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Innervation of the vibrissae of the California sea lion Zalophus californianus.

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Innervation of the Vibrissae of the California
Sea Lion, Zalophus californianus
R. J. STEPHENS, I. J. BEEBE
AND
T. C . POULTER
(WITH TECHNICAL ASSISTANCE OF H. E. NEWTON)
Life Sciences Division, Stanford Research Institute,
Menlo Park, California 94025
ABSTRACT
The vibrissae of the California sea lion are richly innervated
with myelinated fibers that terminate in three distinctly different endings. Large
nerve bundles enter the base of the follicle and immediately branch into smaller
bundles that traverse the connective tissue trabeculae below the large ring sinus.
Some neurons terminate in a lamellated corpuscle in close relationship to the
venous sinuses of the proximal cavernous tissues. The remainder of the nerves
continue distally parallel to the glassy membrane terminating in two specific
types of endings arranged in a ring about the shaft of the vibrissae at the level
of the upper portion of the ring sinus. One type of ending is on the outer surface
of the glassy membrane where the myelin sheath terminates abruptly and the
sensory ending is flattened into a thick, lancet-shaped structure. A n extension of
cytoplasm from a specialized supportive cell covers this terminal segment of the
nerve on two sides, while numerous finger-like extensions protrude into the connective tissue from the narrow, uncovered sides. The second type of ending penetrates the glassy membrane, branches, and terminates in close apposition to the
Merkel cells in the outer root sheath. Amyelinated nerves of various sizes are
frequently observed in the same bundles as the larger myelinated fibers, but to
date, the position of their termination has not been established.
Vibrissae or tactile hairs are a mammalian characteristic that, according to
Vincent ('13), rank f i s t in phylogenetic
appearance and have been the subject of
considerable study for more than a century.
Advanced techniques used in recent years
in investigations related to both the structure and function of peripheral sense reception have greatly increased our understanding of this phenomenon. Andres'
('66) elegant comparative ultrastructural
study of the sinus hairs of the rat, rabbit,
and cat has given us a new perspective of
the complexity of the innervation in these
organs and neurophysiological studies
such as those of Zucker and Welker ('69)
and Iggo and Muier ('69) have also been
particularly valuable in advancing our
comprehension of the functional attributes
of these important structures. To our
knowledge, however, innervation of vibrissae, which are considered to be the most
highly evolved in the pinnipeds (Ling, '66)
ANAT. Rm., 178: 421442.
has not been previously studied in the California sea lion.
According to Poulter ('63a), the sea lion
displays a well-developed sensory localization facility in its underwater environment, and biosonar studies raise important
questions as to acoustic reception by this
animal (Poulter, '63b). In particular, these
questions concern the possibility that
vibrissae may play a role in sound-receiving biological transducer systems. This
complex problem will eventually require an
interdisciplinary effort; however, the present study was undertaken to establish the
nature of the nerve endings relative to the
vibrissae. Although this investigation
should not be regarded as exhaustive, three
types of receptors have been established
and will be described and compared with
those previously reported in the literature
for other species. In addition to traditional
questions, a full understanding of the funcReceived Jan. 23, '73. Accepted April 13, '73.
421
422
R. J. STEPHENS, I. J. BEEBE AND T. C. POULTER
ultramicrotome, and stained with toluidine
blue. Subsequently, the same blocks were
retrimmed to selected areas of interest for
MATERIALS AND METHODS
ultrathin sectioning. Sections were placed
The tissue for this study was obtained on uncoated nickel grids and doublefrom two California sea lions. One was stained with lead citrate and uranyl acetate
found paralyzed in the hindquarters along before observation with a Philips 200 electhe Pacific Coast below San Francisco. This tron microscope.
animal was taken to the Stanford Research
A number of vibrissae were also fmed in
Institute (SRI) Marine Laboratory, where 10% formalin for routine preparation for
it was sacrificed by inhalation of Fluoro- light microscopy. This tissue was dehythane. Several vibrissae were removed drated and embedded in paraffin prior to
quickly, and the large follicle at the lower sectioning at 7 and staining with hemaend was sliced in half longitudinally before toxylin and eosin. Observations on this
fixation in either 2% glutaraldehyde buf- tissue assisted in the interpretation of the
fered with Veronal acetate to a pH of 7.3, plastic-embedded material.
or in 1% OsOl with the pH adjusted to the
OBSERVATIONS
same level with the same buffer, and with
Although the general organization of the
the addition of 7% sucrose. The tissue
placed in glutaraldehyde was allowed to tissue will be presented in this paper, emfix for two hours and was then washed in phasis is placed on elements of the nervous
several changes in buffer before refixation system, where three types of nerve endings
are recognized. A three-dimensional diain 1% OsOr.
A single vibrissa was removed as a gram (fig. l) has ben prepared to assist
biopsy from a healthy animal that had the reader in a full appreciation of the
been in captivity at the Marine Station for spatial relationship of this complex sensory
some time. Osmium tetroxide fixative was organ.
Light microscopy. The histological feaimmediately injected through the outer
connective tissue sheath of the follicle into tures of the sinus hairs of the California
the circular sinus. ‘This procedure accom- sea lion are similar to those described in
plishes two things: first, fixation of the other species, although certain morphodeeper areas is begun immediately, and logical differences exist. The outer capsule
second, the excess blood in the ring sinus of the follicle at the base of each vibrissa
and erectile tissue that interferes with good consists of dense connective tissue (figs.
fixation is flushed away. The outer capsule 1-4) that stains intensely with toluidine
of the bulb was removed in a volume of the blue (fig. 4). The shaft of the hair extends
same fixative so that thorough fixation deeply into the bulbous basal structure
could be accomplished. All tissue was de- (figs. 1, 2 ) , and much of the tissue behydrated in a graded series of ethanol and tween the shaft and the outer capsule repassed through propylene oxide before in- sembles typical erectile or cavernous tissue
filtration and embedment in Araldite.
(figs. 1, 2, 5). A large ring sinus circumWhile the tissue was in 50% propylene vents the shaft of the vibrissa slightly beoxide and 50% Araldite, the hard central low the center of the bulb (fig. 2 ) , and a
part of each vibrissa was removed and the prominent “ringwulst” (ring bulge), conbulb was carefully dissected, under a sisting largely of fine collagen fibrils, prostereomicroscope, into blocks suitable for trudes from the shaft side into the ring
embedding in plastic. Each block was care- sinus (figs. 1-3, 10, 1 1 ) . The cavernous
fully numbered so that its relative position tissue below the ring sinus is more extento the other blocks was known. The pro- sive than that above it, but in both cases
cedure was invaluable to future interpreta- trabeculae of connective tissue transverse
tion of the findings. Since most of the the areas between the anastomotic sinuses,
observations were to be made with the light which are lined by squamous endothelium
microscope, relatively large blocks were (figs. 5-8).
embedded in Araldite, sectioned at 1
The major blood and nerve supply to the
with a glass knife on a Porter-Blum MT2 follicle enters from the basal aspect, where
tion of these organs may also be important
to the interpretation of sonar reception.
INNERVATION OF SEA LION VIBRISSAE
the capsular sheath is thin (figs. 1-3).
Large bundles of nerves (figs. 3, 4 ) penetrate the capsule and divide into numerous
smaller bundles as they pass through the
cavernous tissue below the ring sinus (figs.
1, 3-5). Occasionally, single neurites are
observed within the trabeculae of connective tissue (fig. 6 ) ; they are also observed
in a connective tissue sheath protruding
into the venous sinusoids (fig. 7 ) . These
structures are not numerous and terminate
in what appears to be a lamellated corpuscle in close association with the sinusoids
(figs. 8 , 9). The simple investment of connective tissue around the single neurite
(figs. 6, 7) becomes more complex as it
approaches the terminus (figs. 8,9),where
several layers of cells with attenuated cytoplasm surround a central cell (fig. 9). A
thin lamina, consisting of endothelium and
a small amount of connective tissue, lies
between the sinusoid and the terminal
structures of the nerve. Details of the relationship between the single sensory fiber
(figs. 7, 8) and the cell located in the
central portion of the terminal enlargement (fig. 9) are not yet clear. The centrally located cell is surrounded by concentric layers of squamous cells, giving
an onion-like appearance (fig. 9). These
layers of cells are separated by spaces that
are apparently filled with a highly hydrated
substance, as the only elements observed
within them are fine strands of material
(fig. 9).
Nerves that do not terminate in the
lower sinusoid area continue on in small
bundles along the shaft of the vibrissae,
outside the glassy membrane. They run
through the basal portion of the ringwulst (fig. lo), where they remain in small
bundles (fig, 11). The glassy membrane
covers the external root sheath and varies
in thickness along the length of the shaft.
It is thickest beneath the ringwulst (fig.
l o ) , and its internal surface is irregular
at this point (figs. 11, 12). The longitudinal orientation of the fine collagen fibers
of the ringwulst runs from the glassy membrane, where they insert as tufts on the
glassy membrane (figs. 11, 12), outward
toward the sinus (fig. 1 1 ) . The glassy
membrane becomes considerably thinner
immediately above the ringwulst (cf. figs.
11, 13), and the small bundles of nerves
423
become dispersed into a layer immediately
outside the glassy membrane (figs. 13,
14). Many of the sensory fibers are large
and have a prominent myelin sheath (figs.
14, 15).
Two types of nerve endings are recognized at this position, where the neurites
turn sharply toward the glassy membrane.
One termination is on the external surface
of the glassy membrane (figs. 15, 16),
and the other penetrates the membrane
and ends in conjunction with specialized cells in the outer root sheath called
Merkel cells (figs. 17-20). It was noted
that at the level of the upper edge of the
ringwulst, numerous tufts with a dense
central structure were present along the
glassy membrane when the tissue was cut
in cross-section (fig. 16). Similar tufts
lower on the shaft possessed no central
structure (fig. 14). Careful analysis of
longitudinal serial sections of many tufts
in this area at the light microscope level
revealed a complex organization (fig. 1 5 ) .
The central structure of the tuft is confluent with large myelinated fibers (fig.
15) and is apparently the terminal end of
the neurite. The lighter area (fig. 16) on
both sides of the central core is confluent
with a specialized cell possessing a round
nucleus and a polar cytoplasmic extension
(figs. 15, 23). Many fine collagen fibrils
arise from the central area of the tuft and
some also extend from the area of the
specialized cell (fig. 15). There is no evidence that any cytoplasmic component of
this type of nerve complex penetrates the
glassy membrane.
A second type of nerve ending that penetrates the glassy membrane also exists in
this area. In this case, large myelinated
fibers are observed to approach the glassy
membrane (figs. 17, 18) along with a capillary that is confluent with the ring sinus
(figs. 19, 20). Although there is no evidence that the capillary actually penetrates
the glassy membrane, it is located in close
juxtaposition to the nerve at the point
where the nerve continues through the
membrane (fig. 20). Immediately upon
emergence on the internal surface of the
membrane, the nerve branches (fig. 20).
The branches of the nerve continue parallel to the internal surface of the glassy
membrane for some distance, making con-
424
R. J. STEPHENS, I. J. BEEBE AND T. C. POULTER
tact with the so-called “Merkel cells” in the
outer root sheath (fig. 20).
Electron microscopy. Preliminary examination of the nerve-Merkel cell complex
and the nerve ending on the external surface of the glassy membrane has been accomplished with the electron microscope
(figs. 21-24). Once the nerve penetrates
the glassy membrane, it branches repeatedly and terminates in close juxtaposition
to Merkel cells (figs. 21, 22). The Merkel
cell is easily distinguished from the other
cells of the outer root sheath as the cytoplasm contains numerous small, dense
granules of various sizes (figs. 21, 22).
These small granules resemble neurosecretory granules and may be found very close
to the plasma membrane (fig. 22). The
nucleus of this cell is very irregular (fig.
21). The attenuated nerve ending is
closely applied to the plasma membrane of
the Merkel cell, but no synaptic junctions
have thus far been observed between the
nerve and the Merkel cell. Desmosomal attachments are, however, observed between
the Merkel cell and the basal cells of the
outer root sheath. On the side of the nerve
away from the Merkel cell there is usually
a large intercellular space filled with a fine
granular material (figs. 21, 22). Numerous mitochondria are preferentially distributed toward the Merkel cell in this portion of the nerve (figs. 21, 22).
The glassy membrane is constructed of
fine collagen fibrils intermeshed at random
angles (figs. 21,23,24). A basement membrane appears along the surface facing
the outer root sheath (fig. 21), but none is
present on the opposite surface (figs. 23,
24).
The interesting neural complex terminating on the outer surface of the glassy
membrane, seen in figure 15 at the light
microscope level, has also been examined
with the electron microscope (fig. 23). As
the nerve approaches the glassy membrane,
the myelin abruptly terminates and a specialized cell possessing a spherical nucleus
sends a cytoplasmic projection toward the
terminal end of the neuron (fig. 23). The
cytoplasm of this specialized cell sandwiches the terminal nonmyelinated portion
of the nerve between two leaflets of cytoplasm (figs. 23,24). Numerous pinocytotic
vesicles are observed along the entire
plasma membrane of the specialized cell
(figs. 23, 24). A small amount of rough
endoplasmic reticulum is present in the
body of the cell (fig. 23), and the extensions along the nerve possess fine filaments, a few mitochondria, and smooth
tubular membranes (figs. 23, 24). Numerous finger-like processes extend from the
neurite along the length of the terminus
into the surrounding connective tissue,
from between the cytoplasmic leaflets of
the specialized cell (fig. 23), and at its
tip they extend toward the glassy membrane (fig. 24). These structures are surrounded by a fine fibrous material that extends along the outer surface of the entire
complex (figs. 23, 24) and connects with
the glassy membrane. There is no evidence
that these attenuated finger-like structures
extend into or through the glassy membrane. Many mitochondria and small clear
vesicles are present in the distal portion of
the nerve (fig. 24).
In addition to the three types of large
myelinated neurites described above : ( 1 )
the lamellated corpuscle, (2) the lancetshaped terminus and ( 3 ) those ending in
close apposition to the Merkel cells; amyelinated nerves of various sizes were also
observed within the small bundles of peripheral fibers, both in the trabeculae of
the cavernous tissue and in those that
terminate above the ringwulst. To date,
however, it has not been determined where
these amyelinated nerves terminate.
DISCUSSION
The gross size of the vibrissa, also known
as a sinus hair, tactile hair, bristle, feeler,
whisker or sensory hair, with its large
follicle and corresponding blood and nerve
supply, is a striking feature of the California sea lion. Although biologists were
attracted to the study of the integument
over 200 years ago (Haller, 1766) and a
number of papers have since been published on the vibrissae of a wide variety
of species, no concentrated effort has been
pursued in any one species to present a
concrete understanding of their function.
Cauna (’Fig), in a review of sensory receptors, states that “Systematic work for more
than a hundred years has brought no agreement among anatomists on the fundamental questions relating to sensory recep-
INNERVATION OF SEA LION VIBRISSAE
tors, and the principal problems of today
are still the same as they were at the time
of Kolliker (1852, 1863) when nerves were
studied in unstained razor-cut section.” In
all fairness, however, it must be admitted
that considerable progress has been made
during the past decade, Such detailed
anatomical studies as that by Andres (’66)
as well as physiological data obtained by
Zucker and Welker (’69) and contributions
from other investigators (Patrizi and
Munger, ’66; Ling, ’66; Lyne and Hollis,
’71) have significantly advanced our understanding of the structure and function of
vibrissae.
Histologically, the prominent circular
sinus is the “landmark” of distinction in
this specialized sensory organ. A welldemarcated outgrowth into this sinus from
the shaft side has received considerable
attention and is referred to by several
names, including the ringwulst, ring bulge,
pulvinus, kissen, and bourrelet annular.
According to Vincent (’13), this structure
is highly developed in rodents and carnivores but absent in the horse, cow, and
swine. It may be formed of typical erectile tissue (Messenger, ’00) or it may be a
well-defined connective tissue ring as
shown by Andres (’66). A prominent ringwulst is also present in the California sea
lion and appears to be constructed of fine
collagenous fibers oriented mainly with
their long axis running from the shaft
side outward toward the ring sinus. A
sparse number of cells are randomly distributed among the collagen fibrils. It is
gently tapered throughout its circumference, being narrowest in that portion facing toward the nose.
At present, the function of the ringwulst is unknown, but its position and
specific shape make one suspect that it
must have a precise function, and some
investigators have advanced interesting
hypotheses. Melaragno and Montagna (‘53)
speak of the ringwulst in the hairless
mouse as a “balancer” structure. The
mustacial vibrissae in the elephant seal
(Ling, ’66) have a relatively small ringwulst compared to the mouse, and it was
suggested that it might serve other functions besides “vascular regulation.” Its
tapered shape in the sea lion implies a
specific function. It is difficult at present
425
to speculate with any degree of certainty
on what that function may be; however,
we will make a suggestion later in the discussion in conjunction with the lamellated
corpuscles.
Cavernous or erectile tissue in sea lion
vibrissae is present both above and below
the ring sinus; this tissue is less extensive
in other animals and frequently is not
present above the ring sinus. A study was
undertaken by Messenger (’00) to determine if there was any connection between
the vascular mechanism and the sensory
apparatus of the vibrissae of young dogs
and rabbits. He described nerve fibers in
the erectile tissue of the pulvinus, and
scattered ganglion cells were demonstrated
in Golgi preparations. Wrobel (’65) found
nerve endings concentrated in the proximal
part of the sinus in the tree shrew, and
Andres (’66) describes an encapsulated
lamellated corpuscle apparently located in
the same general region of the follicle.
These observations appear to correspond
to the nerves and lamellated terminals containing a prominent central cell described
here in the cavernous tissue below the
ring sinus. Since these structures bear a
resemblance to the pacinian corpuscle,
which has been established as a mechanoreceptor, sensitive to vibrations (Werner
and Mountcastle, ’65; Talbot et al., ’68;
Lowenstein, ’61), it seems reasonable to
suggest that the lamellated corpuscles of
the sinus hair may serve a similar function. Vibrations could be received via the
shaft of the vibrissa and transmitted to
these receptors through the tissue or vascular system. If the cavernous tissue is engorged when the vibrissae receive such
vibrations, the ringwulst may play an important role in transmitting these vibrations from the shaft to the ring sinus. The
vibrations could then be propagated
through the ring sinus to the sinusoids that
are so intimately related to the receptor,
thus initiating a neural response.
Merkel (1875,1880) identified a specialized cell in close apposition to certain
neurites in the stratum germinativum of
the skin. These observations have been
confirmed many times since then, and
several investigators have noted their presence among the basal cells of the external
root sheath of the vibrissae (Vincent, ’13;
426
R. J. STEPHENS, I. J. BEEBE AND T. C. POULTER
Kadanoff, '28; Szymonowicz, '30, '36;
Patrizi and Munger, '66). The excellent
ultrastructural study by Andres ('66) gives
a comprehensive description of these receptors in the vibrissae of terrestrial mammals, and the present observations in a
marine mammal confirm his earlier work,
with only minor differences. The spatial
orientation of the basal cells and neural
elements appear to have a more specific
relationship in the sea lion than in those
species previously reported. The basal or
supportive cell lies on one side of the
Merkel cell, and desmosomal attachments
are observed between the two cell types.
The flattened nerve ending lies on the opposite side of the Merkel cell and a large
interstitial space Wed with a fmely granular material separates the nerve from the
next basal cell. The sequence is then repeated. At present, it is not known if this
special organization has functional significance. Synaptic junctions between the
Merkel cell and the neurite, described by
Andres ('66), were not observed in the
present study, and further work is necessary before a definitive statement can be
made as to whether they exist. Dense granules in the Merkel cell were seen in contact with the plasma membrane, however,
and it appears possible that their contents
could be released into the intercellular
space between the neurite and the Merkel
cell, initiating a neural response.
The function of the Merkel cell complex
has not been completely resolved, but the
recent study by Iggo and Muir ('69) has
shed considerable light on this long-standing problem. The composite structure has
long been regarded as a mechanoreceptor
related to a sensitive tactile sense. Iggo and
Muir ('69), working with the touch corpuscle on the thigh of the cat that is frequently located close to the base of the
guard hairs, have shown that the tactile
cells (Merkel cells) are rapidly firing,
slowly adapting cutaneous mechanoreceptors, generating > 1000 impulses/sec. Although the corpuscle is capable of functioning independently of the guard hair
or surrounding hair, its proximity to the
base of the guard hair would appear to project its sensitivity to some distance from
the surface of the skin.
The Merkel complex associated with
vibrissae forms a ring around the shaft,
in the outer root sheath at the level of the
upper half of the ring sinus. Deflection of
the vibrissae would cause compression of
the tissue in the direction of the deflection,
thus giving directional significance to the
stimulus. Iggo and Muir ('69) found that
an afferent discharge was evoked by displacement of 1-5 pm. Thus the Merkel
cell complex is very sensitive to vertical
compression. In the vibrissae, it would
appear that two features could significantly
enhance the sensitivity of these structures.
The shaft of the vibrissa would act as a
lever increasing the force exerted on the
receptors, and engorgement of the erectile
tissue, especially the ring sinus, would increase the resistance of the tissue underlying the touch receptors, making them more
sensitive to compression. These features
appear to combine to make the vibrissa a
very efficient and sensitive directional
touch receptor, but the physical limitations
of this system have yet to be determined.
Of particular interest also are the complex neural terminations on the external
surface of the glassy membrane. Andres
('66) describes three different configurations for these endings: straight, branched
and circular; however, in spite of the different size, shape and position, they
showed the same patterns of structure. Although considerable variation was also
noted in the configuration of these terminals in the sea lion, their ultrastructural
details appeared to be identical Andres
('66) considered the terminal supportive
cell to be a specialized Schwann cell, and
this is certainly a possibility. In the present
study, however, it is shown that the nucleus of the specialized cell is often located
at some distance from the neurite and
sends a unipolar extension of cytoplasm
toward the terminal portion of the neurite,
covering it on two sides. It appears likely
that the neural response is initiated in this
complex terminal area either by the fingerlike processes that protrude from the neurite into the surrounding connective tissue
or by the unipolar cell that is in close contact with the nonmyelinated terminus.
Because of the proximity of this receptor
to the glassy membrane and its unique
relationship to it, one is led to speculate
that movement of the membrane is in some
INNERVATION OF SEA LION VIBRISSAE
427
1863 Handbuch der Gewebelehre des
Menschen, 4th edition. Verl. V. Wilhelm Engelmann, Leipsig.
Ling, T. K. 1966 Skin and hair of the S. elephant seal, Mirounga leonina (lh.
I.)
The
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facial vibrissae. Australian J. Zool., 14: 855865.
Loewenstein, W. R. 1961 On the specificity of
a sensory receptor. J. Neurophysiol., 24: 150158.
Lyne, A. G., and D. E. Hollis 1971 Merkel cells
in sheep epidermis during fetal development.
J. Ultrastruct. Res., 34: 464472.
Melaragno, H.P., and W. Montagna 1953 The
tactile hair follicles in the mouse. Anat. Record,
115: 129-147.
Merkel, F. 1875 Tastzellen und Tastkorperchen
bei den Hausthieren und beim Menschen. Arch.
Micr. Anat., 11: 636-652.
1880 Ober die Endigungen der sensiblen Nerven in der Haut der Wirbeithiere.
H. Schmidt, Rostock.
Messenger, J. F. 1900 The vibrissae of certain
mammals. J. Comp. Neur., 10: 399402.
Patrizi, G.,and B. L. Munger 1966 The ultrastructure and innervation of rat vibrissae.
J. Comp. Neur., 126: 423436.
Poulter, T. C. 1963a Sonar signals of the sea
lion. Science, 139: 753-755.
19631, The sonar of the sea lion. Transactions in Ultrasonic Eng. IEEE. UE-10: 109111.
Szymonowicz, W.L. 1930 Die Innervation der
Sinushaare des Seehundes (Phoca vitulina).
Bull. Internat. Acad. Polanaise Sci. et Lettr. C1.
ACKNOWLEDGMENTS
Sci. Math. et Nat. Ser. B. Sci. Nat. (11) Zool.,
(5/6):371-390.
The authors wish to express their ap1936 Vergleichende Untersuchungen
preciation to Dr. Richard C. Hubbard for
iiber die Innervation der Sinushaare bei den
performing the surgery required to obtain
Saugern. 2.Anat. Entwicklungsgeschichte, 105:
the tissue and to Mr. Ronald Moore for his
459490.
Talbot, W. H., I. Darian-Smith, 1%.H. Kornhuber
artistic work in figures 1 and 3.
and V. B. Mountcastle 1968 The sense of
flutter-vibration: comparison of the human
LITERATURE CITED
capacity with response patterns of mechanoAndres, K. H. 1966 Uber die Feinstruktur der
receptive afferents from the monkey hand.
Rezeptoren an Sinushaaren. 2.Zellforsch., 75:
J. Neurophysiol., 31: 301334,
339-365.
Vincent, S. B. 1913 The tactile hair of the
Cauna, N. 1959 The mode of termination of
white rat. J. Comp. Neur., 23 (1): 1-36.
the sensory nerves and its significance. J. Comp. Werner, G.,and V. B. Mountcastle 1965 Neural
Neur., 113: 169-209.
activity in mechanoreceptive cutaneous afferHaller, A. von 1766 First Lines of Physiology
ents: stimulus-response relations, Weber func(Edinburgh Translation).
tions, and information transmission. J. Neurophysiol., 28: 359-397.
Iggo, A., and A. R. Muir 1969 The structure
and function of a slowly adapting touch cor- Wrobel, K. H. 1965 Structure and significance
puscle in hairy skin. J. Physiol., 200: 763-796.
of the blood sinus in the vibrissae of Tupia
glis (tree shrew). Zentr. Veterinaermed., 12:
Kadanoff, D. 1928 Uber Intraepithelialen Ner888-899.
ven und ihre Endingungen bein Menschen und
bei den Saugetieren. 2. Zellforsch., I : 553-576. Zucker, E., and W. I. Welker 1969 Coding of
somatic sensory input by vibrissae neurons in
Kolliker, A. 1852 Ober den Bau der Cutispapilthe rat trigemind ganglion. Brain Research,
len und der sogenannten Tastkorperchen.
12: 138-156.
R. Wagner's 2. Wiss. Zool., 4: 43-52.
way responsible for the initiation of the
neural response. Therefore, this receptor
is also regarded as a mechanoreceptor, responsive to vibrations or movement in the
vibrissae.
To date we have not located the endings
of the amyelinated neurites that accompany the large myelinated fibers as they
course through the tissue in small bundles.
In the sea lion they accompany the large
neurites that terminate in the sinus region
as well as those that terminate in close
apposition to the glassy membrane and
Merkel cells. We are currently attempting
to locate their termini. Andres ('66), who
studied the rat, rabbit and cat, found the
amyelinated nerve present only in the rat
in the inner conical body.
It must be admitted that the innervation
of the sinus hairs in general is impressive
and that the information that they must be
capable of receiving is both diverse and
complex. In this context, then, it appears
reasonable to suggest at this time that
sonar reception by these structures is a
possibility that should be thoroughly investigated.
PLATE 1
EXPLANATION OF FIGURES
1 This semidiagrammatic drawing of the bulbous structure at the base of a vibrissa
shows the gross relationship of various structures. The ringwulst (RW), depicted
in three dimensions, encircles the shaft (S) of the vibrissa. The thin portion of
the ringwulst faces toward the nose of the animal. The ring sinus (RS) in which
the ringwulst is located also completely surrounds the shaft. Cavernous tissue (CT)
is located both above and below the ring sinus between the shaft and the outer
dense connective tissue capsule (CTC). Several large bundles of nerves (N)
enter through the base of the capsule and divide; they then course through the
connective tissue trabeculae of the sinus tissue below the ring sinus. Some
terminate in close association with the sinuses and others continue beneath the
ringwulst and terminate in close association with the glassy membrane (GM)
or specialized cells i n the outer root sheath (ORS).
2
This midlongitudinal section of the bulb structure can be compared with the
drawings. Note the heavy connective tissue capsule (CTC), large ring sinus
(RS), ringwulst that is much larger on one side of the shaft ( S ) than it is on
the other, and the cavernous tissue (CT) both above and below the ring sinus.
The hard central portion of the shaft has been removed to prevent severe tearing
of the tissue while sectioning. The main supply of both nerves and blood vessels
enters the follicle from its base. The invogination of the base d the capsule
shown here is an artifact of preparation. Hematoxylin and eosin. X 6.
3 Artistic license has been taken in this diagram in order to concentrate information. The main distortion is that the length of cavernous tissue shown is greatly
reduced, shifting the ring sinus abnormally toward the base of the shaft. The
venous sinuses (VS) both above and below the ring sinus (RS) are confluent with
the ring sinus. The ringwulst (RW) protrudes into the ring sinus from the side
toward the shaft (S). A slight protrusion is observed on the shaft at the level
of the ringwulst, and the glassy membrane ( G M ) is thickest at this point (see
also fig. 10). The rich nerve supply ( N ) divides immediately after entering the
base of the capsule, and some nerves terminate in close association with the
venous sinuses while others continue beneath the ringwulst to terminate close
to the glassy membrane.
428
INNERVATION OF SEA LION VIBFUSSAE
R. J. Stephens, I. J. Beebe and T. C. Poulter
PLATE 1
429
PLATE 2
EXPLANATION OF FIGURES
4
This cross-section at the lower end of the bulb shows the densestaining capsule coursing through the center of the photograph
from top to bottom. Striated muscle (SM) is seen to the left of this
structure. Cross-sections of several large nerve bundles ( N ) are
present at this level, and the glassy membrane (GM) surrounds
the outer root sheath. x 55.
5
A small portion of a cross-section of the bulb just below the ring
sinus. The outer connective tissue capsule has been removed to
allow better fixation. Numerous large venous sinuses ( V S ) are
observed in the cavernous tissue, and connective tissue trabeculae
run from the glassy membrane toward the capsule. Several smaller
nerve bundles ( N ) are also present. x 125.
6-7
430
Single sensory fiber ( N ) can be observed in the connective tissue
trabeculae of the cavernous tissue; such fibers, surrounded by a
thin sheet of connective tissue, may pr itrude into the sinuses (fie.
7). These neurons are large and possess a prominent myelin sheath.
X 555. x 1,250.
MNERVATION OF SEA LION VIBRISSAE
I. J. Beebe and T. C. Poulter
PLATE 2
R. J. Stephens,
431
PLATE 3
EXPLANATION OF FIGURES
8-9
Single fibers like those shown in figures 6 and 7 terminate in a s m d expanded
structure containing a large central cell (fig. 9). The central cell is surrounded
by two or three layers of squamous cells that are separated by spaces apparently
filled with fluid. A thin wall separates this structure from the venous sinuses
( V S ) . ~1,250.x 1,250.
10 A longitudinal section of a vibrissa at the level of the ringwulst (RW). Nerves
( N ) czn be seen in the base of the ringwulst. There is a slight protuberance
from the shaft of the vibrissae under the ringwulst, and the glassy membrane ( G M ) is thickest at this point. Note that the stratified squamous cells of
the outer root sheath continue u p to the glassy membrane below the protuberance, but an additional layer of more lightly staining cells appears immediately
beneath the glassy membranes a t the level of the protuberance and continues
to be present at higher levels (see also fig. 11). The light area to the right of
the photograph results from the removal of the hard part of the shaft of the
vibrissa. x 125.
11
A cross-section of the vibrissa at the level of the ringwulst (RW). Note the
small bundles of nerves ( N ) in the base of the ringwulst and the heavy glassy
membrane (GM). A layer of lighter-staining cells appears beneath the glassy
membrane. The glassy membrane is thick and irregular on its inner surface at
this level, but becomes thinner and smoother a t higher levels (see fig. 13). x 125.
12 The fine collagen fibrils in the ringwulst ;are attach-d by tufts ( T ) to the glassy
membrane (GM) and radiate outward toward the ring sinus (see fig. 11). The
thick glassy membrane is very irregular on the inner surface. x 1,250.
13 This cross-section of the vibrissa is taken just above the ringwulst. The left half
of the micrograph is occupied by the ring sinus (RS). A small portion of the
outer capsule is seen a t the lower left. A few bundles of nerves ( N ) appear
at the upper right of the micrograph, but most of the sensory fibers that were
in small bundles at the level of the ringwulst (see fig. 11) are now distributed
in a layer outside the glassy membrane (GM). The glassy membrane is thinner
and more uniform along the inner surface. x 125.
432
INNERVATION OF SEA LION VIBRISSAE
R. J. Stephens, I. J. Beebe and T. C. Poulter
PLATE 3
433
PLATE 4
EXPLANATION 0 1 7 FIGURES
14 A higher magnification of the neural elements outside the glassy membrane. Note
the larger peripheral fibers ( N ) with prominent myelin sheaths. Tufts ( T ) inserting on the glassy membrane (GM) do not possess central structural elements as
do those in figure 16. x 1,250.
15 Analysis of serial sections has shown that the three portions of the sensory
fiber indicated by the arrows are confluent in this cross-section of the vibrissae at
a level slightly higher than in figure 14. The configuration shown here and in
figure 16 represents the terminus of many of the large myelinated fibers. Note
the specialized cell (SC) with a round nucleus toward the bottom of the micrograph. A single extension runs from the body of this cell to the terminus of the
myelinated fiber ( N ) just outside the glassy membrane (GM). When the extension of the specialized cell reaches the sensory fiber, it forms a sheath along two
sides of the unmyelinated terminus. Fine collagen fibrils extend outward from
the body of the unipolar cell as well as from the terminus itself. x 1,250.
16 The terminal structures described in cross-section in figure 15 are shown here
as they appear when a longitudinal section is examined. The dark central core
(arrow) of the tufts inserting on the glassy membrane (GM) is continuous with
large myelinated fibers, and the lighter areas along the side of the central core
are continuous with the specialized cells. Figures 23 and 24 arc electron micrographs of this area. x 1,250.
17
In addition to sensory fibers that terminate on the external surface of the glassy
membrane, some large peripheral processes also penetrate the glassy membrane
(GM). Here two such nerves ( N ) are seen very close to the glassy membrane.
The one to the left has partially penetrated the membrane. x 555.
18 An additional example of a large myelinated fiber ( N ) approaching the glassy
membrane (GM); the modifications in the membrane itself indicate that the
neuron will penetrate it. The nucleus of an endothelial cell is observed to the
right of the nerve a t the glassy membrane. See also figure 20. X 1,250.
434
INNERVATION OF SEA LION VIBRISSAE
PLATE 4
R. J. Stephens, I. J. Beebe and T. C. Poulter
435
PLATE 5
EXPLANATION OF WGURES
19 The blood vessel (BV) entering from the top of this micrograph is
directly confluent with the ring sinus just above the ringwulst. A
nerve ( N ) is shown penetrating the glassy membrane (GM) a t the
lower part of the photomicrograph. The vacuoles a t the end of the
nerve are thought to be an artifact of fixation or preparation. x 1,250.
436
20
This micrograph is an excellent demonstration of a large sensory
fiber ( N ) fully penetrating the glassy membrane (GM) and branching immediately. The branches continue for some distance on the
inner side of the glassy membrane and come into contact with
specialized cells known as Merkel cells ( M) . Stratified squamous
cells ‘are present at the extreme right. Note the capillary ( C ) in
juxtaposition to the neurite at the point of penetration of the glassy
membrane. x 1,250.
21
This electron micrograph, at low magnification, is of the cells in
the outer root sheath a t the level where the fibers penetrate the
glassy membrane. Here we observe two small sensory fibers ( N ) i n
close apposition to Merkel cells ( M ) . A well-defined basement membrane-like layer (BM) demarcates the glassy membrane (GM) from
the outer rooth sheath, but the outer surface of the glassy membrane
is less definite (see figs. 23, 24). Note the large intercellular space
(I CS ) between the nerve and one of the cells of the outer ront
sheath. x 8,000.
INNERVATION OF SEA LION VIBRISSAE
R. J. Stephens, I. J. Beebe and T. C. Poulter
PLATE 5
437
PLATE 6
EXPLANATION O F FIGURES
438
22
A section of the nerve-Merkel cell complex at higher magnification.
The dense granules in the Merkel cell are surrounded by a single
membrane and are often seen close to the plasma membrane.
Although we have not obtained conclusive evidence of their release
from the cell, there is strong suggestive evidence that they are
released. Numerous mitochondria are present in this portion of the
nerve. x 19,200.
23
This electron micrograph is of the neural complex that terminates
on the external surface of the glassy membrane (GM). The neurite
( N ) is partially surrounded by the cytoplasmic extension from the
specialized cell (SC) at the upper left. The length of the cytoplasmic
extension from the cell shown here is much shorter than that shown
a t the light microscope level in figure 15. Characteristics of this
cell include a round-to-oval nucleus, a paucity of rough endoplasmic
reticulum (ER) and a sparse population of small mitoc::ondria. A
fine fibrillar material occupies much of the cytoplasmic extension
and portions surrounding the nerve. The moderately electron-dense
material surrounding the terminus (double arrows) is continuous
with the glassy membrane and finger-like extensions (arrows) protrude from the terminus into the surrounding connective tissue.
x 12,000.
INNERVATION OF SEA LION VIBRISSAE
R. J. Stephens, I. J. Beebe and T. C. Poulter
PLATE 6
439
PLATE 7
EXPLANATlON OF FIGURE
24
440
Finger-like extensions (arrows) are seen along the terminal portion
of the complex, extending into the connective tissue from the narrow
sides of the terminus, not covered by cytoplasm of the specialized
cell (SC). Numerous small vessels and mitochondria are present
within the neurite ( N ) , and marked pinocytotic activity is observed
along the plasma membrane of the specialized cell. This micrograph
shows this activity particularly we11 along the plasma membrane
facing the nerve, but pinocytosis is also pronounced on the portion
of the plasma membrane away from the nerve. The glassy membrane ( G M ) is to the lower left. x 25,500.
INNERVATION OF SEA LION VIBRISSAE
R. J. Stephens, I. J. Beebe and T. C. Poulter
PLATE 7
441
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