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Transventricular blood vessels in the third ventricle of the armadillo brain.

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BRIEF COMMUNICATION
Transventricular Blood Vessels in the Third Ventricle
of the Armadillo Brain
PHILLIP JAY IVES AND NEWELL H. MCARTHUR
Texas A and M Uniuersity, Department of Veterinary Anatomy,
College Station, Texas 77843
ABSTRACT
Transventricular filaments were observed with scanning electron microscopy on the dorsolateral wall of the infundibular recess of the third
ventricle of the armadillo brain. Two to seven transventricular filaments per
animal were present in 6 of 18 animals. There were two types of transventricular filaments, ciliated and bare. Using transmission electron microscopy, we
determined that these filaments consisted of a single, central capillary surrounded by ciliated ependymal cells and a small accumulation of axons in five
animals. In one animal, a bare filament had a central capillary surrounded by a
large accumulation of axons with no surrounding ependyma. The consistent
location and structure of these filaments indicate a possible function for a
small vascular network, as well as a possible commissural network connecting
right and left hypothalami in the region of infundibular nuclei.
Scott et al. ('74) described the scanning
electron microscopy (SEMI of a nonciliated
transventricular structure passing across the
infundibular recess of the third ventricle of a
male cat. They did not elucidate the exact ultrastructural cytoarchitecture and presumed
the structure to be a blood vessel. McArthur
(unpublished results) observed, with SEM,
similar structures in the rat third ventricle.
We observed these structures on the surface
of the third ventricle of the armadillo. The
structures were shaped like spines or filaments and extended from the wall of the third
ventricle, across the ventricular lumen and
into the opposite ventricular wall. This report
defines location, orientation and ultrastructure of these filaments using correlative SEM
and transmission electron microscopy (TEM).
MATERIALS A N D METHODS
Eighteen armadillos (Dasypus novemicinatus L3, ten females and eight males, were captured by netting from their natural habitat in
central Texas during summer, winter and
spring. The animals were anesthetized with
pentabarbitol (35 mg/kg). Fixation was accomplished by transcardiac perfusion or by
immersion of tissue using 5% glutaraldehyde5% paraformaldehyde in 0.1 M sodium cacodylate, pH 7.3, 2OoC, and post-fixed in 1%
osmium tetroxide. The brain was removed and
ANAT. REC. (1979) 194: 181-186.
the third ventricle exposed using a parasagittal approach. SEM samples were critical-point
dried in liquid COz, sputter coated with goldpalladium and studied using an AMR-1200.
After examination, SEM samples were immersed in 100% acetone and embedded in
Araldite/Epon plastic for TEM. Serial thick
and thin sectioning techniques were used to
correlate SEM, optical microscopy and TEM.
Thin sections were viewed with an RCA-EMU
3-G transmission electron mciroscope.
RESULTS
Transventricular filamentous structures
were observed in the third ventricle of 6 out of
18 armadillos (1 immature male, 3 adult
males, 2 females). No correlation could be
made between age, sex or season of the year
and presence of the transventricular filaments. There were two to seven filaments per
animal, located on the dorsolateral wall of the
infundibular recess of the third ventricle, immediately rostroventral to the mammillary
bodies (fig. 1).By matching right and left ventricular walls of the six animals with transventricular filaments, we determined that the
filaments passed from one side of the hypothalamic third ventricle to the opposite side. In
cut portions of the transventricular filaments,
Received July 31, '78. Accepted Nov. 3, '78
181
182
PHILLIP JAY IVES AND NEWELL H. MCARTHUR
the lumen of the enclosed vessel could be observed (fig. 5 ) and compared on right and left
halves. In five animals the filament surfaces
were completely covered with ciliated ependymal cells (fig. 2). The ependymal cells
exhibited typical junctional complexes and
desmosomes. These filaments contained a central capillary and an occasional pericyte (fig.
3). Axons were seen both in a supraependymal
position (fig. 4) and between the ependymal
cells and the capillary in each of these filaments. The diameter of these axons ranged
from 0.8-2.0 pm when in a supraependymal
position. One animal had three transventricular filaments not covered with ependymal
cells (fig. 5 ) . These bare filaments had clusters
of axons surrounding a large capillary (fig. 6).
The diameter of these axons ranged from 0.82.5 pm.
DISCUSSION
Two types of transventricular filaments,
bare and ciliated, were present in the armadillo. The ciliated filaments have not previously been reported. They could provide for
vascular exchange between right and left
hypothalami. Their axons could provide neuronal interconnections. The presence of bare
filaments in the armadillo confirms and expands the observations of Scott et al. ('74) in
the male cat. These bare filaments are not
only vascular, as presumed by Scott and coworkers, but are composed of clusters of axons
surrounding a centrally located blood vessel.
These axons and those of the ciliated transventricular filaments, expecially the supraependymal axons, represent a n extension of
the extensive supraependymal axonal network reported by Ribas ('77), Chan-Palay ('77)
and Ives and McArthur ('79).
Our observations suggest that the filamentous structures are transventricular vessels surrounded by axons with either an intraventricular or transventricular neuronal
function. Since the vascular filaments were
confined to the infundibular recess of the
third ventricle of the cat (Scott et al., '74), rat
(McArthur, unpublished) and the armadillo,
we suggest that they could be a factor in the
overall function of the neuroendocrine vascular network of the hypothalamus. These filaments could be an avenue of blood exchange
between right and left hypothalami in caudal
portions of the infundibular nuclei. Animals
without these transventricular filaments and
their accompanying blood vessel could have a
functional vascular exchange in the caudal
hypothalamus, mammillary body or infundibulum. It is well documented that part of
the control and regulation of the hypophyseal
hormones is mediated by a short feedback
mechanism (Martini, '71) and an ultrashort
internal feedback mechanism, FSH-RF (Hyyppa and Motta, '69; Motta, '69).
The presence of a subependymal infundibular hypothalamic vascular network has been
described (Toeroek, '64; Holmes, '67; Akmayev, '71; Negm, '711, but is not supported
by Murakami ('75) in his study of vascular
casts of the rat infundibulum. Data from SEM
of vascular casts of rabbit (Page et al., '76),
dog, sheep, mouse, rat and monkey (Page and
Bergland, '77) support the postulated presence
of subependymal or internal vascular plexus
that could provide a route for hypothalamic
releasing hormones to infundibular tanycytes.
The tanycytes then could transport hormones
into the third ventricle where they would have
access to the supraependymal axons. Such a
route has been suggested by Robinson and
Zimmerman ('73) for neurophysin from the
infundibular process.
Page and Bergland ('77) reported that blood
from the infundibulum may flow via capillaries into the hypothalmus. The transventricular vessels could supplement this function by
exchanging blood between hypothalami; however, the physiological evidence to support
this hypothesis is currently lacking.
LITERATURE CITED
Akmayev, I. G. 1971 Morphological aspects of the hypothalamic hypophyseal system. 11. Functional morphology
of pituitary microcirculation. 2. Zellforsch., 116: 178-194.
Chan-Palay, V. 1977 Indoleamine neurons and their
processes in t h e normal rat brain and in chronic dietinduced thiamine deficiency demonstrated uptake of 3Hserotonin. J. Comp. Neur., 176: 467-493.
Holmes, R. I. 1967 The vascular pattern of the median
eminence of t h e hypophysis in t h e macaque. Folia
primat., 7: 216-230.
Hyyppa, M., and M. Motta 1969 "Ultra-short" feedback
control of t h e secretion of t h e hypothalamic releasing factors. Scand. J. clin. Lab. Invest., 23 (Suppl. 108): 39.
Ives, P. J.,and N.H. McArthur 1979 The armadillo median
eminence: Correlative histochemistry, scanning and
transmission electron microscopy of the ventricular surface. Brain Res., in press.
Martini, L. 1971 Hypothalamic mechanisms controlling
anterior pituitary functions. In: Hormones and Brain
Function. K. Lissak, ed. Plenum Press, New York,
pp. 123-142.
Motta, M. 1969 The brain and t h e physiological interplay of long and short feedback systems. In: Progress
in Endocrinology. C. Gual, ed. Excerpta Medica, Amsterdam, pp. 523-531.
Murakami, T. 1975 Pliable methacrylate casts of blood
ARMADILLO-THIRD
VENTRICLE-BLOOD
vessels: use in a scanning electron microscope study of
t h e microcirculation in r a t hypophysis. Arch. Histol.
japon., 38: 151-168.
Negm, I. M. 1971 The vascular body supply of the pituitary gland and its development. Acta anat., 80: 604-619.
Page, R. B., and R. M. Bergland 1977 The neurohypophyseal capillary bed. I. Anatomy and arterial supply. Am. J. Anat., 148: 345-358.
Page, R. B., B. L. Munger and R. M. Bergland 1976 Scanning microscopy of pituitary casts. Am. J. Anat., 146:
273-302.
Ribas, J. L. 1977 Morphological evidence for a possible
VESSELS
183
functional role of supra-ependymal nerves on the ependyma. Brain Res., 125: 362-368.
Robinson, A. G., and E. A. Zimmerman 1973 Cerebrospinal
fluid and ependymal neurophysin. J. Clin. Invest., 52:
1260-1267.
Scott, D. E., G. P. Kozlowski and M. N. Sheridan 1974 Scanning electron microscopy in the ultrastructural analysis
of the mammalian cerebral ventricular system. Intl. Rev.
Cytol., 37: 349-388.
Toeroek, B. 1964 Structure of the vascular connections
of t h e hypothalamohypophysial region. Acta anat., 59:
84-99.
PLATE 1
EXPLANATION OF FIGURES
1 The third ventricle (V) showing the location of three filaments (arrows). Intrathalamic adhesion (T), mammillary body (MB), infundibular recess (R),median
eminence (ME), optic chiasm (00,preoptic recess (POR).x 20.
2 Two filaments extending from the third ventricle wall. The filaments are covered by
ciliated ependyma and were cut by parasagittal dissection during removal. X 260.
3 Correlative transmission electron microscopy of one of the filaments shown in
figure 2. Note t h e centrally located capillary (C) surrounded by ciliated ependymal
cells (E). x 2,700.
4 Higher magnification of figure 3 showing part of a n ependymal cell (El in contact
with several axons (A). Note the presence of a supraependymal axon (arrow) which
is part of t h e ventricular surface axonal network. X 21,000.
5 P a r t of a transected bare filament on third ventricle wall. Note the absence of ependyma on the filament. x 470.
6 Correlative TEM of the filament in figure 5, showing the capillary (C) and surrounding axons (A). Note t h e absence of ependymal cells. X 4,300.
184
ARMADILLO-THIRD VENTRICLE-BLOOD
Phillip Jay Ives and Newell H. McArthur
VESSELS
PLATE 1
185
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