before spreading laterally and dividing into external and internal
branches. The internal carotids then run rostro-medially in
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the carotid canals before turning dorso-medially to pass into
the distal sella turcica. Here an intercarotid anastomosis is
formed (4). This communication between the right and left
internal carotids is by means of a transverse connecting vessel
or side to side anastomosis. Functionally, this anastomosis is
the equivalent of the mammalian Circle of Willis (5). There
were some studies on the brain arterial vascularization of
birds, such as: Crowe and Crowe (1979) in helmeted guinea
fowl (6), Midtgard (1984) in seagull (7), Campos (1987) in
fowl (8), Holliday et al. (2006) in flamingo (9), Carvalho
and Campos (2011) in Turkey (10) and Nazer and Campos
(2011) in ostrich (11). In other species particularly wild
birds there is a dearth of information (12-14). To the beset
knowledge of the authors, no literature is available in relation
with the brain arterial vascularization of raptors.
The aim of this study was to research the anatomical
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structure of brain base arteries in sparrowhawk (Accipiter
nisus), with the hope that described investigations will help
in understanding the vascular formation of the brain in wild
birds. These results may consequently boost and contribute
to the avian literature in veterinary anatomy.
MATERIAL AND METHODS
This study was carried on a total of 10 wounded and clinically terminal sparrowhawks that were received from the
animal hospital at Atatürk University, Faculty of Veterinary
Medicine, Erzurum, Turkey and provided by certified hunters
in the Rize province. Their weights of the birds ranged from
150 to 250g. Under deep anesthesia using a xylazine-ketamine
combination, the chest cavities of the hawks were opened and
apex of their hearts was cut off to drain the blood. As stated
in literature, vessels were cleaned out by administering 0.9 %
NaCl through the aortae (15). Coloured latex (ZPG 582-G)
was injected into left ventricle of heart. Materials were kept
in 10% of formaldehyde solution at room temperature for 2-3
days for the latex to freze. Then, dissections were carried out
and the pictures were taken. Nomina Anatomica Avium (5)
was used for designation of anatomical terms.
The present study was approved on 22 April 2011 by the
Atatürk University Local Ethical Committee for Animal
Experiments (Approval #4).
RESULTS
Arterial blood was found to be provided to the brain by coupled
carotid arteries which proceeded medially in the neck before
spread laterally and dividing into external and internal carotid
arteries. In all of the samples, the course of the right and left
internal carotid arteries ran to the middle of the ventral side of
the neck, perforating through the cervical carotid canal before
they reached the nearness of the brain base. At this level they
left the canal, deviated latero-cranially, proceeded as the cerebral carotid artery. The right and left internal carotid arteries
were present in all of the samples exhibiting the bicarotid form.
Both the right and left cerebral carotid arteries in all
of the samples were located in the sphenoid bone running
through the cranium (Figure 1/1, 2, 4, 5; Figure 2/3). This
segment consisted of the intrasphenoid segment of the artery.
From this point each cerebral carotid artery deviated craniomedially to form an intercarotid anastomosis, located ventrocaudal to the hypophysis and on the near caudal aspect of the
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optic chiasma (Figure 1/3). This anastomosis was determined
as a side-to-side anastomosis in a ‘X’ shape (Figure 1/3). The
right and left cerebral carotid arteries at the level of the tuber
cinereum divided into two terminal branches, the caudal
and rostral branches (Figure 1/6; Figure 2/4, 6). The caudal
branch of cerebral carotid artery continued caudoventrally
after its origin producing a collateral branch, ventral tectal
mesencephalic artery laterally and this branch distiributed
to the ventral surface of the optic lobe. Then the right and
left caudal branch of cerebral carotid artery in all of the birds
continued caudomedially and developed basilar arteries at the
level of the ventral interpeduncular fossa (Figure 2/1). This
artery (basilar artery) extended itself caudally, on the ventral
median fissure where it gave its collateral branches, the right
and left rostral ventral cerebellar artery (Figure 2/2).
The rostral branch of the cerebral carotid artery was a
continuity of the cerebral carotid artery, after the distribution
the caudal branch, latero-cranially in the course of the cerebral hemisphere. This vessel continued latero-cranially, as an
arch, until it reached the cerebral transverse fissure between
the optic lobe and the cerebral hemisphere. At this level, it
gave off its first collateral branch, the caudal cerebral artery
in six of the birds (Figure 1/7). In these samples the caudal
cerebral artery gave off its terminal branch the dorsal tectal
mesencephalic artery in the cerebral transverse fissure. In
four of the birds the caudal cerebral artery originated from
rostral branch of cerebral carotid artery prior to the cerebral
transverse fissure (Figure 2/7) and gave off the dorsal tectal
mesencephalic artery at the level of the cerebral transverse fissure on the ventral surface of the optic lobe (Figure 2/8). The
dorsal tectal mesencephalic artery dispersed to the ventral
and cranial surface of the optic lobe.
In all of the samples, the second collateral branch of
rostral branch of the cerebral carotid artery was the middle
cerebral artery (Figure 1/8; Figure 2/9). This vessel continued rostrolaterally and medially in the ventral surface of the
cerebral hemisphere, from the optic tract until the vicinity of
lateral surface of olfactory bulb. During this course, it emitted
several lateral hemispheric terminal branches which ascended
the lateral surface of the cerebral hemisphere. The medial
terminal branches of the middle cerebral artery and the
terminal branches of the rostral cerebral artery approached
to the ventral surface of the cerebral hemisphere.
After the formation of the middle cerebral artery, the
rostral branch of cerebral carotid artery, in the base of the
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cerebral hemisphere deviated medially and extended as the
cerebroethmoidal artery (Figure 1/9; Figure 2/10). The cerebroethmoidal artery was present in all but six of the samples,
in the ventral surface of the right cerebral hemisphere where
this vessel was residual or too short. In these samples, the right
cerebroethmoidal artery appeared as the common root of the
rostral cerebral and ethmoidal artery (Figure 1/9). However,
in the remaining four samples, the right and left cerebroethmoidal artery was well developed extending medially from the
middle cerebral artery, at the ventral surface of the cerebral
hemisphere, to the ethmoidal artery (Figure 2/10).
The rostral cerebral artery, a collateral branch of the cerebroethmoidal artery, was a vessel rostrally extended from the
cerebroethmoidal artery, on a ventral region of the cerebral
hemisphere, restrained by the cerebral longitudinal fissure,
the middle cerebral artery and the ethmoidal artery until it
attained rostrally to the olfactory bulb (Figure 1/10; Figure
2/11). The right and left rostral cerebral arteries divided into
two branches medially and laterally, just after its origin in
four of the samples and medial branches continued rostromedially towards the cerebral longitudinal fissure (Figure 2/11).
However, in six of the samples, the right rostral cerebral ar-
Figure 1: Ventral view of the brain base arteries and intercarotid
anastomosis in sparrowhawk after removal of the hypophysis. 1, 2, 4,
5: Cerebral carotid artery, 3: Intercarotid anastomosis, 6: Rostral branch
of the cerebral carotid artery, 7: Caudal cerebral artery, 8: Middle
cerebral artery, 9: Cerebroethmoidal artery, 10: Rostral cerebral artery,
11: Ethmoidal artery, A: Optic chiasm, B: Optic lobe, C: Olfactory
bulb, D: Cerebral hemisphere.
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tery was single vessel. In these birds, the left rostral cerebral
artery was a bifurcate vessel (Figure 1/10).
The ethmoidal artery was found to be the continuation
of the cerebroethmoidal artery after the distribution of the
rostral cerebral artery (Figure 1/11; Figure 2/12). The vessel continued ventrally and rostrally coursing the cerebral
longitudinal fissure leaving the cranium across the olfactory
foramen and finally distributing into the nasal cavity.
DISCUSSION
There is a dearth of literature regarding the sparrowhawk
brain vascularization. Investigations on this topic concentrate
on other birds (2, 4-6, 9, 10). Therefore, in this study we
attempted to carry out an evaluation with this species of bird.
In sparrowhawks, it was observed that arterial blood
was provided to the brain by coupled carotid arteries which
proceeded medially in the neck before spread laterally. The
same structures was reported for Japanese quail by Sharp and
Follett (1969) (4) and for helmeted guineafowl by Crowe and
Crowe (1979) (6). In some references, it was stated that birds
may be bicarotid or unicarotid with regards to whether they
Figure 2: Ventral view of the brain base arteries in sparrowhawk after
removal of the hypophysis. 1: Basilar artery, 2: Rostral ventral cerebellar
artery, 3: Cerebral carotid artery, 4: Caudal branch of the cerebral
carotid artery, 5: Ventral tectal mesencephalic artery, 6: Rostral branch
of the cerebral carotid artery, 7: Caudal cerebral artery, 8: Dorsal tectal
mesencephalic artery, 9: Middle cerebral artery, 10: Cerebroethmoidal
artery, 11: Rostral cerebral artery, 12: Ethmoidal artery, A: Optic
chiasm, B: Optic lobe, C: Olfactory bulb, D: Cerebral hemisphere.
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have the right and left internal carotid arteries or not (5, 16).
Both the right and left internal carotid arteries were present
in the sparrowhawks investigated in present study.Therefore,
they exhibited the bicarotid form with the right and left
cerebral carotid arteries originating from the right and left
internal carotid arteries, respectively. From our observations
in the present study, we believe that this situation might be
specific for the species.
The left and right cerebral carotid arteries of most avian
species are combined to each other by an intercarotid anastomosis (14, 17-21). Some literature reported that the cerebral
carotid artery continued rostro-medially into the carotid canal
and caudal to the hypophysis the two arteries were combined by
the transverse intercarotid anastomosis (8, 22, 23). Baumel and
Gerchman (4) determined patterns of intercarotid anastomosis,
called H, X and I types and Aslan et al. (12) reported two principal shapes of intercarotid anastomosis, namely H and X types.
The latter authors included the turkey and goose in their study
and found a side-to-side anastomosis like ’X’ shape. Their findings were also found in the present study in the sparrowhawk.
Nickel et al. (2) reported that caudal to the hypophysis,
caudal branches of the cerebral carotid artery united to become
the basilar artery in domestic birds. Baumel and Gerchman
(24) reported bilateral symmetry in origin and size of these
vessels in nine out of 82 passerine birds which they examined.
In accordance with the previous studies we found also that
caudal branches of the cerebral carotid artery was bilaterally
symetrical in origin and they united to become the basilar
artery at the level of the ventral interpeduncular fossa in the
sparrowhawk. However, in the white-crowned sparrow, the
basilar artery mostly originated from the right caudal branch
(14), while in the domestic fowl, primarily from the left caudal
branch (19, 25) and the basilar artery was formed by only the
right caudal branch in the Denizli rooster, domestic fowl, and
goose while only the left caudal branch constituting basilar
artery in the pheasant, silver pheasant, and turkey (12).
The ventral tectal mesencephalic artery of the sparrowhawk continued caudolaterally into the inside of the fissure
that spreads to the optic lobe from the rhombencephalon
which vascularized ventrally the ventrocaudal surface of optic
lobe, as stated by Richards (1967), Campos (1987), Campos
et al. (1995) (8, 19, 23) and Nazer and Campos (2011) (26).
The ventral tectal mesencephalic artery originated from the
caudal branch of the cerebral carotid artery in the sparrowhawk in this study while for Midtgard (1984) (7) studying
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the gull, the ventral tectal mesencephalic artery originated
from the rostral branch of the cerebral carotid artery. The
authors surmise that this anatomical situation may result in
an increased perception of sight.
It was reported that the rostral branch of the cerebral carotid artery was a natural continuation of the cerebral carotid
artery and bulged in the form of an arch, until it reached
the cerebral transverse fissure (8, 23, 27). The results of our
study also resembles these findings. As indicated by Midtgard
(1984) (7) and Holliday (2006) (9) the rostral branch continued rostrally and spread the caudal cerebral artery, the middle
cerebral artery, the ethmoidal artery and rostral cerebral artery.
Literature reports have documented that the caudal cerebral artery originated from the rostral branch of the cerebral
carotid artery, close to the transverse fissure of the brain,
between the optic lobe and the cerebral hemisphere (19, 27).
According to Campos (8, 23, 28), the caudal cerebral artery
originated from the rostral branch of the cerebral carotid
artery at the level of the transverse fissure of the brain. In
our study, these same finding were also found in six of the
sparrowhawks examined. For Campos (1987) (8), in 3.3% of
the cases, the right caudal cerebral artery originated from the
rostral branch before it reached the transverse fissure. Similar
determinations were found, in the remaining four samples in
our study both in the right and left the caudal cerebral artery,
in the sparrowhawk.
Studies from a number of authors (2, 8, 19, 23, 29), indicated that the middle cerebral artery in Gallus gallus constituted a belt which reached the olfactory bulb without leaving
the ventral surface of the cerebral hemisphere. In the sparrowhawk, in addition to these findings, it also formed on its
route, innumerable lateral hemispheric branches. In contrast
to the ostrich (26), these lateral hemispheric branches in the
sparrowhawk did not anastomose to the dorsal hemispheric
terminal branches of the interhemispheric artery.
Carvalho and Campos (10) reported that the cerebroethmoidal artery was always present as a single vessel, of large
caliber in the turkey. In contrast to this finding, in six of the
samples in our study, in the ventral surface of the right cerebral
hemisphere, the right cerebroethmoidal artery was residual or
consisted of a short vessel. As claimed by Nazer and Campos
(2011) (26) the rostral cerebral artery was a well developed
vessel projected from the cerebroethmoidal artery in our study.
Some researchers (6, 7, 9, 22, 24, 27), recognized rostral cerebral artery while Schwarze and Schroder (1970) (30), Nickel
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(1977) (2), King and McLelland (1981) (31) did not cite the
existence of the rostral cerebral artery in domestic birds. In the
sparrowhawk, the left rostral cerebral artery was duplicated
in all of the samples while the right rostral cerebral artery
was a single branch in six of the all samples. Howewer, in the
ostrich (26), on the left it was single in 96.7% of the samples.
In summary, in this study the vascular construction and
ramification of the brain base arteries in the sparrowhawk
were determined. It is hoped that the existing outcomes
will ease understanding of the phylogenetic relationships
and morphological similarities among different bird species.
In addition, we believe that this information will provide
particular anatomical data regarding the sparrowhawk.
ACKNOWLED GEMENT
This study was supported by the project No. 2011026, financed from
Atatürk University Department of Scientific Research Projects.
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