The ultrastructure of Ruffini and Herbst corpuscles in the articular capsule of domestic pigeon.код для вставкиСкачать
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. LITERATURE CITED Andres, K.H. (1969) Zur Ultrastruktur verschiedener Mechanorezeptoren von hoheren Wirbeltieren. Anatomischer Anzeiger, 124: 551-565. Biemesderfer, D., B.L. Munger, J. Bink, and R. Dubner (1978) The pilo-Ruffini complex: A non-sinus hair and associated slowly-adapting mechanoreceptor in primate facial skin. Brain Res., 142: 197-222. Boyd, LA., and T.D.M. Roberts (1953) Proprioceptive discharges from stretch-receptors in the knee joint of the cat. J. Physiol., 122: 38-58. Chambers, M.R., K.H. Andres, M.V. Duering, and A. Iggo (1972) The structure and function of the slowly adapting twe I1 mechanoreceDtor in haiw skin. Quart. J. EXP. Physiol., 57: 147-446. 691 Dorward, P.K., and A.K. McIntyre (1971)Response ofvibration-sensitive receptors in the interosseous region of the duck's hind limb. J. Physiol. (Lond.),219: 77-78. Freeman, M.A.R., and B. Wyke (1967)The innervation of the kneejoint. An anatomical and histological study in the cat. J. Anat., 101: 505-532. Goglia, G., and A. Sklenska (1969) Ricerche ultrastructturali sopra i corpuscoli di R a i n i delle capsule articolari nel coniglio. Quaderni Anatomia Pratica, 25: 14-27. Gottschaldt, K.-M. (1974) The physiological hasis of tactile sensibility in the beak of geese. J. Comp. Physiol., 95: 29-47. Gregory, J.E. (1973) An electmphysiological investigation of the receptor apparatus in the duck's bill. J. Physiol. (Lond.), 229: 151-164. Halata, Z. (1971) Die Ultrastruktur der Lamellenkorperchen bei Wasservogeln (Herbstsche Endigungen).Acta Anatomica, 80: 362-376. Halata, Z. (1975) The mechanoreceptors of the mammalian skin. Ultrastructure and morphological classification. Advances in Anatomy, Embryology and Cell Biology, 50: 1-77. Halata, Z. (1977) The ultrastructure of the sensory nerve endings in the articular capsule of the knee joint of the domestic cat (Ruffini corpuscles and Pacinian corpuscles). J. Anat., 124: 717-729. Halata, Z., and H.-P. Groth (1976) Innervation of the synovial membrane of the catsjoint capsule. An ultrastructural study. Cell Tissue Res., 169: 415-418. Halata, Z., and B.L. Munger (198Oa)Sensory nerve endings in rhesus monkey sinus hairs. J. Comp. Neurol., 192: 645-663 (a). Halata, Z., and B.L. Munger (1980b) The sensory innervation of primate eyelid. Anat. Rec., 198:663-676. Ito, S., and R.J. Winchester (1963) The fine structure of the gastric mucosa in the bat. J. Cell Biol., 16: 541-578. Luft, J.H. (1961) Improvements in epoxy resin embedding methods. J. Biophys. Biochem. Cytol., 9: 409-414. Malinovsky, L. (1967) Die Nervenendkorperchen in der Haut von Volgeln und ihre Variabilitat. Zeitschrift fur mikroskopisch-anatomischeForschung, 77: 297-303. Malinovsky, L., and R. Zemanek (1970) Sensory nerve endings in the joint capsules of the large limb joints in the domestic hen (Gallus domesticus) and the rook (Corvus frugilegus). Folia. Morphol. (Prague), 18: 206-212. Malinovsky, L., and R. Zemanek (1971)Sensory innervation of the skin and mucosa of some parts of the head in the domestic fowl. Folia Morphol. (Prague),19: 18-23. Munger, B.L. (1971) Patterns of organization of peripheral sensory receptors. In: Handbook of Sensory Physiology. W.R. Loewenstein, ed. Springer-Verlag Berlin, Heidelberg, New York, Chapter 17, pp. 523-556. Polakk, P. (1966) Receptors of the joints. Their structure, variability and classification. Acta Facultatis Medicae Universitatis Brunensis, 23: 1-107. Polakk, P. (1969) Ultrastructur des Herbstschen Korperchen im Vergleich mit dem Pacinischen Korperchen. Collection Scientific Works Facultatis Medicae Charles University Hradec Kralove, 12: 417-426. PolaEek, P., and 2. Halata (1965) Beziehung der Kapsel der Nervendigungen zu den Hullen des Nervensystems. Scripta medica (Brno), 38: 73-83. PolaEek, P., A. Sklenska, and L. Malinovsky (1966) Contribution to the problem of joint receptors in birds. Folia Morphol. (Prague), 14: 33-42. Quilliam, T.A. (1966) Unit design and array patterns in receptor organs. In: Touch, Heat and Pain. A.U.S. de Reuck and J. Knight, eds. Ciba Foundation Symposium, Churchill, London, pp. 8G116. Reynolds, E.S. (1963)The use of lead citrate a t high pH as an electron-opaque stain in electron microscopy. J. Cell Biol., 17: 208-212.- 692 ZDENEK HALATA AND BRYCE L. MUNGER Saxod,R. (1970)Etude au microscope electronique de l'histogenese du corpuscles sensoriel cutane de Herbst chez le Canard. J. Ultrastruct. Res., 33: 463-482. Saxod,R. (1973) Activite cholinesterasique des corpuscles sensoriels cutanes de Herbst et de Grandry. Etude h i s b chimique en microscopie optique et electronique. Histochemie, 34: 43-63. Schmidt, R.F. (1976) Somato-viscerale Sensibilitat Hautsinne, Tiefensensibilitat, Schmen. In: Einfuhrung in die Physiologie des Menschen. Springer-Verlag Berlin, Heidelberg, New York, pp. 206225. schoultz, T.W., and J.E. Swett (1972) The fine structure of the Golgi tendon organ. J. Neurocytol., 1: 1-26. Schoutz,T.W., and J.E. Swett (1974)Ultrastructural organization of the sensory fibers innervating the Golgi tendon organ. Anat. Rec., 179: 147-162. Shanthaveerappa, T.R., and G.H. Bourne (1963) New observations on the structure of the Pacinian corpuscle and its relation to the perineural epithelium of peripheral nerves. Am. J. Anat., 112: 97-109. Sklenska, A. (1972) Contribution to the ultrastructure of the Golgi tendonorgan. Folia Morphol. (Prague),ZO: 195-197. Sklenska, A. (1973) Die Ultrastruktur des Golgischen Sehnenorgans bei der Katze. Acta Anat., 86: 205-221. Skoglund, S. (1973) Joint receptors and kinestetics. In: Handbook of Sensory Physiology. A. Iggo, ed. SpringerVerlag Berlin, Heidelberg, New York, Vol. 11,pp. 111-136. Wyke, B. (1973) Structural and functional characteristics of articular receptor system. Acta chirurgiae ortopedicae et traumatologiae Cechoslovaca,40: 489-497. Zelena, E., and T. Soukup (1977) The development of Golgi tendon organs. J. Neurocytol., 6: 171-194.