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The sensory innervation of the rat rhinarium.

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THE ANATOMICAL RECORD 214:210-225 (1986)
The Sensory Innervation of the Rat Rhinarium
RICHARD T. SILVERMAN, BRYCE L. MUNGER, AND ZDENEK HALATA
Departments of Anatomy, The Milton S. Hershey Medical Center, The Pennsylvania State
University, Hershey, Pennsylvania 17033 and Anatomisches Znstitut der Universitat
Hamburg, Abteilung fur Funktionelle Anatomie, 0-2000 Hamburg 20
Federal Republic of Germany
ABSTRACT
The present study documents the characteristics of innervation of
the rhinarium or hairless rat snout skin by light and electron microscopy. The outer
glabrous surface is covered with a stratified squamous epithelium that forms both
rete pegs and rete ridges, the latter on the inferior border near the philtrum. The
glabrous skin contains numerous presumptive epidermal and dermal free nerve
endings (FNE’s), Merkel terminals at the base of the rete ridges and pegs, and
simple, nonencapsulated corpuscles. A second region of dense innervation, found on
an elevation of the inner wall of the vestibule, contains similar components of
innervation, with the exception that no Merkel terminals were identified. Since no
Merkel terminals were present in this area of the vestibule, intraepidermal as well
as dermal FNE’s could be identified with certainty. This skin is covered by a thin
squamous epithelium overlying dense connective tissue. The simple corpuscles are
similar to those in the rhinarium, as well as resembling those described in other
species. FNE’s were frequently observed intimately associated with simple corpuscles. Several examples of large FNE’s with two to three layers of cytoplasmic
lamellae were found, suggestive of transitional forms between FNE’s and simple
corpuscles.
Thus, the pattern of sensory innervation in the glabrous rat snout skin is similar
to that found in other furred species described to date, but in addition, the sensory
innervation of ridged skin in the rat also resembles that of epidermis organized into
rete pegs. This dense sensory innervation may be correlated with whisking behavior
of the predominately nocturnal rat.
The snout of most furred animals is highly innervated
with sensory nerve endings. The mystacial pad (or whisker pad, mystak in Doric Greek is moustache) contains
sinus hairs, each associated with a variety of sensory
receptors (Tretjakoff, 1911; Andres, 1966; Gottschaldt et
al., 1973; Halata and Munger, 1980; Renehan and Munger, 1986a,b). The glabrous skin of the snout, properly
referred to as the rhinarium, is also usually highly innervated in a species-specific manner. The sensory receptors described to date in glabrous skin include
intraepidermal and dermal free nerve endings, Merkel
terminals, and various corpuscular receptors including
simple, Meissner, Pacinian, and Ruffini corpuscles
(Munger, 1965; Halata, 1975). Species studied to date in
the ongoing collaborative studies in the authors’ laboratories include the cat (Halata, 1970), mole (Halata,
1972a,b), opossum (Munger, 19651, rhesus monkey (Halata and Munger, 1980),bandicoot (Loo and Halata, 19861,
and raccoon (Munger et al., 1971; Munger and Pubols,
1972). Several of these studies have documented differences between hairy and glabrous skin. The sensory
innervation of the rat rhinarial skin has not been described, yet one would expect to find this region richly
innervated because of the relative dependence of the rat
on tactile sensory perception secondary to decreased visual acuity and nocturnal behavior as part of what is
0 1986 ALAN R. LISS, INC
referred to as “whisking” behavior (Welker, 1964). The
present study was designed as a baseline for subsequent
studies of degeneration and regeneration, especially of
free nerve endings and simple corpuscles, and describes
the variety and distribution of sensory terminals in normal rat rhinarial skin. Our findings show a pattern of
innervation in some ways similar, but in other ways
different from other animals described to date, especially in terms of the distribution of free nerve endings.
MATERIALS AND METHODS
Albino rats were anesthetized with Nembutal (360
m g k g of body weight) and perfused with 6% glutaraldehyde solution buffered with 0.05 M phosphate buffer
with a pH of 7.2. Following perfusion, the snout skin
with its underlying muscle and cartilage was removed,
cut into smaller cubes, and postfixed in 1%osmium
tetroxide in 0.1 M phosphate buffer with 1%sucrose.
The tissue was then dehydrated in increasing concentrations of alcohol and embedded in Epon 812 (Luft, 1961).
Semithin sections were cut and stained for light microscopy employing a technique modified from that described by It0 and Winchester (1963) with three parts of
1% Toluidine blue in 1% borax to two parts 1%pyronin.
Received April 18, 1985; accepted August 25,1985.
211
RAT SNOUT SKIN INNERVATION
Thin sections were mounted on copper grids and stained
with uranyl acetate (20 min) and lead citrate (5 min) for
electron microscopic examination in a Philips 300 electron microscope. In addition, a n entire snout, prepared
according to this protocol, was serially semithin sectioned and stained employing the modified It0 and Winchester technique described above.
In a second protocol, rats were anesthetized with Nembutal (50 mgikg), perfused in the manner described by
Forssmann (1976), and fixed with a 2% paraformaldehyde 2% glutaraldehyde solution. The material was then
postfixed in 10% neutral buffered formalin and embedded in paraffin. The tissue was then serially sectioned
at 6-8 pm and stained with a modified ammoniacal
silver technique (Sevier and Munger, 1965) for light
microscopy. For photomicrography of silver-stained sections we used Kodak Technical Pan film developed with
POTA developer as described in Kodak Technical Data
Sheet #P-255. The procedures to be followed for processing must be followed very carefully. When done correctly the negatives result in considerable contrast
enhancement of blackened (silver-positive) objects such
as axons. The final negative can be magnified considerably without encountering grain permitting photography a t lower magnification and lower N.A., yet with
greater depth of the focus in the specimen (Rice et al.,
and Rice and Munger, 1986).
Fig.?.This photograph of a rat snout shows the regions described by
the light and electron micrographs that follow. The area referred to as
the rhinarium or planum nasale is designated by the asterisk (*), and
RESULTS
Two regions of glabrous skin can be identified in the
rat snout by light microscopy. The outer surface, the
rhinarium or planum nasale (Fig. l), is similar to the
glabrous skin of other animals that have been investigated, and it is characterized by free nerve (FNE’s),
Merkel terminals, and simple, nonencapsulated corpuscles as defined by Halata and Munger (1983).The second
densely innervated region is a small elevation found on
the inner wall of the vestibule (vestibulum nasi) (Fig. 11,
that is characterized by a thin epithelium consisting of
four to six layers of squamous cells. This region has a
dense sensory innervation containing a variety of FNE’s
and scattered corpuscular endings, but no Merkel terminals.
Rhinarium
The rhinarium of the rat is covered with a stratified
squamous epithelium that forms both rete pegs and rete
ridges, apparent by light microscopy. The greatest part
of the snout (Fig. 1)is characterized by pegged skin (Fig.
21, which is more typical of glabrous snout skin described in other species (Munger, 1965; Halata, 1975).
On the most ventral portion of the snout, just above the
philtrum, however, the epidermis is organized into rete
ridges (Figs. 3,4), much like primate digital glabrous
skin. The entire rhinarium is densely innervated based
the prominent bulge into the vestibulum nasi is indicated by the white
arrow. X 12.8.
2 12
R.T. SILVERMAN, B.L. MUNGER, AND Z. HALATA
Fig. 2. These light micrographs represent typical areas of the rhinarium as visualized in silver-stained paraffin sections. The areas of the
boxes in 2a are illustrated at higher magnification in 2b (representing
the boxed area to the right) and 2d is the box to the left. The epidermis
is relatively thick, consisting of many layers of stratified squamous
epithelium. The underlying dermis contains densely packed collagen
fibers, and a superficial loose reticular dermis is not present. The
intraepithelial F N E s in the boxes can be seen to better advantage in
2b and 2d. 2c has a presumptive Merkel terminal within the circle,
and numerous intraepithelial FNE’s indicated by the arrows. Since
the intraepithelial F N E s are derived from axons high in the dermal
papillae, they are probably not axons from Merkel terminals that are
typically present in the basal portions of the rete ridges and rete pegs.
These intraepithelial FNE’s in some cases ascend to the stratum corneum, and the examples of 2b and 2c are near the limits of resolution
of the light microscope. Other axons can be seen that terminate near
the epidermal-dermal junction and can only be presumptively identified as dermal FNE’s (compare with Figs. 5,7, and 8). 2a x 100 2b-2d,
x400.
on our evaluation of silver-stained paraffin sections (Fig.
2). Small bundles of nerve fibers course in the superficial
dermis and contain numerous small diameter myelinated (presumptive A delta) and unmyelinated fibers.
The latter can be identified on the basis of the presence
of numerous fine axons in a single Schwann cell as
described by Richardson (1960). The epidermis is also
heavily innervated. Some axons branch in the region of
the dermoepidermal junction and terminate in the midst
of the basal cells of the eDidermis as DresumDtive Mer-
kel terminals (Fig. 4).Other axons ascend in the epidermis and course towards the stratum corneum. These
axons are presumptively identified as intraepidermal
FNE’s (Fig. 4).Some axons appear to end blindly in the
connective tissue as dermal FNE’s or simple corpuscles
surrounded by lamellar cells as noted subsequently in
electron micrographs.
By electron microscopy, Merkel nerve endings are
found throughout the rhinarium, where they are located
a t the base of the rete pegs or epidermal ridges (Figs. 2,
Fig. 3. This tangential section through the ventral portion of the
planum nasale illustrates epidermal ridges resembling primate digital
glabrous skin. This shows nerve bundles deeper in the dermis branch
as they proceed superficially to supply sensory terminals higher in the
ridges. The dermal papillae between the rete ridges are narrower in
this area of the rhinarium as compared to the areas with rete pegs
where the dermal papillae are broader, as in the center of Figure 2a or
in this figure to the upper left. x 100.
Fig. 4. This photomicrograph was taken from a cross-sectionthrough
the ventral portion of the planum nasale showing the epidermal ridges
illustrated in Figure 3 in tangential section. The stratum corneum in
this section differs from that in Figure 2, which represents epidermis
organized into rete pegs, in that here the ridges are reflected on the
surface (arrowheads). Afferent nerve bundles proceed through the dermis and branch to supply sensory receptors in each of the ridges and
their associated dermal papillae. A presumptive Merkel terminal similar to that of Figure 2c is indicated by the circle, and scattered profiles
of intraepithelial FNE’s are indicated by the arrows to the right. X200.
214
R.T. SILVERMAN, B.L. MUNGER, AND Z. HALATA
4-6). Groups of approximately three to five Merkel cells
and associated axons have the same structure as Merkel
terminals in Tastscheiben or touch discs of other animals. The Merkel cells (Fig. 6 ) exhibit a lobulated nucleus and contain numerous electron opaque granules
polarized toward the associated nerve disc, which contains mitochondria, vesicles, neurotubules, and neurofilaments.
The identification of FNE’s in the rhinarial skin is
presumptive as noted in Figure 7 in the absence of serial
section reconstructions. However, we can be more confident of the identification of FNE’s high in dermal papillae (Fig. 8) as Merkel cells were only present a t the
base of rete ridges and rete pegs. In those areas, we also
could identify presumptive FNE’s, but the possibility for
confusing a FNE terminal with a Merkel terminal was
a constant problem. High in the dermal papillae as in
Fig. 8 we encountered numerous examples of FNE’s of
C fibers that fulfilled the criteria established by Cauna
(1973, 1980) in serial section reconstructions from hairy
and glabrous skin. Other dermal papillae contained
FNE’s resembling those described by Kruger et al.,
(1981) as the polymodal nociceptor FNE’s of small diameter myelinated A delta fibers. In both cases, axonal
varicosities contained vesicular material and scant neurofilaments or neurotubules, and the axon frequently
directly abutted the basal lamina. In some cases the
Schwann cell and associated axons established a n intimate contact with the contiguous basal lamina of the
epidermis (Figs. 7,8). The FNE terminals of A delta
fibers tended to have a 1:l ratio of axon profile to enveloping Schwann cell as noted by Kruger et al., (1981)and
illustrated in Figure 8a. In all other aspects the FNE’s
of A delta fibers were similar to those of C fibers.
Axons were also identified within the epidermis as
presumptive intraepidermal FNE’s (Fig. 7). In this skin,
absolute identification of intraepidermal FNE’s is only
presumptive as they could be axons derived from Merkel
terminals (compare Munger, 1965; with Halata, 1975).
In some cases, the Schwann cell forms one or two layers
of thin cytoplasmic lamellae around the nerve terminal
(Figs. 7,8a). The cytoplasmic lamellae contain numerous
pinocytotic vesicles. The nerve endings lie under the
dermal rete pegs or ridges, as well as high in the dermal
papillae (Fig. 8).
The simple nonencapsulated corpuscles (Figs. 5,9) that
are present in this region are similar in structure to the
simple corpuscles (Krause end bulbs) described in other
species (Munger and Pubols, 1972; Halata, 1975; Halata
and Munger, 1983),but they are quite small in diameter,
measuring approximately 10 pm. The length of the corpuscle is variable, some measuring up to 100 pm. The
corpuscles (Fig. 9) consist of an axon with a terminal
swelling surrounded by cytoplasmic lamellae formed by
modified Schwann cells or by lamellar cells of the inner
core. An incomplete perineural capsule is present. The
corpuscles are located close to the stratum basale, partially under the rete pegs and ridges of the epidermis,
but also high in the dermal papillae. The axons are
generally oriented perpendicular to the surface of the
skin, and they display balloon-shaped terminal swellings. The axons as well as the terminal axon swelling
can extend projections of various lengths between the
lamellae of the inner core. These lamellae are covered
by a thin basal lamina, and collagen fibers are found
between lamellae. In addition, the lamellae contain numerous pinocytotic vesicles. In a few cases, the inner
core branches as many a s three times conforming to the
shape of the dermal papilla. The afferent nerve fiber is
myelinated and has a diameter of 2-3 pm. The nerve
fiber may divide at the first mode of Ranvier, and each
branch can continue on into a corpuscle as observed in
serial paraffin sections. The nerve terminals and axons
show the same features as noted above. The number of
corpuscles is greater in the ale nasi than in the transition zone to hairy skin in the dorsum nasi. In some cases
axons resembling corpuscular terminals in size had scant
lamellae, thus resembling free nerve endings (Fig. 7).
Vestibular ridges
The densely innervated ridge with its characteristic
thin epithelium found on the inner wall of the vestibule
(Figs. 10-12) was described briefly above. This region
contains the same components of sensory innervation as
the rhinarium with the exception of Merkel terminals,
which are not present in this region. Free nerve endings,
however, are present in abundance, including dermal as
well as intraepithelial FNE’s, supplied by C-fibers as
well as delta A-fibers (Fig. 11).Numerous intraepithelial
FNE’s are identified by electron microscopy in this region, and these lie in the stratum basale and the stratum spinosum (Fig. 12). The terminals are balloonshaped, containing the typical features of nerve endings.
FNE’s of C-fibers and A-delta fibers are identical in
appearance with those described above, as are the simple corpuscles, usually found just beneath the stratum
basale (Fig. 12). In addition to the thin epithelium and
the absence of Merkel cells, other notable differences
include more densely packed bundles of collagen and
greater vascularity of the vestibular ridge.
DISCUSSION
The present study documents the presence of a dense
sensory innervation in the glabrous skin of the rat snout
or rhinarium, as well as the presence of a highly innervated ridge protruding into the nasal vestibule. The
variety of sensory receptors in these two regions is similar, with differences in the pattern of these endings and
distribution of Merkel terminals. Both areas contain
numerous FNE’s, and the absence of Merkel terminals
in the nasal vestibule removes the possible confusion of
identifying intraepithelial FNE’s as contrasted to Merkel terminals. These presumptive polymodal nociceptors
have only recently been conclusively identified by electron microscopy by Kruger et al., (1981) and confirmed
by Munger and Halata (1983).
The nature of free nerve endings has been unclear
since their existence was first suggested by light microscopic evidence (see Munger, 1971; and Halata, 1975, for
review). With the use of the electron microscope, these
sensory receptors have been more completely examined
and better characterized (Cauna, 1973, 1980). Recent
authors have ventured to classify them as unassociated
with any specialized epithelial receptor cells in contrast
to axons associated with Merkel cells (Halata and Munger, 1983). Munger (1965) described the latter type of
intraepidermal FNE’s in the opossum, in which the axon
continued from the Merkel-neurite complex and proceeded through the stratum spinosum without regard to
cellular boundaries. Halata later described FNE’s in
RAT SNOUT SKIN INNERVATION
Fig. 5. This survey electron micrograph was taken from a section cut
tangentially through the rete pegs of the rhinarium and has cut
through the base of several rete pegs to the upper left, lower left, and
lower right. The area in the center is a dermal papiIla containing
capillaries, numerous nerve bundles, and a simple corpuscle (S) to the
extreme upper right. A Merkel cell (M) and its associated axon (black
on white arrows) is present in the base of one rete peg to the lower left.
2 15
Numerous FNE’s are indicated by the hollow short arrows. The myelinated axons are all relatively small in diameter, the largest measuring 4 pm in diameter. Subsequent micrographs illustrate the following
features at higher magnification: Merkel terminals in Figure 6; FNE’s
in Figures 8 and 9, and see also Figure 12; a simple corpuscle in Figure
9. ~2,430.
Fig. 6. A typical Merkel terminal is illustrated in this electron abuts a Merkel cell W)that contains numerous electron opaque granmicrograph from an area similar to the Merkel terminal in Figure 5. ules polarized toward the axon. The identity of the cell is verified by
This fortuitous plane of section depicts the axon and associated the presence of desmosomes (circle) and stubby cytoplasmic spikes
Schwann cell (right-hand arrow) prior to entering the epidermis. The ( S t a s ) that penetrate between contiguous epidermal keratinwytes.
expanded axon terminal or disc (arrow to the left) is cup-shaped and X 11,500.
thus curved in profile in this micrograph. The axon terminal closely
RAT SNOUT SKIN INNERVATION
Fig. 7. This electron micrograph was taken from a section at the
midpoint of a dermal papilla and thus removed from any Merkel
terminals. The intraepidermal axon (A) to the right is identified as an
FNE. The cluster of small axons to the left (stars) in a single Schwann
cell are most likely FNE’s of C fibers. The other axons in the dermis
are also considered to be FNE’s, with numerous areas indicated by the
2 17
hollow short arrow where the Schwann cell investment is deficient
and the axon directly abuts the basal lamina. To the upper left, the
black on white arrow indicates the point of fusion of basal lamina of
an axon and its associated Schwann cell with the basal lamina of the
epidermis. Compare this micrograph with Figure 8 taken from the
upper portion of a dermal papilla. X 17,000.
2 18
R.T. SILVERMAN, B.L. MUNGER, AND Z. HALATA
Fig. 8. These two micrographs compare F N E s considered to be
terminals of delta A-fibers (a) and C-fibers (b). In 8a the axons tend to
have a 1:l ratio with Schwann cells, and have numerous areas where
the Schwann cell investment is absent and where axons directly abut
the basal lamina indicated by the hollow short arrow. The axon indicated by the upper left arrow and its associated Schwann cell directly
abut the basal lamina of the epidermis (circle). 8b is photographed at
much higher magnification, and the small bundle of axons in a single
Schwann cell are typical small diameter C-fibers. These axon profiles
are less than half the size of those in 8. Areas of direct contiguity of
axon and basal lamina like that indicated by the hollow are a common
feature. At the circle a strand of filamenous material extends from the
basal lamina of the Schwann cell to the basal lamina of the epidermis.
8a, ~ 8 , 0 0 0Figure
;
8b, x 17,000.
220
R.T. SILVERMAN, B.L. MUNGER, AND Z. HALATA
association with the Eimer organ in the mole, indicating, however, that they were present in a quantity five
times greater than Merkel cells, thus concluding that
not all axons could terminate on a Merkel cell. In these
studies, epithelial cells were observed to invest axonal
endings in the epidermis in the same manner as the
Schwann cell invests axons in the dermis. Loo and Kanagasuntheram (1972) also described intraepidermal
nerve endings in the snout of the tree shrew, specifying
a double membrane surrounding the terminal as evidence of the extracytoplasmic location of the endings,
verifying Munger’s previous conclusion (1965). In addition, they noted mitochondria1 degeneration, which they
attributed to the constant shedding of the superficial
epidermal layers. On the other hand, Loo and Halata
(1986) described intraepidermal nerve terminals in the
long-nosed bandicoot, stating that healthy looking mitochondria were present. While we could not be certain
of the presence of intraepidermal FNE’s that were not
associated with Merkel cells on the outer surface of the
rat snout in the absence of serial section reconstructions,
we are compelled to acknowledge their existence based
on light microscopic evidence in silver-stained sections.
In addition, when one considers the relative paucity of
Merkel cells in comparison to the abundant free nerve
endings, we conclude that most axons not associated
with Merkel cell are most likely intraepidermal FNE’s.
In the vestibule, one can say with certainty that intraepidermal axons that have been identified are unassociated with other epidermal receptor components, since
no Merkel cells are present in this region. These endings
are similar in character to those described above, with
double membranes delineating a n area of clear cytoplasm containing normal mitochondria, vesicles, and
occasionally neurotubules and neurofilaments. Some are
seen closely associated with corpuscular receptors (Munger and Halata, 1983; Halata and Munger, 1983). The
function of the abundance of FNE’s in the vestibule is
admittedly speculative. Similar axon terminals have
been identified as a “cold spot” by Hensel et al., (1974)
and Hensel and Iggo (1971). The FNE’s of AG-fibers
described by Kruger et al., (1981) in both physiologic
and ultrastructural terms were polymodal nociceptors.
Certainly the anatomical arrangement of the vestibular
ridge suggests a protective function for the upper airway, and both thermal as well as mechanically sensitive
axons would be expected.
Dermal free nerve endings are present in abundance
in the rhinarium as well as the vestibule. The morphology of these FNE’s has been described above, and these
endings are similar to those described in the past. Cauna
(1973), in a n electron microscopic study of C-fibers in
serial sections, assigned the descriptive term “penicillate” nerve endings to those endings that appeared as
small-caliber C-fiber axons invested by one Schwann cell
containing up to ten axons. These FNE’s of C-fibers were
supplied by a n afferent nerve that was unmyelinated.
Some of the branches of these endings coursed into close
proximity with the basement membrane of the epithelium, sometimes fusing basal membranes, and sometimes proceeding into the epidermis. Both mechanoreceptor function (Cauna, 1969) and thermoreceptor function (Iggo and Muir, 1969; Hensel, 1969; Hensel and
Iggo, 1971; Meyer and Campbell, 1981)have been attributed to dermal free nerve endings of C-fibers.
Larger free nerve endings of A-delta fibers are also
present in both regions examined, and they are supplied
by myelinated axons. Some of these FNE’s are surrounded by one or two layers of cytoplasmic lamellae
formed by Schwann cells. These endings resemble the
lanceolate terminals commonly found in hairy skin,
which have been shown to be rapidly adapting mechanoreceptors (Iggo, 1974). Alternatively, they may represent a n early stage in the development of the simple
corpuscles.
Merkel cell-neurite complexes are present only in the
rhinarium, where they are found at the base of the rete
pegs and ridges in groups of three to five cells. This
organization is similar to that found in Eimer’s organ of
the mole, but the pattern is not as regular, nor does one
find the other associated structures such as corpuscles
and FNE’s in a n organized fashion as described by Halata (1972a,b). In contrast to the opossum, mole, cat, and
pig, the number of Merkel terminals is small, and not
all epidermal ridges and rete pegs examined have Merkel cells. The Merkel cell-neurite complex has been described above and is identical in structure to those
described in other species. This receptor has been previously characterized as a type I slowly adapting mechanoreceptor (Iggo and Muir, 1969; Munger et al., 1971; Pubols et al., 1973). The significance of the presence of
Merkel cells in the outer region as opposed to the absence in the vestibule is unclear.
The corpuscular receptors found in the glabrous rat
snout skin are similar in structure to Pacinian or simple
corpuscles that have been identified in numerous other
species such as the cat, monkey, pig, snout, and mole.
As in other species, the corpuscle consists of an inner
core surrounded by a variable number of lamellae. The
corpuscles vary in size, but in general, they tend to be
small and relatively simple (like those in monkey sinus
hairs), lacking a perineural capsule in most instances.
This is consistent with the observation that more superficial corpuscles tend to lack a capsule (Munger and
Halata, 1983; Halata and Munger, 1983). Most of the
corpuscles are located high in the dermis, frequently
just under or surrounded by the epidermis (basal lamina
of the stratum basale). The corpuscles vary in shape
depending on the shape of the dermal papillae in which
they are located. Axons are observed to branch just after
the last node of Ranvier, inside the corpuscle, and form
a branched inner core with lamellae conforming to the
shape of the papilla. As many as three branches may be
present. Based on the studies of Munger et al., (1971)
and Munger and Pubols (1972) in the raccoon, these
corpuscles are probably rapidly adapting mechanoreceptors. In comparison to raccoon simple corpuscles, those
found in rat rhinarium lack a complete capsule, but the
terminal axon and associated cytoplasmic lamellae are
otherwise identical. Munger and Halata (1983) and Halata and Munger (1983) have proposed that the absence
of a capsule has no functional significance, but is instead
associated with the position in the dermis, as previously
indicated.
The present study has provided another clear example
of one association of FNE’s with corpuscular receptors.
Ide (1976) studied serial section electron micrographs
and documented the presence of intraepidermal FNE’s
associated with Meissner corpuscles of mouse digital
skin. Halata and Munger (1983)were able to find exam-
Fig. 9. A simple corpuscle is illustrated in this micrograph depicting
a portion of a corpuscle such as that in Figure 5 photographed at low
magnification. The central axon contains numerous mitochondria and
various vesicles and electron opaque inclusions. The axoplasmic spikes
(arrows) that project between the associated lamellae are a common
feature of all corpuscular receptors. The cytoplasmic lamellae have
numerous pinocytotic vesicles, and each lamella is enveloped by basal
lamina. A portion of the nucleus of a lamellar cell (L) is also in this
section. The cells to the right of the corpuscle are fibroblast-like capsular cells that partially encapsulate the receptor. The capsule is
usually not complete. In some areas, basal lamina-like material associated with these capsular cells is present, but no continuous basal
lamina is present in contrast to more heavily encapsulated receptors.
X 17.000.
222
R.T. SILVERMAN, B.L. MUNGER, AND 2. HALATA
Fig. IOa,b,c.These three light micrographs were taken from a set of
serial sections, although these sections were not contiguous. The area
illustrated is the ridge within the vestibule indicated by the arrow in
Figure 1. A very dense plexus of axons is present at the dermoepider-
ma1 junction. The underlying dermis is very vascular, and the epithelium is thin as compared with the rhinarium (see Fig. 2). Intraepithelial
FNE’s do not ascend in the epithelium as in the rhinarium proper (Fig.
ples of myelinated A&-fibersand their FNE terminals
associated with simple corpuscles in the adult monkey
lip. These dermal FNE’s associated with corpuscle may
well be functionally distinct, but since no evidence to
support this hypothesis is known to the authors, we tend
to regard them as a special type of dermal FNE.
A final minor point of interest observed in the present
study is the presence of ridged skin in a nonprimate.
Cummins (1964) noted the presence of ridged skin to be
unique for marsupials and primates. We have not been
able to confirm Cummins’ opinion that the opossum has
ridged skin (unpublished observations), but the rat
clearly does. The phylogenetic relevance of this observation must await further studies on other rodents.
The rat, as noted above, is rather dependent on the
sensory input from its snout as a result of decreased
visual acuity a s we11 as nocturnal behavior. Welker
(1964)examined the sniffing behavior of albino rats, and
found a cycle of four movements: 1)polypnea, 2) protraction and retraction of the mystacial vibrissae, 3) head
movements, and 4) movements of the tip of the nose,
including the glabrous skin described above. This behavior complex, which develops early in the rat’s life, provides the rat with the ability to find food as well as
maneuver in dimly lit surroundings. Rats that were
deprived of somatic snout afferents were handicapped in
food getting functions, and they may have showed an
overall decrease in sniffing. This may serve to show the
importance of the tactile sensation of this region, thereby
causing one to expect dense sensory innervation. In addition, the variety of structures appearing in the glabrous snout skin contributes to the sensitivity of the
region, thus analogous to the use of digital ridged glabrous skin in the reading of braille (Johnson and Phillips, 1981; Johnson and Lamb, 1981). Multiple discrete
sensory terminals of varying physiologic properties are
the peripheral basis of heightened tactile acuity associated with multiple parallel processing in hairy as well
as glabrous primate skin (Munger, 1982; Dell and Munger, 1986).
2). X200.
ACKNOWLEDGMENTS
The authors wish to acknowledge the valuable technical assistance of Debbie Hinton, Marianne Blohm, and
Tjandra Djasputra. Special thanks go to Doris Lineweaver for typing the manuscript. This study was supported in part by U.S. Public Health Service research
contracts NIDR72-2401 and HD4-2869 and research
grants HD11216 and NS 19462 to Dr. Munger, and in
part by grants from the Deutsche Forschungsgemeinschaft awarded to Dr. Halata. This study was done while
R.T.S. was a medical student and recipient of a NIH
Short-Term Research Training Award, HL07477.
RAT SNOUT SKIN INNERVATION
Fig. 11. This electron micrograph was taken from a cross-section
through an elevation of the epithelium of the nasal vestibule, as
illustrated in Figure 10. A nerve plexus in the dermis consists of
myelinated and unmyelinated fibers. A small corpuscle is also present
in rectangle depicted at higher magnification in Figure 12. Note also
223
the dense packing of the collagen fibers, characteristic of vestibule, as
compared to the more loosely-packed collagen that one finds in the
planum nasale (see Figs. 5-7). Numerous unlabeled FNE’s are present
throughout the dermis and epidermis, a few of which are illustrated at
higher magnification in Figure 12. x3,800.
Fig. 12. The area of the rectangle in Figure 11is illustrated at higher
magnification and shows a corpuscle from the vestibule, identical in
structure with that from the planum nasale seen in Figure 11. Intraepithelial F N E s are indicated by the arrows, and they are enveloped
by the cytoplasm of keratinocytes in a manner analogous to a Schwann
cell enveloping an axon. These intraepidermal FNE’s are similar to
those depicted by Ide (1976) in his serial sections of rat glabrous digital
skin where intraepithelial FNE’s associated with Meissner corpuscles
were identified. Numerous dermal F N E s labeled with asterisks are
present surrounding the small simple corpuscle (S). Some of these may
be the parent axons to the intraepidermal FNE’s. Two bundles of Cfibers are present in the lower left. A complete capsule is not present
surrounding the simple corpuscle. X 11,000.
RAT SNOUT SKIN INNERVATION
225
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