Download Arterial Blood Supply to the Auditory Cortex of the Chinchilla

Acta Otolaryngol 2001; 121: 839 – 843
Arterial Blood Supply to the Auditory Cortex of the Chinchilla
JASWINDER PANESAR, HORMOZ HAMRAHI, NOAM HAREL, NAOKI MORI, RICHARD
J. MOUNT and ROBERT V. HARRISON
From the Auditory Science Laboratory, Department of Otolaryngolog y, Uni×ersity of Toronto, Brain & Beha×iour Di×ision, The Hospital
for Sick Children, Toronto, Ont., Canada
Panesar J, Hamrahi H, Harel N, Mori N, Mount RJ, Harrison RV. Arterial blood supply to the auditory cortex of the
chinchilla. Acta Otolaryngol 2001; 121: 829 – 843.
Utilizing optical imaging we identiŽ ed and named the arteries that supply the primary auditory cortex in the chinchilla
(Chinchilla laniger). The primary auditory cortex is located 2 – 3 mm caudal to the medial cerebral artery and is supplied
by it. Using corrosion casts and scanning electron microscopy we visualized the capillary networks in the auditory cortex
and found regional variations in the densities of the capillary bed. We hypothesize that the uneven capillary densities
observed in the auditory cortex correspond to neurologically more active areas. Key words : capillary network, corrosion
cast, medial cerebral artery, optical imaging, primary auditory cortex.
INTRODUCTION
The relationship between neural activity in the cerebral cortex and local hemodynamics has become a
topic of considerable interest and importance since
the introduction and wide-scale use of clinical imaging methods such as positron emission tomography
and functional magnetic resonance imaging (fMRI)
(1 – 3). These techniques, together with optical imaging of intrinsic signals (4, 5), are all techniques in
which the signal detected is a hemodynamic event,
often referred to as a blood oxygen level- dependent
(BOLD) effect. In our experimental work, using optical imaging of intrinsic signals in the auditory cortex,
we have used a chinchilla (Chinchilla laniger) animal
model (6, 7). However, to date there has been no
systematic study of the arterial blood supply to auditory areas of the cortex in the chinchilla (or in similar
small rodents).
The chinchilla has been widely used as a model to
study the function of the auditory system, particularly in North America where it is widely available.
This species has a number of advantages for hearing
research: it can be trained in behavioral psychophysical tasks, and anatomically it has an accessible inner
ear via an enlarged middle ear bulla cavity. For
auditory cortical recordings, the cranium and dura
overlying the temporal cerebrum can be safely removed (8).
There are three components to the present study.
Firstly, we have determined the exact location of the
auditory cortex using optical imaging of intrinsic
signals and determined as far as possible the relationship between primary auditory cortex and local blood
vessels. Secondly, we have used latex polymer infusion techniques to Ž ll and mark the arterial blood
supply to the brain. From such whole brain preparations we describe and provide nomenclature for the
© 2001 Taylor & Francis. ISSN 0001-648 9
major arterial vessels to the auditory cortex. Thirdly,
we have used corrosion cast techniques combined
with scanning electron microscopy (SEM) to visualize
the artery– arteriole connections which supply capillary networks in the auditory cortex.
MATERIALS AND METHODS
Adult chinchillas (n¾ 11; weight 500 – 750 g) were
studied. All invasive procedures were carried out in
anesthetized animals using ketamine hydrochloride
(15 mg kg, i.m.), atropine sulphate (0.04 mg kg, i.m.)
and xylazine hydrochloride (2.4 mg kg, i.m.). All
methods conformed strictly to the guidelines of the
Canadian Council on Animal Care.
In three subjects, optical imaging of intrinsic signals was carried out to determine the boundaries of
the auditory cortex. We have previously described
these methods in detail (6, 7). Brie y, via a 10-mm
wide craniotomy over the temporal lobe, optical images of the cortex were recorded during acoustic
stimulation (broadband noise, 80 dB SPL). Using
suitable monochromatic illumination (wavelength :
540 – 560 nm), local hemodynamic changes in response to the metabolic demands of active auditory
neurons were imaged with a suitable detection system. The derived functional maps, i.e. boundary of
active auditory cortex, and images of the superŽ cial
vasculature were then compared.
A second group of animals (n ¾5) were used for
whole brain blood vessel identiŽ cation studies. Using
a trans-cardiac cannulation technique, subjects were
perfused with : 1000 ml of heparinized saline. The
descending aorta was then clamped and the ascending
aorta infused with latex. Return of  ow was achieved
by incising the right atrium. Approximatel y 15 – 20 ml
of latex was used to ensure complete Ž lling of all
major cerebral arteries and their branches.
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J. Panesar et al.
For high resolution microscopy of arterial connections to capillary beds a corrosion casting technique
(9) was employed in a third group of animals (n ¾3).
Casts of the cerebral vasculature were prepared by
perfusing, again via the ascending aorta, 50 ml of
heparinized PBS followed by 20 ml of Batson’s
17
resin. Complete polymerization of the resin took :
12 h, after which the brain was dissected from the
cranium. Soft tissue was macerated in 40% KOH at
50°C for 24 h with intermittent distilled water rinses.
The plastic cast was air-dried, mounted onto a stub
with colloidal silver and sputter-coated.
RESULTS AND DISCUSSION
Position of auditory cortex
Optical imaging of intrinsic signals essentially shows
areas of increased blood  ow that are directly related
to metabolic demands of activity in the auditory
cortex resulting from acoustic stimulation. Fig. 1
shows results from three typical subjects. Each panel
shows an image of temporal cortex through the craniotomy, with the boundary of the auditory areas
superimposed (black lines). Generally it is possible to
recognize three separate areas of hemodynamic
change, which we identify as primary auditory cortex
(AI), secondary auditory cortex (AII) and the anterior auditory Ž eld (AAF). The position of the AI as
identiŽ ed by optical imaging corresponds to the electrophysiologically deŽ ned AI in the chinchilla (8).
Single-unit recordings from the area have short onset
latency responses that are characteristic of primary
auditory neurons (7). As a rule of thumb we can say
that the AI is situated 2 – 3 mm posterior (caudal) to
the medial cerebral artery (MCA) along the middle
temporal artery (MTA). Often the AI coincides with
the bifurcation of the MTA into its superior and
inferior branches, but as the location of the bifurcation varies somewhat this is not always the case.
Major arterial ×essels
Intra-aortic latex infusion allows reliable visualiza-
Acta Otolaryngol 121
tion of all major cerebral arteries, as shown in Fig. 2.
Viewed from the ventral direction (lower panel), the
anatomy of the arterial circle and its associated major
vessels can be seen. The general plan (from caudal to
rostral) of vertebral arteries converging to form the
basilar artery, which in turn bifurcates to form the
caudal end of the arterial circle, is similar in all
mammalian species, including humans. The arterial
circle of the chinchilla resembles that of other rodents
(10) and is analogous to the circle of Willis in primates (11).
The cerebellum is supplied by the caudal and rostral cerebellar arteries. The caudal cerebellar artery
arises from the basilar artery at the lower part of the
pons whilst the rostral cerebellar artery arises at the
termination of the basilar artery, close to the upper
border of the pons.
The arterial supply of the cerebral cortex is provided by the three cerebral arteries: caudal, medial
and rostral. The caudal cerebral arteries are given off
at the cerebral peduncle. Each caudal cerebral artery
is joined to the internal carotid artery by the caudal
communicating artery. The relative diameter of the
internal carotid arteries of the chinchilla, and presumably of rodents in general, is considerably reduced compared to those in humans. Of particular
interest here is the MCA, which supplies most of the
temporal cortex including all auditory areas. It
courses laterally along the sulcus between the frontal
and temporal lobes. The medial cerebral and rostral
cerebral arteries are given off anterior to the internal
carotid arteries. The rostral cerebral artery runs medially to reach the longitudinal Ž ssure between the
two cerebral hemispheres above the optic chiasm. In
many mammalian species the rostral cerebrals are
joined by the rostral communicating artery; however,
in seven of the eight chinchillas examined this communicating artery was lacking, and thus the arterial
circle is not fully closed. Similarly, Jablonski and
Brudnicki (12) noted rostral communicating arteries
in only 2 of 28 chinchillas examined.
Fig. 1. Optical imaging of intrinsic signal results from three typical subjects, in response to acoustic stimulation.
Acta Otolaryngol 121
Arterial blood supply to auditory cortex of the chinchilla
841
Fig. 2. Chinchilla brain following
aortic latex infusion showing all major cerebral arteries.
The upper image in Fig. 2 is a lateral view of the
chinchilla brain showing the MCA and its branches.
The MCA, coursing laterally around the surface of
the temporal cerebrum, gives rise to three main arteries supplying the temporal lobe: the inferior, middle
and superior temporal arteries. The MTA (our particular focus here) further divides into superior and
inferior branches.
Fig. 3 is a schematic representation summarizing
the major arterial supply associated with the auditory
cortex. Whilst variations in the arterial tree may be
expected and comparative studies by Jablonski and
Brudnicki (12) have demonstrate d variations in the
caudal cerebral arteries, the location of the branch
point of the MCA and MTA is remarkably consistent. In making a craniotomy for electrophysiological
Fig. 3. A schematic representation summarizing the major arterial supply associated with the auditory cortex (not to scale).
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J. Panesar et al.
Acta Otolaryngol 121
or optical studies of the auditory cortex we can
recommend using the following surgical landmarks.
Anteriorly (rostrally), the caudal wall of the orbit
overlies the MCA; using the zygoma as a ventral
boundary and the horizontal part of the parietofrontal bone as the dorsal edge, a craniotomy will reveal
temporal cortex with the MTA running centrally
across it.
Final connections to cortical capillary network
The Ž nal stages in the supply of blood to the auditory cortex are depicted in Fig. 4. Fig. 4a is an SEM
image of the corrosion cast of vasculature viewed
from the caudal direction looking along the cortical
surface at the bifurcation of the MTA into superior
(sMTA) and inferior (iMTA) branches. The lower
surfaces of both the inferior and superior branches
of the MTA give rise to collateral vessels which
directly penetrate the cortical surface. In addition
there are a number of side-branching collateral vessels which tend to either extend from the artery at
right-angles across the cortical surface for a short
distance ( : 500 mm) before penetrating the surface,
or have a superŽ cial course of several millimeters
before becoming intracortical. Some arteries give rise
to a capillary bed : 750 mm deep located in the
superŽ cial layer of the cortex. Other arteries contribute few if any collateral branches to this capillary
bed, penetrating deeply into the cortex. Some of the
latter type bend at 90° and course parallel to the
cortical surface at a depth of : 1 mm and give rise
to upward-coursing arterioles which contribute to the
overlying capillary bed. Within the superŽ cial capillary bed, arterioles give off both collateral and terminal capillaries. The superŽ cial capillary bed is not
evenly distributed throughout the temporal cortex. It
is shown in Fig. 4a and c that there are areas of
dense capillary networks separated by regions of few
to no capillaries. It is our working hypothesis that
the uneven capillary bed densities that we observe in
auditory areas of temporal cortex may correspond to
regions in which auditory neurons are more active,
or perhaps more densely packed, demanding differing amounts of hemoglobin supply.
Fig. 4.
Fig. 4. SEM images of corrosion cast of cerebral vasculature supplying the auditory cortex. (a) View from the
caudal direction looking along the cortical surface at the
bifurcation of the MTA into sMTA and iMTA branches.
(b) An arteriole bifurcates with one branch (½ ) giving rise
to the superŽ cial capillary network and the other (*) penetrating deeper into the cortex without further branching. (c)
Two dense regions of the superŽ cial capillary network are
separated by a low density region which is penetrated by an
intracortical arteriole (*).
Arterial blood supply to auditory cortex of the chinchilla
Acta Otolaryngol 121
ACKNOWLEDGMENTS
This research was supported by grants from the Medical
Research Council (Canada) and by the Masonic Foundation of Ontario.
8.
9.
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Submitted March 17, 2000; accepted April 26, 2001
Address for correspondence:
Dr. Robert V. Harrison
Auditory Science Laboratory
Dept. of Otolaryngology
The Hospital for Sick Children
555 University Avenue
Toronto, Ont. M5G 1X8
Canada
Tel.: »1 416 813 6535
Fax: » 1 416 813 8456
E-mail: [email protected]