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The ultrastructure of Ruffini and Herbst corpuscles in the articular capsule of domestic pigeon.

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THE ANATOMICAL RECORD 198581-692 (1980)
The Ultrastructure of Ruffini and Herbst Corpuscles in
the Articular Capsule of Domestic Pigeon
ZDENEK HALATA AND BRYCE L. MUNGER
Anatomisches Institut der Uniuersitat Hamburg, Abteilung fur Funktionelle
Anatomie, Hamburg, Germany (Z.H.), Department of Anatomy, Pennsylvania
State University College of Medicine, Hershey, Pennsyluanin 17033 (B.L.M.)
ABSTRACT
The present study identifies two types of sensory nerve endings in
the articular capsule of the shoulder joint of domestic pigeons: Ruffni corpuscles
(spray-like endings), and Herbst corpuscles. Ruffini corpuscles occur in the fibrous
membrane of the articular capsule and consist of two to four branched cylindrical
segments within a network of fascicles of collagen fibers. At the terminal ends of
the cylinders the perineural sheaths of the capsule are deficient and surround the
fascicles of collagen fibers. The axon terminals in each cylindrical segment of a
Ruffini corpuscle repeatedly ramify, giving rise to delicate neurite profiles. These
neurites and associated Schwann cells envelope small fascicles of collagen fibrils.
Schwann cells cover only a part of the neurite profiles. The myelinated afferent
axon enters the midregion of the cylinder and has a diameter of -3 pm. Herbst
corpuscles are situated in the subsynovial connective tissue and in the transition
zone between the fibrous membrane and the muscular fascia. They appear as
elongated ovals in longitudinal section and round in cross section. Small corpuscles
measure -5 pm x 200 pm in length and large ones -100 pm x 600 pm. Each has a
myelinated afferent axon (diameter 2.5-7.5 pm) that terminates in one to three
inner cores. The inner core contains the nonmyelinated receptor portion of the
nerve fiber surrounded by numerous cytoplasmic lamellae, a subcapsular connective tissue space, and a perineurai capsule of eight to 12 layers. Avian joint
receptors are similar to those present in the skin of various birds and Ruffini
corpusclesresemble in fine structure equivalent receptors in joint corpuscles of the
domestic cat.
The sensory nerve endings of the articular
capsules are considered to be proprioceptive receptors (Schmidt, 1976).Proprioceptors in various mammals and birds were described by
PolaEek (1969), who examined many capsules
from different joints by light microscopy after
silver staining. The sensory innervation of articular capsules in birds has been described in
additional studies by PolaEek et al., (19661,and
Malinovsky and Zemanek (1970, 1971). By
light microscopy, three types of nerve endings
have been described in the articular capsules of
birds: free nerve endings, spray-like endings,
and Herbst corpuscles. According to the above
authors, it is possible to discern differences in
the structure of various receptors as well as
differences in the innervation pattern of individual joints. The wing joints of birds tend to be
more richly innervated than those of the legs.
Studies on the ultrastructure of joint receptors have been limited to mammalian species
0003-276X/80/1984-0681$02.30
@ 1980 ALAN R. LISS, INC.
(Halata, 1975, 1977; Halata and Groth, 1976).
Our knowledge of the cytology of sensory receptors is in fact frequently extrapolated from
studies on skin (Saxod, 1970; Munger, 1971;
Halata, 1975). An example of this extrapolation between skin and musculoskeletal nerve
endings is the recent description of the cytologic nature of the Ruffini corpuscle. The present authors independently have established
identical cytologic criteria for identifying Ruffini corpuscles in mammalian joints and facial
hairs (Halata, 1977 and Biemesderfer et al.,
1978). In both cases the receptor bears a striking similarity in ultrastructure to Golgi tendon
organs as described by Schoultz and Swett
(1972, 1974). These common findings from diReceived April 7, 1980; accepted June 19, 1980.
Address correspondence to: Bryce L. Munger, MD, Department of
Anatomy, Milton S. Hershey Medical Center, Hershey, Pennsylvania
17033.
ZDENEK HALATA AND BRYCE L. MUNGER
682
verse tissues might form a basis to characterize
the sensory terminals known to be variable in
the articular joint capsules ofbirds. In addition,
the major corpuscular receptor of birds, the
Herbst corpuscle, has only been studied in beak
skin (Andres, 1969; Saxod, 1970,1973;Halata,
1971; Munger, 1971).
The present study was undertaken to assess
i n ultrastructural terms the variability of
cytologic organization of Herbst corpuscles
comparing those of the pigeon shoulder joint
with those of the beak skin (Andres, 1969;
Saxod, 1970, Halata, 1971). In addition, a receptor was encountered that fulfills the previously established criteria for the identification
of Ruffini corpuscles in mammals (Halata,
1977, Biemesderfer et al., 1978).
MATERIALS AND METHODS
Four fully grown domestic pigeons (Columba
livia f. domestica L.) were anesthetized with
intravenous Nembutal. The birds were perfused via the left ventricle with a 6% glutaraldehyde solution in 0.05M Millonig phosphate
buffer (pH 7.2). The capsules of the shoulder
joints were dissected out and cut into small
segments which were then postfixed in 1%
OsO, in 0.1 M Millonig phosphate buffer with
the addition of 1% saccharose. The material
was embedded i n Epon 812 (Luft, 1961).
Semithin sections were stained according to the
method of Ito and Winchester (1963). Ultrathin
sections were stained with uranyl acetate and
lead citrate (Reynolds, 1963)and examined in a
Philips 300 electron microscope at 60 kV accelerating voltage.
Herbst corpuscles were easy to identify in
semithin sections by light microscopy. Other
nerve terminals, i.e., presumptive Ruffini corpuscles, were impossible to recognize in semithin sections and were identified only after extensive searching in the electron microscope.
Portions of four separate Ruffini corpuscles
were studied by electron microscopy.
RESULTS
The articular capsule of the shoulder joint of
the domestic pigeon is similar in structure to
that of a mammalian joint. It consists of two
layers: a t h i n i n n e r layer-the synovial
membrane-and a n outer dense connective tissue layer, the fibrous membrane. The fibrous
layer may be reinforced by ligaments. In some
places the capsule is covered by the epithelium
of an air sac. Our major emphasis was the study
of Herbst corpuscles, and the Ruffini endings
will be dealt with briefly first.
Two types of sensory corpuscles were found in
the articular capsule: Ruffini corpuscles and
Herbst corpuscles.
Ruffini corpuscles occur only in the fibrous
membrane of the articular capsule. The Ruffini
endings were difficult to identify by light microscopy of thick sections and many blocks had
to be sectioned to find the areas illustrated in
the present report. The dense collagenous matrix also presented difficulties in obtaining
artifact-free sections. By electron microscopy
areas of Ruffini endings were characterized by
the following criteria. Each corpuscle consists
of two to four intertwined cylindrical segments
which are approximately 80 pm long and approximately 30 p m wide (Figs. 1-3). The afferent axon is myelinated with a diameter of approximately 3 p m (Fig. 1).After entering the
long side of the cylinder of a Ruffni corpuscle,
the nerve axon loses its myelin sheath (Fig. 1)
and branches several times within the cylinder.
The neurites and associated Schwann cells spiral between bundles of collagen fibrils (Figs. 1
and 2), appearing to envelop bundles of collagen fibrils. The neurite profiles have focal dilatations or varicosities (Figs. 1-3). The varicosities contain many mitochondria and vesicles with diameters ranging from 400 to 600 A
as well as clumps of glycogen granules (Fig. 3).
The neurite profiles in part are enveloped by a
cytoplasmic lamella of a Schwann cell, but
many are covered by a basal lamina (Fig. 3).
The connective tissue core in the corpuscles
(Figs. 1-3) consists of parallel bundles of collagen fibrils which are separated by the cytoplasmic extensions of Schwann cells and by the
flat cytoplasmic processes of fibroblasts referred to as septa1 cells (Schoultz and Swett,
1972,1974).The bundles of collagen run parallel to the longitudinal axis of the cylinder and
leave the corpuscle from the pointed ends of the
cylinder.
The capsule of the Ruffhi corpuscle (Figs. 1,
2) is continuous with the perineurium of the
afferent nerve fiber and consists of two to five
layers of flat cells. The cells of each layer are
connected by means of desmosome-like structures. The cells of the capsule are usually invested by some basal lamina-likematerial. Collagen fibrils course between the basal laminae
of consecutive cells. Capsular cells contain
many pinocytotic vesicles. The perineural capsule of a cylinder is incomplete a t the tapered
ends of the cylindrical profiles. At these points
the bundles of collagen fibrils of the corpuscle
become continuous with collagen fibrils at the
fibrousmembrane as summarized in Figure 13.
ULTRASTRUCTURE OF THE ARTICULAR MECHANORECEPTORS
683
Fig. 1. Cross section through a cylinder of a Ruffini corpuscle. The afferent axon (1)is myelinated and has a diameter of 3
fim. The perineurium of the axon continues to form the capsule of the cylinder (4). Nerve terminals (2) and Schwann cells (3)
encircle bundles of collagen fibrils. x 4,800.
Fig. 2. Cross section through a cylinder of a Ruffini corpuscle. The nerve swellings with mitochondria are surrounded by
Schwann cell cytoplasm processes. Bundles of collagen fibrils course between nerve terminals. x 4,800.
Fig. 3. Longitudinal sectionthrough a cylinder of a Rflini corpuscle in detail. Small finger-likeprojections (arrow)extend
from the axon. Besides the Schwanncells (2)fibroblasts as well as septa1 cells (3)compartmentalizebundles of collagen fibrils.
x 10,Ooo.
684
ZDENEK HALATA AND BRYCE L. MUNGER
Herbst corpuscles occur in the subsynovial
connective tissue between the synovial and the
fibrous membranes and in addition were frequently seen in the connective tissue between
the articular capsule and the muscular fascia.
Herbst corpuscles vary considerably in size and
can be basically divided into small and large
corpuscles. The latter occur in two variantsthose with a thick inner core and those with
several thin ones. Each corpuscle consists of an
afferent nerve fiber, one or more branched
inner cores, a subcapsular space, and a capsule.
Small Herbst corpuscles (Figs. 4-6) occur
singly or in groups of two to five in the subsynovial connective tissue of the capsule. They appear round in cross section (Fig. 4)with a width
ranging from 20 to 50 pm and often have a
somewhat meandering course in longitudinal
sections. The length ranges from approximately 80 to 300 pm.
The afferent axon of the small Herbst corpuscle is myelinated and has a diameter of 3-5 pm.
The nerve fiber loses its myelin sheath on entering the corpuscle. The axon is then enveloped in cytoplasmic lamellae of Schwann cells
of the inner core. The axon may branch or remain unbranched in the core (Figs. 4 and 5 ) .
The terminal end of the axon is dilated and
contains many mitochondria and vesicles with
diameters of approximately 500 A. Axoplasmic
processes of varying lengths penetrate from the
dilatation of the axon into the gaps of the inner
core.
The inner core of small Herbst corpuscles is
formed by thin cytoplasmic lamellae of modified Schwann cells and is more variable in
appearance than the inner core of large corpuscles, as noted below. A cross section through a
small corpuscle demonstrates the interdigitated lamellar profiles of the two paired
Schwann cells (Fig. 4).The axon, which is oval
in cross section, lies in the center of the inner
core. The lamellae are separated by gaps of
approximately 200 A. Collagen fibrils can often
be seen in the space between the outer cyto-
plasmic lamellae of the inner core, but are not
present between inner lamellae.
The number of cytoplasmic lamellae in an
inner core of small corpuscles ranges from 2 to
20; the variation occurs not only between inner
cores of different corpuscles but also along the
course of an inner core. The number of cytoplasmic lamellae in the inner core is greater in
the region of the cell nuclei (up to 20 cytoplasmic lamellae) than in the junction between two
neighboring (connective) cells of the inner core.
At such a junction the cytoplasmic lamellae
may be single or even deficient and the neurite
is enveloped only by a basal lamina (Fig. 6).
These sites resemble a node of Ranvier of
myelinated axons. The innermost cytoplasmic
lamella often has club-like swelling abutting
the neurite (Fig. 6) and desmosome-like contacts can often be seen between these cytoplasmic lamellae of the inner core. The outer cytoplasmic lamellae contain many mitochondria,
scattered elements of Golgi apparatus and
granular endoplasmic reticulum, polyribosomes, and glycogen granules. The inner cytoplasmic lamellae are thin (approximately 600
A) and rarely contain mitochondria or ribosomes. The outermost lamella is enveloped in
filmentous material resembling basal lamina
in appearance.
The subcapsular space of small Herbst corpuscles (Figs. 4, 5 ) extends from the basal
lamina of the inner core to the basal lamina of
the capsule. The width of the subcapsular space
is determined by the size of the corpuscle and
the circumference of the inner core. The subcapsular space contains fibroblasts with long,
flat processes and collagen fibrils and an electron-lucent matrix. Besides thin fibrils with a
diameter of approximately 250 A, there are
thick fibrils with a diameter of 2500-3500 A
present in cross section that appear to be composed of several thin ones (Fig. 4).
The large Herbst corpuscles have an elongated oval shape; they are 300-600 pm long
and 60-120 pm wide. They occur singly in the
Figs. 4, 5. Cross (4) and longitudinal (5) &ion through small Herbst corpuscles. The axon (1) is not myelinated in the inner
core (2).There are collagen fibrils of varying thickness in the subcapsular space (3).The capsule (4) consists of several layers of
perineural cells. x 2,500.
Fig. 6. Longitudinal section through the inner core of a small Herbst corpuscle. The inner core (2) is formed of thin cytoplasmic
lamellae of Schwann cells. Adjacent Schwann cells abut one another in a manner similar to the cells on a node of Ranvier of a
myelinated axon. At this site (arrow) the axolemma of the axon is covered only by a basal lamina. x 8,000,
ULTRASTRUCTURE OF THE ARTICULAR MECHANORECEPTORS
685
686
ZDENEK HALATA AND BRYCE L. MUNGER
adipose tissue of the articular capsule, and in
the periarticular space between the fibrous
membrane and the muscular fascia. Some corpuscles have one large, symmetrical inner core
(Figs. 7 and 10) and others have a branched
inner core (Fig. 11).
The afferent nerve fiber is myelinated and
has a diameter of 5-7.5 pm. It loses its myelin
sheath after entering the corpuscle. The axon
terminal (Fig. 11) in some cases may branch
and the terminal part of the neurite is often
dilatated. The terminal end of the neurite is
larger in diameter and contains many mitochondria and vesicles (Fig. 9). The nerve fiber
and the inner lamella of the Schwann cell of the
inner coreare oftenconnectedbydesmosome-like
membrane specializations (Fig. 9). Small processes arise from the terminal swelling of the
axon and penetrate into spaces between the
cytoplasmic lamellae of the inner core.
The inner core of the large Herbst corpuscles
in cross section is symmetrical in structure
(Fig. 10)and cytoplasmic lamellae may number
up to 60. The outer lamellae contain granular
endoplasmic reticulum, free ribosomes and
mitochondria, and they are thicker than the
inner lamellae. The lamellae are separated by
spaces of 200-300 containing collagen fibrils
in the five to ten outer cytoplasmic lamellae,
mainly running parallel to the longitudinal
axis of the inner core. No collagen fibrils occur
between the inner cytoplasmic lamellae of the
inner core. Adjacent lamellae have desmosomelike membrane specializations (Fig. 8). The outermost lamella of the inner core is enveloped by
basal lamina-like material. Individual branched
inner cores resemble the inner core of small
Herbst corpuscles.
The subcapsular space in large Herbst corpuscles is similar in contents and structure to
small corpuscles described previously.
The capsule of small (Figs. 4 and 5)as well as
large Herbst corpuscles (Figs. 7 and 10) is a
continuation of the perineurium of the nerve
fiber and has a similar structure. There may be
up to 12 layers of perineural cells. The larger
the corpuscle, the greater the number of capsular cell layers. Each layer is enveloped in a
basal lamina. Collagen fibrils extend between
the basal lamina of adjacent layers generally
running parallel to the longitudinal axis of the
corpuscle.
Free nerve endings could not be identified in
the electron micrographs in the present study.
Scattered unmyelinated axons were encountered in the adventitia of blood vessels.
DISCUSSION
The present study verifies in the pigeon the
existence of significant variability in the ultrastructure of Herbst corpuscles and a striking
lack of variability in Ruflini corpuscles even
between avian and mammalian species. These
conclusions verify in ultrastructural terms
previous light microscopic studies of PolaEek
(19661, PolaEek et al., (19661, and Malinovsky
and Zemanek (1970). These studies also regarded Ruffini corpuscles in birds as resemblingin size and structure those in the articular
capsules of various mammals. However, according to PolaEek (1966), Ruffini corpuscles
are far less common in the articular capsules of
birds than of mammals.
The distinctive ultrastructure of avian Ruffini corpuscles, as noted above, resembles those
in other species described to date whether in
the articular capsules of various mammals including the rabbit (Goglia and Sklenska, 1969)
and cat (Halata, 1977), or in similar terminals
associated with hairs in monkey facial skin
(Biemesderferet al., 1978;Halata and Munger,
Fig. 7. Longitudinal section through a large Herbst corpuscle. The nonmyelinated axon (1)lies in an inner core (2) consisting
of 40-60 thin cytoplasmic lamellae of Schwann cells. The subcapsular space between the capsule (4) and the inner core contains
collagen fibrils and fibroblasts. X 1,700.
Fig. 8. Longitudinal section through an inner core of a large Herbst corpuscle. The cytoplasmic lamellae of the inner core are
approximately 200 A wide, and at some sites there are desmosome-likecontacts (*) between the cytoplasmic lamellae. x 15,000.
Fig. 9. Longitudinal section through an inner core of a large Herbst corpuscle. The axon (1)contains many mitochondria. The
cytoplasmic lamellae of the inner core (2) have demosome-like contacts (arrows) between the axolemma of the nerve terminal.
x 13.000.
ULTRASTRUCTURE OF THE ARTICULAR MECHANORECEPTORS
687
688
ZDENEK HALATA AND BRYCE L. MUNGER
ULTRASTRUCTURE OF THE ARTICULAR MECHANORECEPTOFS
1980a; 1980b). The Ruffini corpuscle is
furthermore remarkably similar in ultrastructure to that of Golgi tendon organs as
described by Sklenskh (1972, 1973), Schoultz
and Swett (1972,1974),and Zelena and Soukup
(1977).Whether we are dealing with a tendon,
joint capsule, or hair, the receptor is similar.
A three-dimensional concept of a R e i n i corpuscle summarizing the experience of the present authors is illustrated in Figure 13. The
large myelinated nerve fiber enters a Ruffini
corpuscle along the long axis of the corpuscle
similar to the entry into Golgi tendon organs
(Schoultz and Swett, 1972, 1974).After losing
its myelin sheath in the corpuscle, the nerve
fiber branches repeatedly and spirals between
the fascicles of collagen fibrils in the corpuscle,
resulting in a similar relationship of collagen
fibrils, Schwann cells and associated nerve f i bers, and septa1 cells as is present in Golgi
tendon organs (Schoultz and Swett, 1972,
1974).The nerve terminal has focal varicosities
similar to those in mammalian Ruffini corpuscles (Gogliaand Sklenska, 1969;Halata, 1977).
In mammals the axon varicosities in Ruffini
corpuscles are usually covered by Schwann-cell
cytoplasmic lamellae whereas the axons in Ruffini corpuscles in avian articular capsules are
often covered only by basal lamina. The capsule
of the corpuscle is a continuation of the
perineurium of the sensory nerve, as is the case
of other corpuscular receptors (Shanthaveerappa and Bourne, 1963; PoIaZek and
Halata, 1965; Munger, 1971; Halata, 1977).
The capsule of avian Ruffini corpuscles is not
complete and in this respect resembles those of
Ruffini corpuscles of the skin (Chambers et al.,
1972; Biemesderfer et al., 1978).
Ruffini corpuscles in mammals have been
considered to be a type of mechanoreceptors
(Boyd and Roberts, 1953; Chambers et al.,
1972; Skoglund, 1973; Biemesderfer et al.,
689
1978).R d i n i corpuscles in the domestic pigeon
may have similar functions to those of mammals (Boyd and Roberts, 1953; Freeman and
Wyke, 1967) and are possibly sensitive to
changes of pressure in the joint or in tension in
the joint capsule, and thuse could monitor the
relative positions of the bones. We can only
speculate on the suggestion of Schoultz and
Swett (1972) that the transduction mechanism
might involve “collagen bundles squeezing the
axon.”
The second type of sensory corpuscle in the
articular capsule of birds is the Herbst corpuscle present in the loose collagenous connective
tissue of the margin of the articular capsule.
PolaEek et al., (1966) and Malinovsky and
Zemanek (1970) have published light microscopic studies describing the differences in the
structure and size of Herbst corpuscles in the
articular capsules of various birds. The variability of the corpuscles in the skin of birds has
been discussed in detail by Malinovsky (1967)
and Malinovsky and Zemanek (1971). They
conclude that plumigerous skin contains only
one type of Herbst corpuscle, namely the large
Herbst corpuscle with an unbranched inner
core, while the rhamphotheca and mucous
membranes contain Herbst corpuscles of various sizes with single or branched inner cores.
Unlike the Herbst corpuscles in the rhamphothecae of some aquatic birds (PolaEek, 1969;
Saxod, 1970,1973;Halata, 19711,there are two
types of Herbst corpuscles (large and small) in
pigeon articular capsules. The large corpuscles
in turn can be divided into typical Herbst corpuscles with unbranched inner cores, and corpuscles with branched inner cores. Each small
as well as each large Herbst corpuscle has a
capsule of presumptive perineurium resembling other corpuscular receptors (Shanthaveerappa and Bourne, 1963;Munger, 1971;Halata
and Groth, 1976).
Fig. 10. Cross section through a large corpuscle with one inner core. The axon in the inner core (1)is oval in cross section.The
inner core consistsof a system of cytoplasmic lamellae from two Schwann cells situated opposite each other (2). In the subcapsular
space (31, the thick collagen fibrils are closer to the inner core, the thin ones closer to the capsule (4).x 2,000.
Fig. 11. Cross section through a large corpuscle with several inner cores. Each of the three inner cores is made up of
cytoplasmic lamellae from Schwann cells (2). One of the inner cores has two axons (1).x 3,000.
Fig. 12. Cross section through a lamellar system of an inner core of a Herbst corpuscle. At some points there are desmosomelike contacts (arrows) between the cytoplasmic membranes of the Schwann cell lamellae. x 34,000.
Fig. 13. Semidiagrammatic representation of a Ruffini corpuscle from an articular capsule. Several myelinated axons
enter the corpusclefrom the long side. Bundles of collagen fibrils pass through the cylindersof the corpuscle. The longitudinal
axis of the cylinder lies parallel to the course of the collagen fibrils. A and B represent hypothetical cross-sectionalimages
through the planes of the diagram of the corpuscle as indicated.
ULTRASTRUCTURE OF THE ARTICULAR MECHANORECEF'TORS
The structure of the inner core of the large
Herbst corpuscles is similar to the inner core of
the Herbst corpuscles in the rhamphothecae of
various aquatic birds (Quilliam, 1966; Halata,
1971). The inner core of small corpuscles is
variable in appearance, but we have no reason
to suggest that it would not also have pseudocholinesterase as described by Saxod (1973).
The absence of the cytoplasmic lamellae resembling nodes of Ranvier a t the junction of
successive inner core cells has not been described previously. In these regions the axon
terminal in some places is covered only with a
basal lamina. The functional significance of
these areas is speculative at present.
Herbst corpuscles are regarded as rapidly
adapting (RA) receptors (Donvard and McIntyre, 1971; Gregory, 1973; Gottschaldt, 1974)
analogous to Pacinian corpuscles or simple corpuscles (Munger, 1971; Halata, 1975) in mammals. While most physiologic studies have involved Herbst corpuscles from duck bill skin
(Gregory, 1973; Gottschaldt, 19741, Donvard
and McIntyre (1971) studied Herbst corpuscles
in the interosseous membrane of the hind limb.
Such corpuscles in the tibiofibular membrane
are similar physiologically to those of the beak.
We thus conclude that Herbst corpuscles of
joint capsules a r e most likely similar in
physiologic parameters and that avian joint
capsules have two functional classes of receptors, as do mammalian joint capsules. Ruffini
corpuscles thus subserve SA function and
Herbst corpuscles RA function. The striking
variability in structure of Herbst corpuscles is
thus reflected in an equivalent variability in
physiologic parameters defined to date.
ACKNOWLEDGMENTS
This work was supported in part by Deutsche
Forschungsgemeinschaft and by U.S. Public
Health Service research contracts NIDR 722401 and HD4-2869 and research g r a n t
HD11216.
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