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Fine structural studies of the sino-auricular nodal tissue in the heart of a teleost fish misgurnus with particular reference to the cardiac internuncial cell.

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Fine Structural Studies of the Sino-auricular Nodal
Tissue in the Heart of a Teleost Fish, Misgurnus,
with Particular Reference to the Cardiac
Internuncial Cell
AKIO YAMAUCHI, YOKO FUJIMAKI AND REIKO YOKOTA
Department of A n a t o m y , Iwate Medical University School of Medicine,
Morioka 020, J a p a n
ABSTRACT
The sino-auricular nodal tissue of the heart of the loach (Misgurnus anguillicaudatus, Cantor) contains ( 1 ) myocardial cells receiving rich
innervation, (2) isolated nerve cells, and ( 3 ) cardiac internuncial cells which
are interposed between autonomic axon terminals and myocardial cells. S-Ctural specializations are noted at the synapse between the autonomic axon and
the myocardial cell, as well as at the axon-internuncial cell synapse. Between
the internuncial cell and the myocardial cell, attachment plaques are present
with a patchy locus of a close junction, wherein the extracellular space appears
to be almost obliterated. Estimations were made of the surface areas of an internuncial cell body and a nerve cell body as revealed by serial sampling of the
tissue at about 0.5 p intervals. The results show that for an internuncial cell
body followed over a length of 15 p , 52.5% of its total surface is covered by
vesiculated axons, 3.8% by non-vesiculated axons, 12.2% by myocardial cells,
and 3.1 % by Schwann cell processes; for a nerve cell body followed over a length
of 16 p, only 1.8% is covered by vesiculated axons, 0.5% by non-vesiculated
axons, nil by myocardial cells, and 96.4% by a satellite cell and its processes.
It is considered that the internuncial cell represents a specialized cell type in
the nodal tissue of the fish heart, playing a role in modulating the autonomic
nerve impulses before they are transmitted to the effector myocardial cells.
Recent electron microscopic investiga- microscopic studies of the heart from a
tions on innervation of the heart of the variety of fishes (Keith and Mackenzie,
trout, Salmo trutta (Yamauchi and Burn- ’10; Mackenzie, ’13; Laurent, ’62).
In this paper, further observations are
stock, ’SS), the loach, Misgurnus anguillicaudatus, (Yamauchi, ’69) and the plaice, made of the fine structure of the nodal
Pleuronectes platessa, (Santer, ’72) have tissue in the loach heart. Particular emindicated the occurrence of peculiar myo- phasis will be placed on the morphology
cardial tissue at the border region between of the internuncial cell that occurs bethe sinus venosus and the auricle of the tween autonomic axon terminals and myofish heart. The sino-auricular myocardium cardial cells.
is said to be specialized, particularly in the
MATERIAL AND METHODS
sense that it receives a n unusually dense
Mature loaches (Misgurnus anguillicauautonomic innervation, each myocardial
cell being in contact with at least one and datus, Cantor), 10-15 cm long, were
probably many more axon terminals. studied. The beating heart of the pithed
Topographically, such myocardial tissue is fish was exposed and fixation commenced
concentrated at the base of the venous by applying ice-cold glutaraldehyde soluvalves to form a nodal thickening of mus- tion (2% in 1/15 M Na-K-phosphate buffer
cle around the sino-auricular orifice, and at pH 7.4) to the surface of the heart. The
no doubt corresponds to the “sino-auricu- whole heart, together with portions of adlar nodal tissue” as found by earlier light jacent organs, was then removed and
AM. J. ANAT., 138: 407430.
407
408
A. YAMAUCHI, Y. FUJIMAKI AND R. YOKOTA
placed in the same fixative. Since it was
necessary to minimize the glutaraldehyde
immersion time so as to obtain adequate
preservation of the autonomic axon terminal in the fish heart, excision of the sinoauricular border region of the fish heart in
the aldehyde solution was performed as
quickly as practicable and the specimens
soon transferred into an ice-cold 1%
Os04 solution ( i n the same phosphate
buffer as above) for a n additional 90 minutes. Usually the total period for glutaraldehyde immersion did not exceed 15 minutes. Specimens were then dehydrated in
ethanol and embedded in Epon 812 (Luft,
'61) through n-butyl glycidyl ether (QY-1,
Oken Shoji, Japan) as a n infiltration
medium (Kushida, '63).
To orient the sino-auricular region, 1,sections cut from Epon blocks and stained
with 1% toluidine blue in 1% borax
(Yamamoto, '63) were examined with a
light microscope. Thin (0.1 p ) sections
were stained with 2% uranyl acetate for
15 minutes followed by Reynolds' ('63)
lead stain and viewed in the electron microscope. Three-dimensional analysis of
the surface area of an internuncial cell and
a nerve cell body was based on a sampling,
at 0.5 -C 0.4
intervals, of thin sections
serially cut over a distance of 25 p from
the nodal tissue. Each group of consecutive five sections (representing 0.5 p thickness of tissue depth) was mounted on a
Formvar-coated 150-mesh grid and a
montage was prepared at a magnification
of 12,800 times of the relevant profile of
the cell as observed on successive grids.
Serial sections were mounted in a ribbon
with few sections being lost, but it was
only possible to make records of a n internuncial cell on 23 of a total of 30 successive grids attempted and records of a nerve
cell on 22 of a total of 32 grids attempted.
This loss was due mainly to grid bars intersecting the cell profiles. Surface area of
the cell was estimated by measuring
lengths of the surface membrane of cells
at each recorded level.
OBSERVATIONS
The principal portion of the sino-auricular nodal tissue in the heart of the loach
represents a relatively compact ring-like
musculature occupying the base of the
venous valve SO as to surround the sinoauricular orifice (fig. 1 ) . The wall of the
sinus in the loach, like that of the trout
(Yamauchi and Burnstock, '68), is amuscular except for very occasional smooth
muscle cells that are encountered near the
sino-auricular junction. Distally, the ring
of the sino-auricular nodal tissue is broken
down into a loose meshwork of myocardial
cells (tail of the sino-auricular nodal
tissue), spreading within the venous valve
toward its free margin (fig. 2). The transition between the auricular myocardium
and the sino-auricular nodal tissue occurs
at the outer circumference of the node. The
nodal tissue as a whole may be distinguished readily by light microscopy because
it is often lightly tinted with toluidine blue
in contrast to the deeply stained myocardium.
Closer inspection of the sino-auricular
nodal tissue by electron microscopy shows
it to be basically a n aggregation of extensively innervated cardiac muscle cells
(fig. 3 ) . They show a sparsity of myofibrils
in many sectional levels and have no cytoplasmic granules which characterize, as in
the atrial muscle cells i n mammals
(Jamieson and Palade, '64), the oridinary
auricular myocardial cells in fish. Ordinary
nerve cells are also encountered in the
sino-auricular nodal tissue, They occur
singly or i n small groups, without being
encapsulated by connective tissue cells,
and are intermingled with the nodal myocardial cells. A third cellular element of
the nodal tissue is the cardiac internuncial
cell, the soma of which forms synaptic
junctions with many autonomic axon terminals and at the same time is in direct
contact with apparently a smaller number of myocardial cells (figs. 4, 5 ) . The
internuncial cells differ from the nodal
myocardial cell in that they are entirely
devoid of myofibrils and also from the
nerve cell in that, among other features,
they have a remarkably poor content of
ribosomes within the cytoplasm.
Internuncial cells. When perikaryal
portions of the internuncial cell appear in
random sections they show in 18 out of
21 different cells observed a more or less
elongated profile, with ranges of major
and minor diameters of 7-15 p and 4-10 p,
respectively, whereas in other cases they
NODAL TISSUE OF FISH HEART
are round in profile with a diameter ranging from 5 to 10 p. The nucleus of the
internuncial cell often is irregularly indented and has finely granular chromatin
which is dispersed rather evenly within
the karyoplasm except for a slight tendency to condense towards the edge of the
nucleus. The nucleolus is not prominent,
occurring preferentially in the peripheral
portion of the nucleus. Generally, the perikaryal cytoplasm (figs. 4, 5) has a low
electron opacity, due to its remarkably
poor content of cell organelles, particularly
of free ribosomes. Cisternae of the granular endoplasmic reticulum are not only
sparse but also partly devoid of ribosomes
along their membrane. On the other hand,
the Golgi apparatus and smooth-surfaced
endoplasmic reticulum are quite highly
developed within the perikaryal cytoplasm
of the internuncial cell. Some particulate
glycogen is always present, but mitochondria are few. Fine filaments, about
50 A in thickness, are also present in the
internuncial cell body and its processes
(figs. 5, 6, 7, 8). These filaments are isolated or in a bundle with a dense body
resembling the Z-band substance of myocardial cells (I3 in fig. 4). The internuncial cell does not contain myofibrils
like those in the nodal myocardial cell
or tubular structures like neurotubules i n
typical neurons. Finally, a cilium may be
seen emanating from the cell body of the
internuncial cell (fig. 9 ) .
A n important feature of the internuncial
cell is that its perikaryon and processes are
in direct contact with a large number of
autonomic axons. Many of these axons are
extensively vesiculated and form a synaptic junction with the surface membrane
of the internuncial cell (figs. 6, 7). The
presynaptic axon terminal thereby contains clear, round vesicles ca 500 A in
diameter and a few large granular vesicles
700-1000 A i n diameter. At the synaptic
region, the width of the interspace between apposed membranes is more uniform than between the plasma membranes
elsewhere. Other features of the axoninternuncial cell synapse include a presynaptic projection of dense material
attached to the axolemma, an intermediate
band in the synaptic cleft, and a postsynaptic aggregation of dense cytoplasmic ma-
409
terial subjacent to the internuncial cell
membrane. A subsynaptic cistern of the
smooth endoplasmic reticulum may also
be seen i n the internuncial cell cytoplasm.
Aggregations of dense material to the synaptic membranes are much more frequent
in sectional levels on the presynaptic than
on the postsynaptic side, but they are
greater, when they occur, on the postsynaptic than the presynaptic side of the
synapse (figs. 6, 7).
The shape of the clear synaptic vesicles
mentioned above differs according to the
manner of fixation: they are rounded after
brief glutaraldehyde fixation followed immediately by osmication, whereas they become flattened after a relatively prolonged
glutaraldehyde fixation (up to 90 minutes)
followed by rinsing in buffer solution prior
to osmication. In the latter case, however,
the flattened vesicles appear not only in
the presynaptic bags attached to the internuncial cell, but also in the axons terminating on the nodal myocardial cell and
the cardiac nerve cell body.
Another feature of the internuncial cells
is that they are in direct contact with nodal
myocardial cells and with other internuncial cells as well. The intermediate junction (zonula adhaerens), occuring commonly between the internuncial and
myocardial cells (figs. 4, 8), may have in
places an extremely narrow interspace of
less than 50 A width (fig. 8 ) , establishing
a patchy locus of a close junction. Because the thin sections used in this study
had a thickness of 1,000 A, it was rather
difficult to make more accurate measurements of the diameter of membrane separation in such a close junction, and to
determine if it were comparable with the
“gap junction” of higher vertebrates
(Uehara and Burnstock, ’70).
A serial sampling of 23 levels of sections
of one particular internuncial cell shows
that this cell has synaptic junctions with
autonomic axons as well as direct contacts with myocardial cells over its entire
length of 15 followed three-dimensionally, rather than at a limited area of its
surface (table 1 ) . In almost all of the 23
levels sampled, 6 to 14 (average 9 ) vesiculated axon profiles are in direct apposition
to the internuncial cell, so as to cover as
much as 25% to 75% of its surface mem-
TABLE 1
23
18
19
20
21
22
17
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
1
Level
52.3
43.2
40.0
42.6
47.8
52.1
49.8
45.4
42.1
40.8
46.8
47.8
44.8
48.6
47.0
27.0
40.0
35.3
38.4
43.2
35.3
24.4
13.8
948.5
Total length
of cell
surface
(cm at 12,800
mamification)
29.4
(3.1% )
-
3.7
1.6
4.4
1.6
1.7
0.9
3.0
-
1.1
1.0
-
1.9
3.2
0.5
0.6
3.0
1.2
Cell surface
covered by
Schwann
cell
urocesses
13.1
23.5
18.0
25.0
27.1
29.6
29.0
25.4
15.4
14.2
18.7
13.4
20.4
27.8
29.4
15.4
30.9
20.0
24.3
19.7
24.4
20.3
12.7
497.7
(52.5% )
Cell surface
contacting
with
vesiculated
axons
11
10
6
10
8
14
9
12
11
9
8
7
8
5
8
10
12
6
11
9
9
9
12
(Number of
vesiculated
axon profiles
in contact)
0.2
36.3
(3.8%)
-
4.7
2.0
2.4
-
-
1.6
2.5
3.0
5.6
2.4
-
1.1
-
4.4
3.9
2.5
Cell surface
contacting
with nonvesiculated
axons
115.9
(12.2% )
16.8
2.2
5.9
8.0
12.0
7.7
7.0
6.2
10.8
5.8
4.6
4.7
3.5
4.7
4.5
5.8
0.8
2.3
2.6
Cell surface
contacting
with cardiac muscle
cells
123.4
(13.0% )
1.3
16.0
7.6
6.4
5.6
5.7
6.2
7.5
5.7
5.4
5.9
9.3
7.2
10.1
6.8
8.0
0.9
1.3
3.8
2.7
Cell surface
contacting
with other
internuncial
cells
0.8
136.1
(14.3% )
1.9
2.6
6.8
17.5
9.6
4.2
15.2
7.6
5.9
5.0
3.3
1.5
2.6
2.5
2.1
4.7
3.7
5.7
6.5
11.5
11.7
9.5
(1.0% )
-
-
-
-
0.4
-
0.4
-
-
-
-
0.7
-
-
-
+
+
+
+
+
+
+
+
+
+
+
Cell surface Appearance
contacting of the interwith unnuncial cell
identified
nucleus
cells
at levels
4.5
2.3
4.4
Cell surface
exposed to
connective
tissue
space
Measurements of the s w f a c e of an internuncial cell at 23 levels sampled for electron microscopy. The interual from one level to the next is 0.5 f 0.4 p,
0.4 ,U between levels 4 and 5 . A whole circumference
except f O T 1.0 k 0.4 p between levels 1 and 2 , 2 and 3 , 5 and 6 , 8 and 9, 13 and 14, and 1.5
o f the cell was recorded at all levels except for level 16, where about a half of a cell profile was intersected by a grid bar
NODAL TISSUE OF FISH HEART
brane at each level. An axon-internuncial
cell synapse, which is observed to occur i n
20 of the 23 levels, is actually formed by
one to five of those vesiculated axon profiles at each level. Since the sampling
method in the present study does not permit following the courses of individual
axons three-dimensionally, nothing can be
said about the number of axons making
synapses on a n internuncial cell.
When, in a plane of section, seven internuncial cells cut in the nuclear region
were examined, 34% to 67% (average
48.3% ) on their surface is revealed to be
covered by autonomic axons and 0% to
34% (average 18.6%) by nodal myocardial
cells. This observation implies that the particular cell subjected to the three-dimensional analysis (table 1) is not a special
case, but represents a standard character
of a n internuncial cell in the nodal tissue
of the loach heart.
The cellular processes of the internuncial cell also form synapses with autonomic
axons and at the same time are in a close
junction with the nodal myocardial cell
(figs. 4, 8). I n a plane of section, such
cellular processes are mixed with the profiles of axons, myocardial cells, and cell
bodies of the internuncial cell. Cytoplasm
within the internuncial cell process is
characteristically clear and contains no
synaptic vesicles. Its content of mitochondria, which resemble those within the
mother cell bodies and are fundamentally
different from intra-axonal mitochondria
(figs. 3 , 4), serves to differentiate the internuncial cell process from a thick, nonvesiculated segment of a n autonomic
axon. Also, the internuncial cell process is
to be distinguished from the myocardial
cell portion lacking myofibrils by its content of fine filaments running in random
directions (fig. 8).
Judging from the fact that the internuncial cell process is virtually absent in
regions where internuncial cell bodies do
not appear, the process from the internuncial cell seems not as long as axons from
nerve cell bodies. Because of the technical
limitation of serial sampling, it is impossible to follow the individual processes i n
the present study. However, in a fortuitous
level of section a tapering cellular process
about 2 p thick i n its initial segment ex-
41 1
tends from one pole of an internuncial cell
body. In that case the cellular process was
cut longitudinally for a length of 7 p, and
its cytoplasmic content showed no drastic
changes at the transitional zone to the
cell body.
The internuncial cell body and its processes sometimes contact other cell bodies
or processes of their own kind. No specialized junctions occur in the contact area
between the internuncial cells. About
14.3% of the surface of an internuncial
cell is uncovered by any cellular element
in the nodal tissue and is exposed to the
extracellular space through a faintly preserved basal lamina substance.
Nerve cells. Nerve cells are larger
(average size: 10
X 20
at nuclear
levels) than the internuncial cell. The perikaryal cytoplasm, being more voluminous
than in the internuncial cell, possesses all
of the ultrastructural characteristics of
neuronal cytoplasm, i.e., richness in free
ribosomes and cisterns of the granular endoplasmic reticulum, multivesicular bodies,
lysosomes, and neurotubules (figs. 10, 11).
It is remarkable that the nerve cell bodies,
even when they occur singly, tend to be
more or less isolated from the nearby myocardial and internuncial cells. The axon
terminals impinging on the nerve cell
bodies are much fewer than those on the
internuncial cell surface; only one or two
profiles of axons are usually observed
around the neuronal soma at each sectional level, so that the chance to encounter the axosomatic synapse (fig. 10)
is relatively remote. Thus, in contrast with
internuncial cells a major portion of the
surf ace of the nerve cell soma is covered by
a satellite cell or its processes (fig. 11).
By measurements at 22 levels of the surface of one particular nerve cell body
serially sampled for a distance of 16 p, it is
clear that 96.4% of the total cell surface
of the soma is covered by the satellite cell,
1.8% by vesiculated axons, 0.5% by nonvesiculated axons, 0.5% by the cytolemma
of other neuronal soma, and 0.9% by unidentified cellular profiles. The nerve cell
body subjected to this analysis is revealed
to receive axosomatic synapses at three
separate sites on its surface. In addition to
the axosomatic form, the axodendritic
form of synapse also occurs between pre-
412
A. YAMAUCHI, Y. FUJIMAKI AND R. YOKOTA
ganglionic fibers and the nerve cell in
nodal tissue.
At the contact area between neighboring
nerve cell bodies, no specializations like an
attachment plaque or a synapse are found.
The apposed membranes in this case are
separated by an irregular gap about 200 A
across with no intervening basal lamina.
Contact between a nerve cell body and a
nodal myocardial cell was not observed.
Myocardial cells. Myocardial cells in
the sino-auricular nodal tissue of the loach
heart, as in those in the trout heart
(Yamauchi and Burnstock, ’68), receive a
dense supply of autonomic nerve terminals.
A specialized junction between the vesiculated axon and the myocardial cell surface
is encountered frequently (figs. 12, 13). In
regions of specialized neuromuscular contact the interspace measures about 200 A
in width, and is more constant in width
than the interspace between plasma membranes elsewhere. A presynaptic accumulation of electron-opaque material, together
with an aggregation of small clear vesicles
300-500 A in diameter, is always associated with the axolemma in apposition, but
no appreciable differentiations are present
on the postsynaptic side of the neuromusc d a r junction, except for an occasional
occurrence of a subsynaptic cistern adjacent to the sarcolemma.
Myocardial cells in the sino-auricular
node of the loach heart are 4-7 ,U in width
and in many sectional levels have poor
development of myofibrils within the cytoplasm. They are connected with the internuncial cell by an attachment plaque with
an occasional close junction, and with
other myocardial cells by an intercalated
disc which also contains a patchy locus
of the close junction essentially similar to
that shown in figure 8, whereby the extracellular space appears to be virtually
obliterated. A morphological feature distinguishing the sino-auricular nodal myocardial cell from the auricular muscle cell
is complete absence in the former of granulated vesicles, 1500-3000 A in diameter;
these characterize the sarcoplasm of the
auricular muscle cell. Also, the innervation density is much lower for the auricular muscle cells than the nodal myocardial
cells.
DISCUSSION
Cardiac internuncial cells described for
the first time in the present study in the
nodal tissue of the loach heart show a morphological similarity to the “interstitial
cells” previously found in the avian and
mammalian smooth muscle by Imaizumi
and Hama (’69), in that they are interposed between the autonomic axon and
the effector cell. Nevertheless, the term
“interstitial cell” was avoided in the present
study considering the risk that such a term
may imply a connective tissue cell. The
terminology, internuncial cell, emphasizes
the location of the cell so named within
the neuronal link of the autonomic innervation apparatus. The finding of a number
of separate axons terminating on each
cardiac internuncial cell further supports
the idea that the cell plays an associative
role like those cells called internuncial in
the central nervous tissue (Ranson and
Clark, ’59).
In analogy to the autonomic “interstitial
cell” described by Imaizumi and Hama
(’69), i t seems resonable to anticipate that
a cell junction of low-resistance impulse
conduction (tight junction called by these
authors) would exist also between cardiac
internuncial and myocardial cells in the
fish heart. The present observations were
made on sections which were rather thick
(0.1 p ) to resolve leaflets of cell membrane, thus revealing the presence of no
more than close membrane apposition between internuncial cell processes and effectors. In order to clarify more details of the
efferent pathway of cardiac internuncial
cells, it is necessary to reexamine the tissue
with thinner sections. Also to be checked
is how the dimensions of a low-resistance
pathway, if present, could be altered by
the choice of a variety of preparatory procedures for demonstration of such structure by electron microscopy (Dewey and
Barr, ’64; Uehara and Burnstock, ’70).
Since the presence of internuncial cells
has not been recognized in cardiac muscle
of the loach heart except for the sinoauricular nodal tissue (unpublished) nor
in any part of the heart of other species
of fish (Yamauchi and Burnstock, ’68;
Santer, ’72), it is clear that the distribution of such a cell type is limited to a considerable extent. In view of the usual small
NODAL TISSUE OF FISH HEART
413
amount of tissue that can be sampled for copy in heart of the trout (Yamauchi and
electron microscopy, however, additional Burnstock, ’68), loach (Yamauchi, ’69)
studies are needed to show whether a and the plaice (Santer, ’72). The present
species difference actually exists in the study further shows that a specialized synoccurrence of internuncial cells within the aptic junction exists between the autofish heart and, alternatively, whether these nomic axon terminals and the myocardial
cells occur commonly but in a rather con- cell surface in the sino-auricular nodal
fined area of cardiac nodal tissue in fish tissue of the loach heart. An accumulation
of many species. Further the same state- of synaptic vesicles near the appositional
ment applies to other vertebrate classes axolemma and a presence of the presynincluding mammals, where a number of aptic “thickening” of the axonal membrane
earlier electron microscopic studies have at such neuromuscular junctions fulindicated a n absence of the internuncial fill the morphological criteria for identifycells between axons and effectors, leading ing synapses in general (Peters et al., ’70;
the investigators to conclude that “inter- Gray, ’71).
No kind of structural specialization has
stitial cell of Cajal” corresponds to a fibroblast (see Rogers and Burnstock, ’66) or a yet been recognized in the contact region
Schwann cell (Hager and Tafuri, ’59; between autonomic terminal axons and
Nemetschek-Gander, ’64). It is noteworthy myocardial cells of the vertebrate heart,
that Honjin et al. (’65) find by electron except for a n observation by Novi (’68) of
microscopy a n autonomic axon-internun- a neuromuscular junction in the rat vencia1 cell synapse in the tunica mucosa of tricle where a myocardial cell, separated by
the human intestine, although the relation- 660 A from a vesiculated axon, showed a
ships of the internuncial cell with the local thickening of its sarcolemma with a n
effector, smooth muscle cells remain un- adjacent postsynaptic web. In contrast
with the rat heart, the specialized neuroclarified.
There seems to be a considerable species muscular junction in the fish heart has no
or regional difference in the number of differentiations on the postsynaptic side exnerve endings received by a n internuncial cept for a n occasional subsynaptic cistern,
cell in the autonomic effector tissues of ver- but constantly has axoplasrnic dense matebrates. Thus, whereas only one vesiculat- terial aggregated close to the presynaptic
ed axon appeared in a plane of section to membrane.
make a synapse with the internuncial cell
Those myocardial cells with dense inin the avian and mammalian alimentary nervation have in general a poor developcanal (Honjin e t al., ’65; Imaizumi and ment and random orientation of myoHama, ’69), the present study shows from fibrils within their cytoplasm. This observaone to five synapses in any plane of section tion coincides with that previously made
through the internuncial cell of the fish i n the trout heart (Yamauchi and Burnheart. Although the actual number of stock, ’68), but varies with the situation
axons terminating on an internuncial cell in the heart of plaice where Santer and
and the number of myocardial cells con- Cobb (’72) found no basic difference in
tacted in turn by the same internuncial the structure between the sino-auricular
cell remain obscure in the present study, a myocardial cells and the rest of the myomasked difference between the percentage cardium. Membrane-bound granules spearea of vesiculated axon-internuncial cell cific to the auricular myocardial cell cytocontact (52.5% ) and that of the in- plasm are absent from the sino-auricular
ternuncial cell-myocardial cell contact myocardial cells of the loach and trout.
(12.2% ) suggests that the internuncial
In regard to nerve cells in the heart
cell in the fish is concerned with input of lower vertebrates including fish, it has
from a large number of neuronal sources been observed (unpublished) that they
and in output to a relatively confined area tend to occur singly or in small groups
of the effector tissue.
rather than forming an encapsulated ganAn extremely rich innervation of the glion mass as is typical of the mammalian
myocardial cells at the sino-auricular junc- heart. Whether nerve cell dispersion within
tion has been revealed by electron micros- the sino-auricular nodal tissue of the fish
414
A. YAMAUCHI, Y. FUJIMAKI AND R. YOKOTA
may simply reflect a primitive state of
phylogeny for the cardiac ganglion, or may
be significant in facilitating nervous regulation of the nodal activities remains to be
clarified .
ACKNOWLEDGMENTS
A part of this work was carried out in
the Tokyo Metropolitan Institute for Neurosciences during the tenure by A. Y. of a
Guest Research Fellowship. We acknowledge with thanks technical assistance from
Mr. K. Kumagai and Miss K. Tsushida, and
photomicrographic work by Mr. M.
Takahashi.
LITERATURE CITED
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(Cavia
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Honjin, R., A. Takahashi and Y. Tasaki 1965
Electron microscopic studies of nerve endings
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PLATES
PLATE 1
EXPLANATION OF FIGURES
1 A photomicrograph to show the location of sino-auricular nodal tissue
(NT) in the heart of a loach, Misgurnus anguillicaudatus. The principal portion of the nodal tissue lies at the base of the venous valve
(VV), whereas the tail of the nodal tissue spreads towards the free
margin of the venous valve, which separates the sinus venosus (S)
from the auricle ( A ) of lhe heart. V, ventricle. Calibration: 100 p.
2
A photomicrograph of the sino-auricular region showing continuity
between the nodal tissue (NT) and the auricular myocardium (A).
VV, venous valve, NC, nerve cell bodies within the nodal tissue.
Calibration: 50 p.
3 An electron micrograph from the sino-auricular nodal tissue of a
loach, showing its content of myocardial cells ( M l , M2), an internuncial cell body ( I 1) and numerous axon terminals, e.g., A l , A2.
Note that appearances of internuncial cell processes (12, 13) are different from the preterminal thick axon ( A 3 ) . A part of this micrograph is enlarged in figure 4. Calibration: 5 p.
416
NODAL TISSUE OF FISH HEART
A. Yamauchi, Y. Fujimaki and R . Yokota
PLATE 1
PLATE 2
E X P L A N A T I O N OF FIGURE
4 A higher magnification of the internuncial cell body labelled I 1 in
figure 3. The cell (level 7 of serial sampling, table 1 ) is in direct
contact with 11 vesiculated axon profiles as well as with a myocardial cell ( M l ) . Three of those vesiculated axon profiles synapse
with the surface of the internuncial cell body. The area i n the
rectangle includes a portion of an internuncial cell process ( I 2 ) and
a myocardial cell ( M 2 ) and corresponds to the area shown in figure 8
at higher magnification. Other processes of the internuncial cell ( I 3,
14) are distinguished easily from axons due to their content of
mitochondria which resemble those in 1 1 . Calibration: 1 p .
418
NODAL TISSUE OF FISH HEART
A. Yamauchi, Y. Fujimaki and R. Yokota
PLATE
a
419
PLATE 3
EXPLANATION O F FIGURE
5
420
Level six of the same internuncial cell body as shown in figure 4
( I 1). Note an extensive development of the Golgi complex in the
perikaryal portion of the internuncial cell cytoplasm. Arrows indicate
fine filaments running in random directions within the perikaryal
cytoplasm. Areas in the rectangle are enlarged in figures 6 and 7.
Calibration: 1 w.
NODAL TISSUE OF FISH HEART
A. Yamauchi, Y. Fujimaki and R. Yokota
PLATE 3
421
PLATE 4
EXPLANATION O F FIGURES
6-7
422
Axon-internuncial cell synapses are shown at a higher magnification.
Occurrence of an intermediate band in the synaptic cleft is indicated by arrows. SC, subsynaptic cistern. Also note the presence of
fine filaments in the internuncial cell cytoplasm. Calibration: 0.5 p .
NODAL TISSUE OF FISH HEART
A. Yamauchi, Y. Fujimaki and R. Yokota
PLATE 4
423
PLATE 5
EXPLANATION O F FIGURES
8
A n attachment plaque between a process of a n internuncial cell ( I )
and a myocardial cell ( M ) is shown in between single arrows. At
a patchy locus of close junction (double arrow), the extracellular
space appears to be almost obliterated. This micrograph is from
one of the five sections mounted on a grid, another section being
used to make a record of the internuncial cell shown in figure 4.
Calibration: 0.1 p.
9
A portion of the seriaIly sampled internuncial celI at level 11. A
cilium emanates from the perikaryal cytoplasm oE the cell. Nu,
nucleus of the internuncial cell. Calibration: 1 p.
10 An axosomatic synapse on a nerve cell body i n the sino-auricular
nodal tissue of a loach heart. Note the presence of neurotubules
within the postsynaptic neuroplasm. Calibration: 1 p.
424
NODAL TISSUE OF FISH HEART
A. Yamauchi, Y. Fujimaki and R. Yokota
PLATE 5
425
PLATE 6
EXPLANATION O F FIGURE
11
426
Nerve cells ( N l , N2), mixed with myocardial cells ( M ) in the sinoauricular nodal tissue of a loach heart. The neuronal soma is distinguished from the internuncial cell body by its content of the
nucleus with a prominent nucleolus, as well as by a n abundance
of ribosomes within the cytoplasm distributed either freely or
attached to cisterns of the endoplasmic reticulum. Also vesiculated
axon profiles in direct contact with the neuronal soma are much
more limited in number than for the internuncial cell. Calibration:
1 w.
NODAL TISSUE OF FISH HEART
A. Yamauchi, Y. Fujimaki and R. Yokota
PLATE 6
427
PLATE 7
EXPLANATION OF FIGURES
12-13
428
Portions of the sino-auricular nodal tissue in the loach heart. A
specialized synaptic junction between the autonomic axon and
the nodal myocardial cell is indicated by arrows. Note the sparsity
of myofibrils i n the nodal myocardial cells ( N i ) . Calibration: 1 p.
NODAL TISSUE OF FISH HEART
A. Yamauchi, Y. Fujimaki and R. Yokota
PLATE 7
429
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misgurnus, teleost, references, heart, tissue, cells, particular, auricular, structure, noda, sino, internuncial, fish, studies, fine, cardiaca
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