Ultrastructure of the Eimer's organ of the star-nosed mole

THE JOURNAL OF COMPARATIVE NEUROLOGY ,765~343-354 (1996)

Ultrastructure of the Eimer’s Organ of the Star-Nosed Mole

KENNETH C. CATANIA Department of Psychology, Vanderbilt University, Nashville, Tennessee 37240

ABSTRACT The nose of the star-nosed mole consists of 22 fleshy appendages that fan out from around

the nostrils and are covered with specialized epidermal sensory receptors called Eirner’s organs. The Eimer’s organs of the star-nosed mole are domed epidermal papillae approximately 40 to 50 pm in diameter. The center of each papilla contains a column of stacked circular epidermal cells closely associated with five to ten neural processes that originate from three myelinated fibers in the underlying dermis. At middle and lower levels in the cell column, a single nerve fiber is located in the center of the column, enclosed by the epidermal cells which wrap around the fiber and form desmosomes between their own adjacent plasma membranes. An additional five to ten fibers travel up the sides of the column ensheathed in the margins of the epidermal cells. At the top of the cell column, the nerve fibers produce a repeated series of terminal swellings. These terminal swellings converge in the center of the column, where a single epidermal cell completely encapsulates each circular arrangement of nerve terminals. No synapses or other cellular junctions were observed between the nerve terminals where they converge within the cell column. There is a single Merkel-like ending at the base of the cell column, and a single encapsulated corpuscle beneath the cell column, in the connective tissue of the dermis. The structure of Eimer’s organs is consistent with a mechanoreceptive function. 1996 X‘i’ilpp-Liss, Inc.

Indexing terms: epidermis, mechanoreceptor, skin, tactile, insectivore

In addition to dramatic skeleto-muscular adaptations for digging (Yalden, 19661, talpid moles have sensory specializations that enable them to successfully navigate tunnels and find food in their underground habitat. As might be ex- pected, moles have poor eyesight, with small eyes and a tiny optic nerve. Instead of depending on sight, moles have a well-developed sense of touch. They have many sensory vibrissae on both their nose and forelimbs, but their most important sensory surface seems to be the glabrous tissue of the snout, which contains specialized sensory receptors called Eimer’s organs. Eimer’s organs are domed epidermal papillae, usually about 60 km in diameter, containing a column of epidermal cells in association with free nerve endings, Merkel cell-neurite complexes, and encapsulated corpuscles. These structures were first described by Eimer (1871), in the European mole, Talpa europaea, and they have subsequently been found on all talpid moles that have been examined (Giacometti and Machida, 1965; Van Vleck, 1965; Shibanai, 1988; Catania, 1995a). They are also found on the snout of the pyrenean Desman, Galemys pyrenaxus (Richard, 1985), and on the snouts of some shrews (Per- netta, 1977). All of these species explore their environment by touching the glabrous tissue of their snout to objects and prey items, suggesting that Eimer’s organs are used for tactile discrimination. Recently, physiological recordings from the somatosensory cortex of the star-nosed mole have

confirmed that Eimer’s organs are highly sensitive to fine tactile stimulation (Catania et al., 1993; Catania and Kaas, 1995).

The star-nosed mole is the most conspicuously specialized mole, having 22 fleshy nasal appendages that are covered with tens of thousands of Eimer’s organs. The nose of the star-nosed mole is unique from that of other species, both in the gross anatomy of the snout and in the fine structure of Eimer’s organs in the epidermis (see Catania, 1995a, for a discussion of ecological factors affecting the structure of Eimer’s organ). The snout of the star-nosed mole has recently been examined using scanning electron microscopy and light microscopy (Catania, 1995b). The results revealed Eimer’s organs that are smaller than those of other mole species and that possess a complex pattern of nerve endings nut found in any other mammalian skin surface. The somatosensory representation of these Eim- er’s organs is greatly enlarged relative to other body parts, and is specialized in the form of modular units that represent each nasal appendage (Catania and Kaas, 1995).

Accepted August 21, 1995. Address reprint requests to Kenneth C. Catania, Department uf Psychol-

ogy, Vanderbilt University, 301 Wilson Hall, 111 21st Ave South. Nashville TK. 37240

o 1996 WILEY-LTSS, INC.

344

This study was undertaken to further explore these specialized sensory organs, with emphasis on the fine structure of the newly described neural configuration within the epidermis, and the relationship between the nerve terminals and the surrounding epidermal cells.

K.C. CATANIA

MATERIALS AND METHODS For this study two star-nosed moles (Condylura cristata)

were caplured in Potter County, Pennsylvania under per- mit number COL0087. After being given a lethal dose of sodium pentobarbital (90 mgikg), they were perfused with phosphate buffer (pH 7.4) followed by phosphate-buffered 4% glutaraldehyde solution. The snouts were removed and immersed in fresh, phosphate-buffered 4% glutaraldehyde overnight. Tissue from appendages 1, 5, and 11 was removed and postfixed in osmium tetroxide, dehydrated in a graded ethanol series, transferred into propylene oxide, and then embedded in Durcupan (EM Sciences). Ultrathin sections where cut on a Reichert Ultracut E ultramicro- tome with a diamond knife, mounted on formvar-coated slot grids, and stained with lead citrate for 2 minutes. Tissue was viewed in a Jeol lOOCX transmission electron microscope.

For scanning electron microscopy, the contralateral appendages where removed, washed in tap water overnight, and then dehydrated in a graded ethanol series. The tissue was then transferred from 100% ethanol into a critical point dryer in which the ethanol was replaced with liquid carbon dioxide. After critical point drying, the specimens were mounted on aluminum stubs, sputter coated with gold, and viewed in a Cambridge 360 Stereoscan scanning electron microscope.

RESULTS External appearance

There are 25,000-30,000 Eimer’s organs located on the 22 nasal appendages that fan out around the nostrils of the star-nosed mole (Catania, 199513). On the surface of the appendages the Eimer’s organs appear as raised papillae approximately 40 pm in diameter (Fig. lA,B). They completely cover the distal portion of each appendage, as well as the proximal surface around the nostrils. The Eimer’s organs are arranged in a continuous honeycomb pattern with each organ typically surrounded by six neighbors. The outer keratinized skin surface of each Eimer’s organ contains a circular disk, at the apex of the domed surface (Fig. 1C). This circular disk is a single keratinized cell of the outermost skin layer (the stratum corneum), and it is the uppermost cell in a stack of epidermal cells that form a column running from the underlying dermis to the external skin surface (Fig. 2). As with any skin surface, there is a constant turnover of cells that make up Eimer’s organ, such that the lower epidermal cells die and join the stratum corneum, while the stratum corneum sheds dead cells from its outer surface. Some of these sloughing cells are visible on the surface of Eimer’s organ (Fig. 1B). The circular disk on the thin stratum corneum of Eimer’s organ is a reflec- tion of the columnar organization of the underlying epidermal cells from which the stratum corneum was derived.

Internal structure The sensory receptors within Eimer’s organ are orga-

nized in a linear array in association with the column of

epidermal cells. There is a series of neuronal terminal swellings just under the stratum corneum at the top of the cell column, in addition to a Merkel-like terminal at the base of the column and an encapsulated corpuscle immediately below the cell column, in the connective tissue of the dermis. The basic structure is shown in Figure 2, and this schematic diagram is used as a reference to the locations and orientation of the photomicrographs in the remaining figures.

Among .the basal epidermal cells at the bottom of each Eimer’s organ there is a single cell that stands out in osmium-fixed preparations, exhibits a convoluted nucleus, and is contacted by a neurite on its basal surface. In light microscopic sections (Catania, 1995b), its appearance and location are almost identical with the Merkel cell-neurite complexes identified in the Eimer’s organs of the European mole (Halata, 1972; Andres and von During, 1973). However, the tran.smission electron micrographs in this study did not reveal dense core granules polarized to the neurite or numerous cytoplasmic spikes within the contacted cell (Fig. 3A,€3), features typical of Merkel cells in most species (Munger and Ide, 1988).

The long (horizontal) axis of the cell is roughly 9 pm. It has a convoluted nucleus located toward the basal side of the cell, just above the contacting neurite. The cytoplasm contains many mitochondria as well Golgi complexes. The plasma membrane of the cell is interdigitated with the membranes of the surrounding epidermal cells, where there are numerous desmosomal attachments. The neurite con- tacts the basal side of the cell and exhibits many neurofila- ments and mitochondria. Areas of increased density occur along the junction of the neurite and Merkel-like cell, where the intercellular space is obscured between the adjacent plasma membranes.

In the dermis approximately 4 pm below the basal cells of the central column of each Eimer’s organ, there is a single encapsulated corpuscle oriented with its long axis parallel to the skin surface (Fig. 3C,D). A single unbranched nerve terminal is completely encapsulated by numerous lamellae. The nerve terminal is approximately 2.5 pm in diameter, is circular in transverse section: and contains numerous mitochondria arranged close to the plasma membrane. The long axis of the corpuscle is approximately 30-35 pm, and the short axis is approximately 20-25 pm. The lamellae immediately surrounding the terminal are tightly packed, becoming less dense and larger at a distance of 4-5 km from the terminal. There is no clear distinction between inner and outer cores, as seen in Pacinian corpuscles.

The epidermal cell column. The epidermis on the snout of the star-nosed mole is relatively thin, usually only 60 pm in thickness from the connective tissue of the dermis to the exterior surface of stratum corneum, when measured in the center of an Eimer’s organ. The stratum corneum at the apex of the cell column is only 5-7 pm in diameter, and it overlies the remaining 12 to 15 cells that form the cell column. This column in the center of each papilla is a stack of flattened disk-shaped epidermal cells and is only one cell in diameter (Figs. 4, 5A). Because the column spans the entire vertical extent of the epidermis, the cells differ in their morphology at various levels in the column, reflecting different states of keratinization. At its base, among the germinal epidermal cells, the cell column is indistinct and the cells appear roughly cuboidal in shape. Midway toward the outer skin surface, there is a clear distinction between a

Merkel-like complex.

Encapsulated corpuscle.

EIMER’S ORGANS 345

Fig. 1. The external skin surface on the snout of the star-nosed mole as revealed by scanning electron microscopy. A A single appendage (ray 5 ) from the nose is covered with small raised papillae called Eimer’s organs. Most of the 22 nasal appendages have over 1,000 Elmer’s organs on their surface. B: A higher-magnification micrograph of individual Eimer’s organs shows the typical hexagonal arrays of 40- to 50-km domes, cach containing a circular disk in the center. C: The

distinctive circular disk is a single keratinized cell of stratum corneum and is the top cell of a vertical column of cells that runs from the dermis to the exterior. The arrow marks a dimple found on most Eimer’s organs of the star-nosed mole and relates in position to an inclusion in the stratum corneum derived from an encapsulated nerve terminal (see text for details).

central column and surrounding epidermis, and cells in both areas have become somewhat flattened (Figs. 2, 5B). The last two to three cells at the top of the column are in the later stages of keratinization and have a polarized internal morphology (Fig. 5D) with electron-dense tonofibrils, keratohyaline granules, and the nucleus situated at the lower surface and nerve terminals (encapsulated by the epidermal cell) above. All of the cells of the column and the surrounding support cells of the structure are interdigitated with one another and exhibit multiple desmosomes along their junc-

tional boundaries. The external surface of the cell column (stratum corneum) usually consists of six to seven flattened and keratinized cells, also exhibiting the remnants of numerous desmosomal adhesions between membranes.

h’erue terminals within the cell column. There are usually between five and ten neural processes that branch from three separate myelinated fibers in the dermis (Cata- nia, 199513). They lose their myelin sheath before entering the epidermis (Fig. 5C) and then ascend toward the outer skin surface in close association with the cells in the central

346 K.C. CATANIA

toward the periphery. This terminal neural configuration is repeated several times at the top of the column (Fig. 71, appearing to be in the process of formation at lower levels.

Because this neural complex is encapsulated by a single epidermal cell at each level, lhere are four plasma membranes visible at the juncture of any two terminal swellings, one membrane from each terminal swelling, and a membrane of the epidermal cell surrounding each terminal swelling (Fig. 6C, and see schematic Fig. 9). There is a small, 70- to lOO-nm, intercellular space of the epidermal cell between the nerve terminals (Fig. 6C), and thus there does not seem to be any form of communication between the terminals (e.g., synapses or junctional complexes).

Within the encapsulating epidermal cell, the nucleus is often visible below the nerve terminals, as though cradling the entire complex (Figs. 5D, 7A). Below the nucleus, many keratohyaline granules are present in association with tonofibrils. Horizontal sections through the very bottom of the nerve terminals (Fig. 6B) reveal a series of dense tonofibrils, within the enclosing epidermal cell, that seem to anchor the terminal at its base. There are no desmosomes or other junctions apparent between the enclosing epidermal cell and the nerve terminals, so it is unclear how the plasma membranes and the tonofibrils interact.

In favorable sections a remnant of the central terminal swelling is visible in the center of the keratinized cells of stratum corneum (Fig. 8). This remnant corresponds to the position of a dimple on the outer surface of the cell column (arrow, Figs. l C , 8B). The unusual relationship between the central nerve terminal and the epidermal cells results in this visible artifact (dimple) on the surface of Eimer’s organ (see discussion).

DISCUSSION The appendages of the star-nosed mole are covered with a

remarkably specialized skin surface. As in other species of talpid moles, the skin is made up of epidermal papillae that contain a central cell column in association with sensory

Quilliam, 1966; Halata, 1972; Shibanai, 1988; Catania, 1995a). These structures in the star-nosed mole are uniquely

Fig. 2. Schematic of the internal structure of Eimer’s organ in the star-nosed mole. A thin stratum corneum (keratinized epidermal layer) overlies a column of epidermal cells in the center of each papillae. There is encapsulated corpuscle, a Merkel-like complex, and series of terminal

linear array in association with the cell column. The labeled correspond to the approximate location and orientation of the corre-

neural swellings just a under the corncum, all .&gned in a receptors (Eimer, 1871; Giacometti and Machida, 1965;

sponding figure plate.

cell column. The fibers form a concise geometric pattern, with a single fiber in the center of the cell column, surrounded by five to ten satellite fibers on the margins of the cell column (Figs. 4, 5A). At intermediate levels, the central fiber is enclosed by the flattened cells of the column, which surround the fiber and form multiple desmosomes between their own adjacent plasma membranes. This main- tains the epidermal cell’s circular shape, while allowing the nerve fiber to pass through the center of the column.

As the fibers pass upward and approach the stratum corneum, branches of the satellite fibers turn inward into each upper epidermal cell in the column (Fig. 5B). These branches become entirely encapsulated by each corresponding epidermal cell of the column. They form terminal swellings that abut a terminal swelling of the central fiber (Fig. 61, which is likewise cncapsulated by the epidermal cell. In horizontal sections-tangential to the domed surface-this unusual neural configuration appears as a “hub and spoke” arrangement wilh the central terminal swelling in the center, and the satellite terminal swellings radiating

organized and have features not observed in any other mammalian skin. The most notable specialization is the organization of the cell column and the associated nerve terminals that lie just under the stratum corneum. These structural features are discussed with an emphasis on the nerve terminals in the epidermis and their relationship to the epidermal cells, followed by a discussion of the function of Eimer’s organs. Last, the structure of Eimer’s organ is briefly discussed in an evolutionary context, based on recent comparisons with other mole species and their respective environments (Catania, 1995a).

The epidermal cells that form the central cell column and surrounding support structure of Eimer’s organ are keratinocytes, so named because their primary role in most skin surfaces is to produce the keratinized outer layer of stratum corneum. In addition to this role, the keratinocytes in the Eimer’s organs of the star-nosed mole also act as a structural framework for the sensory receptors in the form of the central cell column, and they encapsulate the nerve terminals a t the top of the cell column. The combined require- ments of these two roles, sensory support structure and keratinocyte, lead to the unique external and internal

Structure of Eimer’s organ.


Fig. 3. The presumptive Merkel cell-neurite complex and encapsulated corpuscle at the hase of Eimer’s organs. A: A neurite (nJ enters the epidermis and makcs contact with a uniquc cell (M) among the germinal epidermal cells. The cell membrane is interdigitated with those of the surrounding epidermal cells. x 5.500. B: Higher magnification of‘ the contacting neurite 1 nJ and the convoluted nucleus 1 nUCJ of the contacted cell. There are many mitochondria visible within the rieurite and the cell. Areas of increased density are visible periodically

features of Eimer’s organ. The most obvious external feature is the presence of a circular disk on the outer surface of each papillae. This disk is the outermost keratinized cell of the central epidermal column; thus the external surface of Eimer’s organ reflects the internal columnar organization of the cells. A more subtle exlernal landmark is the dimple in the center of this keratinized cell, which seems to be the remnant of an encapsulated nerve terminal. Internally, the association of the nerve terminals with the cells within the central column is unique and diverges from the pattern seen in other talpid Eimer’s organs that have been examined (Catania, 1995a).

Free nerve endings that penetrate the epidermis of mammals often have an intimate association with the surrounding epidermal cells (Munger and Ide, 1988). This

along the adjacent membranes of the neurite and cell. ~12,500. C: The encapsulated corpuscle is located in the connective tissue of the dermis, immediately below the epidermal cell column (upper right). A single neurite I arrow) is enclosed by many lamellae that hecome progressively less dense toward the periphery. e, epidermis ~ 2 , 6 0 0 . D: The encapsulated neurite contains numerous mitochondria located close. to the plasma membrane. x 10,000. See Figure 2 for the approximate location of A and C relative to Eimer’s organ structure.

is also true for the nerve terminals in the Eimer’s organs of other mole species, which are also invested to various degrees in epidermal cells of a cell column (Shibanai, 1988; Catania, 1995a). In the star-nosed mole, however, the role that single small epidermal cells play in encapsulating a relatively large and complex array of terminal swellings at the top of the cell column is unparalleled among mammalian intra-epidermal nerve fibers. Nevertheless, comparison of the organs of‘ the star-nosed mole with those of other north American species strongly suggests that these nerve terminals are homologous to intra-epidermal free nerve endings found in other mammalian glabrous skin. In the eastern American mole, the nerve terminals within the epidermis form terminal swellings that are not associated with a well-organized cell column (Catania, 1995a). This

348 K.C. CATANIA

downward at their margins (Fig. 2). The effect is to further elevate the nerve terminals. This also gives the impression of increased turgidity within the central column, an effect that may be important if differential compression of the terminals is the appropriate stimulus,

In addition to the dramatic differences in the configuration of the nerve terminals within the cell column, the Merkel-like ending at the base of the column also seems to differ from those found in the Eimer’s organs of other species. There were no cytoplasmic spikes observed in the presumptive Merkel cell. Although none were reported or illustrated for Merkel cells of the Japanese shrew mole (Shibanai, 19881, cytopasmic spikes are typical of Merkel cells in most mammals. There was also an absence of dense-core granules within the presumptive Merkel cell. In spite of these apparent differences, the consistent association of a contacting neurite with this unique cell in the epidermis, and its overall similarity in position and appearance to the Merkel cells reported in the Eimer’s organs of other mole species (Halata, 1972; Andres and von During, 1973; Shibanai, 19881, indicate that it is likely a homologous structure, perhaps having specializations unique to the star-nosed mole.

What is the function of the Mole’s star? It is difficult to view the nose of the star-nosed mole without entertaining the possibility that this species has very unusual sensory capacities. Indeed, it has been tentatively hypothesized that the star of the mole is used as an electroreceptive organ (Gould et al., 19931, based heavily on comparisons with the ecology and behavior of the duck-billed platypus, which has been shown to respond to electric fields (Scheich et al., 1986; Gregory et al., 1987, 1988; Iggo et al., 1988). How- ever, recent reports, including the present study, have greatly clarified the nature of the sensory organs on this mole’s unusual snout. An important finding regarding the overall function of the star of the star-nosed mole is that it is devoted entirely to Eimer’s organs. There is no evidence of other large receptor complexes such as the gland duct electroreceptors, ampullary type organs, or ciliated cells that might mediate an electric sense (Catania, 1995b). In fact, when comparing the sensory organs of the duck-billed platypus and the star-nosed mole, one finds a striking similarity between the mechanoreceptive push-rods of the platypus, and the Eimer’s organs of the star-nosed mole (and the Eimer’s organs of other mole species), and a lack of any organ comparable to the gland-duct electroreceptors of the platypus.

Electroreceptors are invariably specialized so as to give direct access of hair cells or nerve endings to the environment (Zakon, 1986; Andres and von During, 1988). This is not the case for Eimer’s organs of the star-nosed mole or other mole species. The results of this study show a layer of six to eight keratinized cells of stratum corneum that overlie the nerve terminals. These cells are joined to one another by numerous desmosomes along their borders. They are also extensively interdigitated with neighboring cells at the margins of the cells column, where there are also numerous desmosomal adhesions. The opposing plasma membranes of the cells of the stratum corneum show a thickening and increased density, characteristic of the intercellular glycolipid deposition that forms a water barrier between the environment and the underlying tissues in the epidermis. Although the stratum corneum over the cell column is very thin compared to other mammalian skin

Fig. 4. Horizontal section (parallel to the skin surface) midway through an Eimer’s organ and stained by the Winkelmann Schmit method and toluidine blue. A single circular epidermal cell of the cell column is located in the center with the associated neural processes that travel through the column. The nerve fibers form a concise pattern with a single fiber in the center (cnf), surrounded by (in this case) six satellite fibers (snf). Nuclei aredarkly stained (nuc). Scale bar = 10 pn. See Figure 2 for the approximate level of the tissue section.

may be due to a harsher soil environment which requires a much thicker stratum corneum on the snout of this species, thus preventing the formation of the cell column. The result is a less-specialized array of sensory organs on the snout of the eastern American mole, a condition which is very similar to the arrays of sensory receptors (encapsulated corpuscles, Merkel-cell neurite complexes, and free nerve endings) seen in other mammals (Munger, 1965; Quilliam, 1980; Halata, 1990).

In addition to the encapsulation of the nerve terminals, another unusual feature of this structure is the location of the terminal swellings relative to the stratum corneum. Of the several repeated levels of terminal swellings, the top- most (outermost) is encapsulated by the very last epidermal cell that has not yet joined the stratum corneum. Thus there is an apparently fully functional nerve terminal encapsulated within a cell undergoing the final stages of keratinization, at a distance of only 5-6 ym below the exterior skin surface. That these nerve terminals are present and functional until the very last stages of keratinization is further indicated by a remnant of the central terminal swelling, complete with degenerated mitochondria, that appears as an inclusion within the overlying cells of the stratum corneum. It seems that the nerve terminal area simply “pinches off,” leaving a remnant as the epidermal cell joins the stratum corneum. This inclusion in the stratum corneum cell leaves a weak point in its center that manifests itself as a dimple on the outer surface when viewed in the scanning electron micrographs (see arrowheads, Figs. lC, 8B).

Other features of Eimer’s organ also seem designed to bring these terminals as close as possible to the external environment. For example, the outermost layer of stratum corneum is thinnest over the cell column, being only 5-6 pm in diameter, and thicker (10-15 pm) over the margins of each papilla. Also, the uppermost epidermal cells that surround the cell column flex upward where they attach to the column, whereas those that make up the column flex


Fig. 5. The cell column and associated fibers. A Horizontal section through Eimer’s organ at roughly the same location as Figure 4, showing a single epidermal cell of the cell column and the circular pattern of nerve fibers. There are six satellite fibers on the periphery of the column and a single fiber in the center, within the convexity of lhe surrounding nucleus. Note that the epidermal cell of the column encircles the central fiber and interdigitates with itself (arrowheads) as also occurs between the column and adjacent epidermal cells (arrows). snf, satellite nerve fiber; cnf, central nerve fiber. ~ 6 , 6 0 0 . B: Vertical section through the column shows the stack of epidermal cells as well as a single satellite nerve fiber (snf) and portions of additional fibers (same orientation as schematic in Fig. 2). A portion of the central terminal swelling (ds) can be seen at t,he top of the column, adjacent to a

surfaces, it does not appear to be specialized to allow access of the nerve terminals to the environment.

Eimer’s organs are gener- ally assumed to be tactile sense organs, and recent electro- physiological evidence from the cortex of the star-nosed mole confirms this in the case of the star-nosed mole. The Eimer’s organs in the star-nosed mole are highly responsive to fine tactile stimulation and have a large representation in both the primary somatosensory 61) and secondary somato-

Function of Eimer’s organ.

terminal swelling of the satellite fiber (sts). Arrows mark cell boundaries characterized by numerous desmosomes. ~4,500. C: A fiber losses its myelin sheath as it enter the cpidermis to travel up the column. ~6,200. D: The polarized internal morphology of the cells at the top of the column (same orientation as B). Large arrows mark the upper and lower boundaries of the epidermal cell, where numerous desmosomes are present. The lower portion of the cell contains electron-dense tonofibrils in close association wilh keratohyalinc granules (k). Just above this, the nucleus (N) is located, seemingly compressed by the central (cts) and satellite terminal swellings (sts) that are encapsulated by the epidermal cell. x 17,500. The approximate locations of A-C are indicated on the schematic in Figure 2.

sensory (S2) areas (Catania et al., 1993; Catania and Kaas, 1995; Catania, 1995~). They are responsive to the onset and offset of depression, to rocking a small probe on the surface, and to sustained depression (Cataniaand Kaas, 1995). Each of the appendages of the star of the mole is represented in cortex by a stripe visible in both the primary (Sl) and secondary (Y2) somatosensory areas. All striped areas were responsive to tactile stimulation, and within these areas, there were no subfields that were not sensitive to tactile

Fig. 6. The organization of terminal swellings at the apex of the cell column, as seen in a horizontal section, just below the circular disk visible in Figure 1C (see Fig. 2 for approximate level of section). A: A single terminal swelling (CTS) of the central fiber is surrounded by seven terminal swellings of the seven satellite fibers (STS). The entire complex is encapsulated within a single flattened epidermal cell at the top of the cell column that is undergoing the final stages of keratinization before joining the stratum corneum. Many tonofibrils are present within the cytoplasm of the encapsulating cell, as well as part of its nucleus (Ni. The surrounding electron-dense cells are part of the stratum corneum (SC) that forms the exterior of Eimer’s organ. Numerous desmosomes are visible bctween adjacent epidermal cell

membranes, but there are no junctions apparent between the terminal swellings. ~9,400. B Section through the bottom of a satellite terminal swelling (STS) showing an anchoring framework of tonofibrils at its base. The nucleus of the encapsulating epidermal cell (N) is visible in close association with the base of the terminal swelling. x 34,000. C: At the juncture of the terminal swellings a small intercellular space of the epidermal cell remains ( k J . There arc four plasma membranes visible (between arrows) between the intracellular space of the central terminal swelling (CTS) and the intracellular space of satellite terminal swellings (STS). One membrane surrounds each terminal swelling, and the other two are part of the encapsulating epidermal cell (see schematic in Fig. 9). ~ 8 6 , 0 0 0 .

Fig. 7 . The organization of the nerve terminals and epidermal cells at lower levels in the cell column. A: Section taken at a level just below that of Figure 6. At this level the area immediately below the nerve terminals is revealed, showing the dense network of tonofibrils (t) and keratohydine granules tk! that, is closely associated with the lower part of the nerve terminals. The nucleus of the encapsulating epidermal cell (nj can he seen in several areas of the section. Desmosomes (d! are visible at the boundary between the cell culurnn and the stratum corneum (SC). Arrows mark the presumptive location where the

plasma membrane of the encapsulating epidermal cell meets itself after it has wrapped around the central terminal fiber (cnf ) as in Figure 5A. ~9,000. B: A portion of the lower tier of terminal swellings (cts, sts) is visible in the middle of the section. whereas the seven satellite fibers (arrows1 continue upward to form the upper tier of swellings seen in Figure 6. A circle of electron-dense keratohyaline granules (kJ and tonofibrils are visible close to the nerve fibers. The approximate level of this section is show on the schematic in Figure 2. X 7,000.

352 K.C. CATANIA

Fig. 8. Nerve terminals encapsulated by epidermal cells below the stratum corneum (vertical section, see Fig. 2 for location). A: The central terminal swelling (CTS) encapsulated by an epidermal cell lies immediately below the fully keratinized cells of stratum corneum (SC). In the overlying keratinized cell, there is a remnant of the central terminal swelling (r) that contains degenerated mitochondria. These features suggest that the nerve terminal is maintained in a superficial location, even as the epidermal cells join the stratum corneum. ~ 2 0 , 0 0 0 . B: Lower magnification of a region similar to A shows the

stimulation. Thus there does not appear to be an area that is solely responsive to a non-tactile modality such as electroreception. However, it remains possible that Eimer’s organs are responsive to non-tactile stimuli, such as tem- perature, given the superficial location of the terminal swellings.

How do Eimer’s organs function to detect mechanical stimuli? In the absence of physiological recordings from single derents , the function of the individual sensory structures within Eimer’s organ cannot be determined with certainty. However, it seems likely that the encapsulated corpuscle and Merkel-like complex at the base of Eimer’s organ are rapidly adapting and slowly adapting mechanoreceptors, respectively, as has been found for similar structures in other species (Loewenstein, 1966; Iggo and Muir, 1969; Catton, 1970; Andres and von During, 1973; Pubols et al., 1973; Hunt, 1974). Both of these structures, as well as the terminal swellings within the cell column, are arranged so as to be compressed by pressure on the cell column. Because the terminal swellings below the stratum corneum are located directly below the central circular disk at the apex of the cell column, they are especially well positioned to be compressed by the slightest contact with surfaces in the mole’s environment.

In slow-motion macrovideo recordings, star-nosed moles can be seen repeatedly pulling back the appendages and then quickly swinging them forward into contact with the substrate as they search for food (unpublished observa- tions). This behavior is repeated at a rate of 10 times per second, each touch occurring at a different location in the environment. Such behavior supports the proposal that compression of the cell column occurs to stimulate the sensory receptors. A similar mode of function has been

central terminal swelling (CTS) and the overlying layers of stratum corneum. The uppermost keratinized cell lies on the outer skin surface and corresponds to the circular disk visible on the exterior or Eimer’s organ (Fig. 10. The arrow points out a weak area in the keratinized cell, caused by the inclusion of the degenerated nerve terminal. corresponding in location to the dimple on the outer surface of Eimer’s organ (arrow in Fig. 1C). Note the electron-dense appearance of the opposed plasma membranes in the stratum corneum, characteristic of a glycolipid layer deposited to form a water barrier. x 10,500.

suggested for the push-rod mechanoreceptors that are found on the snout of the echidna and the duck-billed platypus (Andres and von During, 1990). Although moles and monotremes are distantly related species, the push-rod and Eimer’s organ are remarkably similar in structure.

Why does the star-nosed mole haue a “star”and smaller, more organized Eimer’s organs than those of other mole species? Eimer’s organs are a specialization of the epidermis, which has the important function of protecting underlying tissues from desiccation and abrasion. The appendages of the star-nosed mole contain highly vascular tissue and have a high surface area-to-volume ratio. In addition,

Fig. 9. Schematic representation of the nerve terminals and their relationship to the epidermal cells of the column. A The hub-and-spoke arrangement of nerve terminals at the apex of the cell column. In this example, eight satellite terminal swellings surround a single central terminal swelling. The entire complex is encapsulated by a single epidermal cell. This pattern is repeated at lower levels in each Eimer’s organ. Note that actual tissue sections cannot reveal the entire terminal complex as illustrated, owing to the concave shape of the structure in the horizontal plane (see Fig. 2). B: Schematic of the terminal swellings showing the two membranes that surround each nerve terminal. Each nerve terminal is surrounded by its own plasma membrane, which is adjacent to the membrane of the encapsulating epidermal cell. This results in the presence of four plasma membranes between any two nerve terminals (as seen in Fig. 6C). The satellite nerve fibers descend through the margins of the cell column (F). C: Vertical orientation showing two successive levels of terminal swellings derived from a single satellite nerve fiber (F), as they terminate adjacent to the central terminal swellings. Each level of terminal swellings forms within a single epidermal cell at the top of the cell column (same orientation as schematic in Fig. 2). SC, stratum corneum; cts, central terminal swelling; sts, satellite terminal swellings.


Figure 9

the Eimer’s organs on the surface of these appendages have a relatively thin stratum corneum. There are often only six or seven cells of stratum corneum overlying the nerve terminals and living epidermal cells, which means there is a space of only 5-6 pm between the external environment and the living tissues. Although a thin stratum corneum may greatly enhance the sensitivity of the structures to mechanical stimuli, it also means that the nasal appendages and the Eimer’s organs of the star-nosed mole are very delicate structures.

The star-nosed mole is the only mole that lives in wetlands and digs in mud (Yates and Pedersen, 1982). Although all talpid moles have a highly specialized glabrous snout, comparisons between the Eimer’s organs of the star-nosed mole and those of other mole species, which live in drier soil, suggest that the environmental constraints imposed on the nasal epidermis by the abrasion and desiccation in most soil environments have been greatly lessened in the wetland habitat of the star-nosed mole (Catania, 1995a). This may have allowed for the elaboration of the appendages and the refinement of the Eimer’s organs. Since the Eimer’s organs form the fundamental receptor unit on the nose, their small size, and hence higher density per unit area, may increase the tactile acuity of the nose in the case of the star-nosed mole, whereas at the same time the greater surface area of the appendages allows for more area of the environment to be explored with each touch.

ACKNOWLEDGMENTS Special thanks go to Tom Deerinck and Grace Kennedy

for assistance in preparing and sectioning material for electron microscopy. This work was conducted with the aid of the San Diego Microscopy and Imaging Resource. Thanks are due to Glenn Northcutt and Jon H. Kaas for their support and advice during many phases of this research. Supported by NIH Grants NS16446 to J. Kaas and NS 09857-01 to K. Catania.

LITERATURE CITED Andres, K.H., and M. von During (1973) Morphology of cutaneous receptors.

In A. Iggo (ed): Handhook of Sensory Physiology, Vol. 2. New York: Springer, pp. 3-28.

Andres, K.H., and M. von During (1988) Transdudion and cellular mecha- nisms in sensory receptors. In W. Hamann and A. Iggo (eds): Progress in Brain Research. New York: Elsevier Science Publishers, pp. 113-131.

Andres, K.H., and M. von During (1990) Comparative and functional aspects of the histological organization of cutaneous receptors in vertebrates. In 2. Wolfgang and L.W. Neuhuber (eds): The Primary Afferent Neuron. New York: Plenum Press, pp. 1-17.

Catania, K.C. 11995a) A comparison of the Eimer’s organs of three north American moles: i,he hairy-tailed mole V‘arascalops breweri), the star- nosed mole (Condylura cristata) and the castcrn mole (Scalopus aquati- cusj. J. Comp. Neurol. 354:150-160.

Catania, K.C. (1995h) The structure and innervation of the sensory organs on the snout of the star-nosed mole. J. Comp. Neurol. 351536-548.

Catania, K.C. (1995~) Magnified cortex in star-nosed moles. Nature 375:453- 454.

Catania, K.C., and J.H. Kaas (1995) The organization of the somatosensory cortex of the star-nosed mole. J. Comp. Neurol. 351:549-567.

Catania, K.C., J.H. Kaas, R.G. Northcutt, and P.D. Beck (1993) Nose stars and brain stripes. Nature 364t493.

Catton, W.T. (1970) Mechanoreceptor function. Physiol. Rev. 50:297-318. Eimer, T. (1871) Die schnauze des maulwarfes als tastwerkzeuf. Arch.

Giacometti, L., and H. Machida (1965) Thr. skin of the mole (Seapanus

Gould, E., W. McShea, and T. Grand (1993) Function of the star in the

Mikrosk. Anat. 7t181-191.

townsendzc). Anat. Rec. 253:3140.

star-nosed mole, Condylura cnstata. J. Mammal 74:108-116.

354 K.C. CATANIA

Gregory, J.E., A. Iggo, A.K. McIntyre, and U. Proske (1987) Electroreceptors in the platypus. Nature 326:38&388.

Gregory, J.E., A. Iggo, A.K. McIntyre, and U. Proske (19881 Receptors in the hill of the platypus. J. Physiol. (Lond.) 400:349-366.

Halata, Z. (1972) Innervation der unbehaarten nasenhaut des maulwurfs (Talpa europaeu). Z. Zellforsch. 125:108-120.

Halata, Z. 11990) Sensory innervation of the hairless and hairy skin of mammals including humans. In Z. Wolfgang and L.W. Neuhuber (eds): The Primary Afferent Neuron. New York: Plenum Press. pp. 19-34.

Hunt, C.C. (1974) The Pacinian corpuscle. In J.I. Hubbard (ed): The Peripheral Nervous System. New York: Plenum Press, pp. 405420.

Iggo, A,, and A.R. Muir (1969) The structure and function of a slowly adapting touch corpuscle in hairy skin. J. Physiol. (Land.) 200:763-769.

Iggo, A,, U. Proske, A.K. McIntyre, and J.E. Gregory (1988) Cutaneous electroreceptors in the platypus: a new mammalian receptor. In W. Ilamann and A. Iggo (eds): Progress in Brain Research. Amsterdam: Elsevier Science Publishers, pp. 133-138.

Loewenstein, W.R. (1966) Input and output ends of a transducer process. In A.V.S. De Reuck and J. Knight (eds): Touch, Heat, and Pain: Ciba Foundation Symposium. London: Churchill, pp. 18&201.

Munger, B.L. (1965) The intraepidermal innervation of the snout of the opossum. J. Cell Biol. 26:79-97.

Munger, B.L., and C. Ide (1988) The structure and function of cutaneous sensory receptors. Arch. Histol. Cytol. 51:l-34.

Pernetta, J.C. (1977) Anatomical and behavioral specializations of shrews in relation to their diet. Can. J. Znol. 55:1442-1453.

Puhols, B.H., P.J. Donovick, and L.M. Pubols (1973) Opossum trigeminal afferents associated with vihrissae and rhinarial mechanoreceptors. Brain Behav. Evoi. 7t360-381.

Quilliam, T.A. (1966) The mole’s sensory apparatus. J. Zool. (Lond). 149:76-88.

Quilliam, T.A. (1980) Nerve fibers and free nerve endings in the epidermis of seven mammalian and one reptilian species. In R.I.C. Spearman and P.A. Riley (eds): The Skin of Vertebrates. London: Academic Press, pp. 293-301.

Richard, P.B. 11985) The sensorial world of the Pyrenean desman, Galernys pyrenuicus. Acta Zool. Fennica. 173:255-258.

Schcich, H., G. Langner, C. Tidemann, R.B. Coles, and A. Guppy (1986) Electroreception and electrolocation in platypus. Nature. 31 9:401402.

Shibanai, S. (1988) Ultrastructure of the Eimer’s organs of the Japanese shrew mole, Umtrichus talpoides (Inseetivora, Mammalia) and their changes followinginfraorbital axotomy. Anat. Anz. 165:105-129.

Van Vleck, D.B. (1965) The anatomy of the nasal rays of Condyluru cristatu. J. Mammal 46:24&253.

Yalden, D.W. (1966) The anatomy of mole locomotion. J. Zool., Lond. 149:55-64.

Yates, T.L., and R.J. Pedersen (1982) Moles. In J.A. Chapman and G.A. Feldhamer (eds): Wild mammals of North America. Baltimore: Johns Hopkins University Press, pp. 37-51.

Zakon, H.H. (1986) The electroreceptive periphery. In R.G. Northcutt ted): Electroreception. New York: John Wiley and Sons, pp. 103-156.

Ultrastructure of the Eimer's organ of the star-nosed mole

Documents

Transcript of Ultrastructure of the Eimer's organ of the star-nosed mole