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Direct contact between a neuron soma and myocardial cells; an electronmicroscopic finding in the sinus venosus of the turtle heart.

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Direct Contact between a Neuron Soma and Mvocardial
Cells; An Electronmicroscopic Finding in the Sinus
Venosus of the Turtle Heart
1
AKIO YAMAUCHI, YOKO FUJIMAKI AND KENICHI KUMAGAI
Department of Anatomy, Iwate Medical University, School of Medicine,
Morioka 020, J a p a n
ABSTRACT
Electron microscopy of the turtle sinus venosus shows an unusual neuron soma which is immediately surrounded by myocardial cells so as
to form a somato-muscular complex. Studies of 36 sections cut through this
neuron soma indicate that 27.4% of the somal surface studied is directly covered
by cardiac muscle cells without any intervening basal lamina. Similarly, 18.8%
of the somal surface studied is in contact with unmyelinated axons which at
places make typical axosomatic synapses. A coupling of peripheral cisterns of
the sarcoplasmic reticulum and the sarcolemma exists a t the somato-muscular
contiguity as well as at the border between cardiac muscle cells. It is suggested
that neural influences upon the pacemaking activity of the turtle heart sinus
can well be exerted through the somato-muscular pathway. Additionally, an axon
which is presynaptic to the neuron soma has been observed to be simultaneously
in a synaptic relation with a cardiac muscle cell; a remarkable deviation from
the classical picture of the efferent nervous outflow to the heart.
The cardiac ganglion has been treated
only briefly, if at all, in the previous ultrastructure studies of the innervation of the
vertebrate heart (VirBgh and Porte, '61;
Yamauchi and Burnstock, '68; Santer, '72;
Yamauchi, '73). Recent studies which were
more specifically devoted to the ganglionic
synaptology have shed some light on the
two different types of cardiac interneurons,
one a granulated type occurring in the
turtle heart (Chiba and Yamauchi, '73)
and the other a non-granulated type in the
fish heart (Yamauchi et al., '73). As regards the ordinary neurons in the cardiac
ganglion, however, i t remains entirely uncertain whether they may be subdivided
into classes according to the fine structure
particularly of their synapses or whether
they may represent a rather simple cell
population in which all constituents are
essentially alike.
In the course of studies of ganglion cells
in the sinus region of the turtle heart, we
encountered a neuron soma immediately
surrounded by cardiac muscle cells. An
analysis of the fine structure of this pecuANAT. REC., 179: 491-4913,
liar somato-muscular complex and its innervation will be presented in this paper.
MATERIALS AND METHODS
A soft-shelled turtle, Pseudemys scripta
elegans, was decapitated and the heart
quickly removed into a 2.5% solution of
glutaraldehyde buffered in 1/15 M phosphate at pH 7.4. The sino-auricular region
of the heart was then excised under a dissecting microscope, postosmicated, dehydrated in ethanol and embedded in Epon
812 (Luft, '61) through an infiltration
medium, n-butyl glycidyl ether (Kushida,
'63). Sections were cut at about 0.1 on
a Porter-Blum microtome from the sinus
wall, mounted on a series of grids, stained
with uranyl acetate and lead citrate (Reynolds, '63), and viewed in the electron microscope.
Recordings of one particular neuron
soma in contact with cardiac muscle cells
were made at 36 different sectional levels.
Using a thin thread, lengths of the surface
of that neuron were measured on the elecReceived Nov. 8, '73. Accepted Jan. 30, '74.
49 1
492
A. YAMAUCHI, Y. FUJIMAKI AND K. KUMAGAI
tron micrographs at a magnification of
16,000 times obtained at each recorded
level.
OBSERVATIONS
The wall of the sinus venosus of the
heart of Pseudemys scripta elegans contains a well-developed cardiac muscle
layer, which is attached to islets of smooth
muscle cells located subendocardially.
Nerve cell somata are for the most part
encountered in the subepicardial connective tissue space, but a few of them are
present within the muscle layer as well as
in the subendocardial space in the sinus
wall.
The somato-muscular complex to be reported here as a single case in a single
turtle heart consists of a neuron soma
which is intimately surrounded by cardiac
muscle cells at the border of myocardial
layer and the subendocardial connective
tissue space in the sinus wall (fig. 1). This
neuron soma, like many other nerve cell
bodies in the turtle heart, is rather small
in size (about 10 X 15 p ) but is identifiable as such because, first of all, it receives
the axon terminal synapsing upon its surface (fig. 2). Second, the soma1 nucleus is
large and contains the electron-lucent
karyoplasm with a very conspicuous nucleolus (fig. l ) , which is typical of the neuron in general. Third, the perikaryal cytoplasm of the soma contains at places a
considerable amount of the ribosomes
which are set into small, polysomal rosetts,
in a manner being recognized as characteris)tic of nerve cells (Peters et al., '70).
And fourth, the thin sheet of satellite cell
processes is present attached to a part of
the surface membrane of the soma (fig. 1),
At the contact zone between the soma
and the muscle cell, the plasma membranes are apposed leaving a narrow gap
about 200 A in width, where no basal
lamina substance is detectable, Subsarcolemma1 cisternae containing a dense material are observed to occur not only at the
somato-muscular, but also at the axo- muscular (fig. 2 ) and the myo-myal (fig. 1 )
junctions.
When the surface lengths of the neuron
soma with its initial processes are measured at 36 planes of thin sections, i t be-
comes evident that 27.4% of the total surface is covered by cardiac muscle cells,
18.8% by axons. (table 1 ) . The vesiculated segment of axons forms an axosomatic synapse at two separate loci on the
surface membrane of the neuron soma.
Profiles of those axons synapsing to the
neuron soma are large in size, and the axosomatic contact length measures up to
6 p. This finding suggests the occurrence
of a large, probably calyciform axon terminal which covers a considerable area of a
neuron soma within the turtle heart. Of
particular interest is a case of the axosomatic synapse (fig. 2), where an axon
terminal presynaptic to the neuron soma
shows at the same time a broad contact
with the cardiac muscle cell, which in turn
abuts against the neuron soma.
All the presynaptic boutons revealed in
the present study show a predominance of
agranular synaptic vesicles with a few,
large granular ones: A vesicular content
typical of cholinergic nerve terminals.
DISCUSSION
The sinus venosus of the turtle heart
has been known, for a long time, to have
a muscular wall where the dominating
rhythm of the heart originates normally
(Gaskell, 1883; Keith and Flack, '07; Meek
and Eyster, 15-16). Much attention was
also focused in these earlier studies on the
nerve cells and fibers situated in the sinus
wall, being in connection with the vagal
and sympathetic nerve trunks.
The somato-muscular complex disclosed
presently in the sinus venosus of the turtle
heart provides an unusual pathway of impulses from the postganglionic parasympathetic (see below) neuron to the effector,
myocardial cells. Direct apposition between
Fig. 1 A neuron soma-cardiac muscle complex i n the sinus venosus of a turtle heart. The
neuron soma in this level of sections (Level 8
in table 1 ) contains a large nucleus ( N ) with a
prominent nucleolus (Nu) and shows a small
process (P). Two profiles of the cardiac muscle
cell ( M l , M2) are in direct contiguity to the neuron soma. A n axon (A), which is i n contact with
both a cardiac muscle cell ( M l ) and the neuron
soma, forms synapses to those elements at the
other sectional level shown i n figure 2. Arrows
indicate subsarcolemmal cisternae occurring at
the border between myocardial cells. S: Satellite
cell sheath of the neuron soma. Calibration: 1 p .
NEURON SOMA-CARDIAC MUSCLE CONTIGUITY
493
494
A. YAMAUCHI, Y. FUJIMAKI AND K. KUMAGAI
Fig. 2 A typical synapse between the axon ( A ) and the neuron soma ( S ) is indicated
by a double arrow. Level 10 i n table 1. Single arrows show the occurrence of subsarcolemmal
cisternae at the junctions between the axon and a cardiac muscle cell ( M 1 ) and between
the soma and cardiac muscle cells (M1 and M2). Calibration: 0.5 p.
the neuron soma and the muscle cells
would obviously enable fewer effectors to
be brought under the more intense care
of a postganglionic neuron than the ordinary connection between the postganglionic axon branches and the effector
cells.
In view of the presence of large, heavily
vesiculated axon terminals presynaptic to
the neuron soma described in the present
study, there is little room for supposing
that this particular neuron should represent the intracardial sensory neuron put
forward by Skok ( ' 7 3 ) . On the other hand,
a previous work (Chiba and Yamauchi,
'73) has indicated an absence of adrenergic
neuron soma in the heart of the turtle. The
exception is the chromaffin cell type adrenergic interneuron whose ultrastructure
was quite different from that of the ordinary neuron soma as shown in this study.
Based on the above facts, i t is considered
that the nature of the neuron soma presented here would certainly be postganglionic, cholinergic and most probably
parasympathetic. As far as we know, a
well-developed axosomatic synapse characterizes the parasympathetic (cardiac,
ciliary and intestinal at least) ganglia of
the vertebrates (cf. Szentagothai, '64; Taxi,
'65; Gabella, '72; Yamauchi, ' 7 3 ) .
Present observations of a preganglionic
axon which directly terminates o n a myocardial cell provide evidence of a remarkable deviation from the classical concept
of the arrangement of the parasympathetic
outflow.
The subsarcolemmal cisternae containing an amorphous material have been
recognized in the myocardial cells of lower
vertebrates (Sommer and Johnson, '70;
Beringer and Hadek, ' 7 3 ) . An impression
was obtained in this study that those cisternae in myocardial cells of the turtle
sinus venosus are so indiscriminately distributed as to make their significance in the
intercellular impulse transmission rather
difficult to imagine. They might well bear
a metabolic function, e.g., in transport or
export of proteins that may be involved in
the movement of calcium (Sommer and
Johnson, ' 7 0 ) .
495
NEURON SOMA-CARDIAC MUSCLE CONTIGUITY
TABLE 1
Measurements of the surface of a neuron soma in the turtle heart sinus venosus, made at 36 levels
sampled from 60 serial sections mounted on 20 successive grids. The interval from one level to the
next is not more accurately known than to be less than about 0.8 p. The whole circumference o f the
neuron soma with its initial segment of processes was estimated at all levels except for level 7, where
about a quarter of a neuronal profile was intersected by a grid bar.
Level
Total length of
neuron surface
(cm at 16,000
magnification)
1
2
3
4
5
6
7
8
9
10
11
12
13
14
15
16
17
18
19
20
21
22
23
24
25
26
27
28
29
30
31
32
33
34
35
36
91.7
86.2
85.0
77.5
81.2
82.0
68.8
79.2
60.1
73.3
52.7
61.7
60.9
63.3
64.3
64.7
71.0
69.9
69.3
54.4
53.5
54.1
51.0
50.6
53.5
47.8
46.7
45.7
53.5
48.3
50.2
43.5
39.7
42.2
52.4
42.9
S u m total
The neuron surface
in contact with
vesiculated and
non-vesiculated
axons
2192.8
ACKNOWLEDGMENTS
We are grateful to Miss R. Yokota for
advice and Miss K. Tsushida for her expert assistance in typing the manuscript.
LITERATURE CITED
Beringer, T., and R. Hadek 1973 Ultrastructure of sinus venosus innervation in Petromyzon marinus. J. Ultrastruct. Res., 42: 312323.
Chiba, T., and A. Yamauchi 1973 Fluorescence
and electron microscopy of the monoaminecontaining cells in the turtle heart. Z. Zellforsch., 140: 25-37.
The neuron surface
in contact with
myocardial
cells
22.5
21.7
20.6
10.2
15.5
15.4
14.1
17.2
8.1
14.5
8.1
7.5
7.8
9.0
7.4
6.7
9.8
7.6
10.6
17.6
16.0
15.8
22.5
21.5
24.7
10.5
6.2
5.0
5.2
5.5
4.2
4.0
4.7
5.0
4.6
4.2
17.0
15.9
15.7
16.3
24.7
25.5
23.7
23.O
18.2
23.8
17.8
17.5
20.8
22.0
21.0
22.5
24.0
24.7
23.7
17.8
15.5
14.7
8.0
8.6
8.1
9.1
10.5
10.7
13.3
14.0
17.0
11.0
9.5
10.5
13.6
11.0
411.5
(18.8%)
600.7
(27.4%)
Appearance
of the nucleus
of the neuron
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+
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-
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