&p.1:Abstract The sensory innervation of the hard palate ofthe rhesus monkey was studied by light and electron mi-croscopy. The mucosa of the hard palate is subject to aparticularly heavy mechanical load requiring functionalspecialisation of the horny epithelium in the form ofthickenings – the papilla incisiva and eight pairs of rugaepalatinae. A thin layer of firm connective tissue (laminapropria) attaches the mucosa to the periost of the hardpalate. Sensory nerve fibres were found most abundantlyin the papilla incisiva and first rugae palatinae. Theirnumber decreases in an aboral direction. Five types ofsensory nerve endings were found. Free nerve endingswere ubiquitous in the epithelium and lamina propria.Merkel nerve endings were found in the basal layer ofthe epithelium of the papilla incisiva and rugae palatinae.Meissner corpuscles were located in the connective tis-sue between epithelial pegs, while lamellated corpuscleswere seen below the epithelial pegs. Ruffini corpuscleswere found in the deeper layer of the lamina propria.Thus, a variety of sensory nerve endings were found inthe hard palate, especially in those areas that are in closecontact with the tongue during chewing of food. Thisrich innervation suggests an important role in monitoringthe mechanical properties of food and the position of thetongue.

&kwd:Key words Mechano-receptors · Palate · Merkel cell ·Ruffini corpuscle · Free nerve ending · Lamellatedcorpuscle · Meissner corpuscle&bdy:

Introduction

Parts of the oral mucosa are exposed to a particularlyheavy mechanical load. In those areas the mucosa has a

horny epithelium with a firm underlying connective tis-sue (lamina propria). This type is termed masticatorymucosa and can be found in the gingiva and hard palate.In the palate, the mucosa forms macroscopically visiblethickenings: a papilla incisiva and several pairs of rugaepalatinae. Food is pressed with the tongue against theseregions to check its mechanical properties and monitorwhether it is ready for swallowing. For this complexfunction, the mucosa of the hard palate and papilla incis-iva needs to be well equipped with mechanoreceptors.

Following early light microscopic studies of the hu-man palate by Gairns (1955), various investigators havecarried out electron microscopic studies on the innerva-tion of the papilla incisiva in smaller mammals: rat (Yehand Byers 1983; Byers and Yeh 1984; Chan and Byers1985; Watanabe and Konig 1986), squirrel monkey(Garant et al. 1980), mouse (Watanabe and Yamada1988; Tachibana et al. 1990). However, this is the firstsuch investigation carried out in a larger primate (Rhesusmonkey) with intact connection to the underlying bonein order to study the topographic arrangement of thesemechanoreceptors in situ. This study provides evidencefor a rich supply with free nerve and Merkel nerve end-ings, and Ruffini, Meissner and lamellated corpuscles inthe primate hard palate that are likely to play an impor-tant role in monitoring mechanical properties of food.

Materials and methods

Two adult Rhesus monkeys were killed with an overdose of thio-pental and perfused with 6% glutaraldehyde in 0.05 M phosphatebuffer via the left cardiac ventricle. The upper jaw and hard palatewere removed from the animals and postfixed for several days inthe same solution. The tissue was then decalcified by storing in5% EDTA solution with 0.1 M sodium phosphate buffer (pH 7.4,room temperature) for 5 years. The solution was changed everymonth. The state of decalcification was checked regularly by me-chanical probing and by X-ray just before embedding.

Following decalcification the hard palate was cut into 1.5-mm-thick strips, and each strip was divided into 20 sections from theoral to the aboral end, resulting in several thousand blocks of tis-sue. These blocks were postfixed in 1% OsO4 in 0.1 M sodium

Z. Halata (✉) · K.I. BaumannDepartment of Functional Anatomy, Institute of Anatomy,University Hospital Hamburg- Eppendorf, Martinistrasse 52,D-20246 Hamburg, Germanye-mail: kbaumann@uke.uni-hamburg.de,Fax: +49-40-4717-2845&/fn-block:

Anat Embryol (1999) 199:427–437 © Springer-Verlag 1999

O R I G I N A L A RT I C L E

&roles:Z. Halata · K.I. Baumann

Sensory nerve endings in the hard palateand papilla incisiva of the rhesus monkey

&misc:Accepted: 30 September 1998

phosphate buffer with 1% sucrose at pH 7.4 for 2 h before embed-ding in gycidether 100.

Serial semithin sections obtained from these blocks were stainedaccording to Laczko and Levai (1975) and examined by light mi-croscopy. Selected semithin sections were re-embedded, cut into ul-trathin sections and contrasted with 1% uranyl acetate and 1% leadcitrate (Reynolds 1963) for electron microscopy (Philips 300).

Results

In the Rhesus monkey, the mucosa of the hard palate iscovered by a multilayered, horny, flat epithelium firmlyconnected with the periost through the lamina propria.The whole mucosa has a thickness of 2.5 to 3 mm. Inthis location, the epithelium has no stratum granulosum.The front part behind the processus alveolaris is thick-ened to form the papilla incisiva, behind which eight ru-gae palatinae are located (Fig. 1).

Epithelial thickenings (pegs) reach into the laminapropria to different degrees. In the papilla incisiva and

rugae palatinae these pegs are especially thick and well-developed. The lamina propria consists of a superficiallayer facing the epithelium, forming a negative of theepithelial form – thinner below the epithelial pegs andprotruding between them. By analogy to the nomencla-ture of the skin this could be called the papillary layer.The deeper layer consists of dense connective tissue withsome seromucous salivary glands. This layer is firmly at-tached to the periost of the hard palate, allowing minimalmovement against each other.

Five types of sensory nerve endings were found:

1. Free nerve endings within the epithelium and the su-perficial layer of the lamina propria (Figs. 2, 3, 6–8)

2. Merkel nerve endings in the bases of epithelial thick-enings (Figs. 4, 5)

3. Ruffini corpuscles in the deeper layer of connectivetissue about 250–400 µm below the basement mem-brane of the epithelium (Figs. 9–11).

4. Meissner corpuscles in the lamina propria close tothe epithelium between the epithelial thickenings(Figs. 12–14)

5. Small lamellated corpuscles below the epithelial thick-enings (Figs. 15, 16)

Sensory receptors in the epithelium

Free nerve endings

Intraepithelial free nerve endings are supplied by thinlymyelinated (A) afferent axons with diameters of 1–2 µmand characterised by accumulation of mitochondria.Their number is highest at the papilla incisiva and de-creases in the aboral direction. They can be found in thestratum spinosum and in the stratum basale. After losingtheir myelin sheath in the lamina propria the nerve fibrespenetrate the basal lamina. The first type branches toform enlarged nerve terminals between keratinocytes ofthe stratum spinosum (Figs. 2, 3).

A second type of intraepithelial free nerve ending isseen just above the basal lamina in direct contact withcells of the stratum basale (Fig. 6).

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Fig. 1 Schematic drawing of the monkey palate with papilla incis-iva (IP) and eight pairs of rugae palatinae. The surrounding teethare marked as incisors (I1 and I2), caninus (C), premolars (P1 andP2) and molars (M1 to M3). ×1&/fig.c:

Fig. 2 Free nerve ending in the papilla incisiva. The enlargednerve terminal (★) is located in the statum spinosum of the palateepithelium, showing the characteristic accumulation of mitochon-dria. ×7600&/fig.c:

Fig. 3 Detail view of a free nerve ending (★) located between ke-ratinocytes of the stratum spinosum. Multiple desmosomal junc-tions between keratinocytes are indicated by arrows. ×17000&/fig.c:

Fig. 4 Epithelium of the papilla incisiva. Merkel cells (M) withcytoplasmic protrusions (★) are seen in the stratum basale. Theyare connected with the surrounding keratinocytes by desmosomes(arrows). Nerve terminals (T) are associated with the Merkel cellson their labial side. In the lamina propria an afferent axon (N) withsheath of peripheral glial cells can be seen. ×7600&/fig.c:

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Fig. 5 Merkel cells (M) with cytoplasmic protrusions (arrows) inthe papilla incisiva. Nerve terminals (★) are on the labial side ofthe Merkel cells. ×5400&/fig.c:

Fig. 6 Two types of free nerve endings in the basal layer of theepithelium and the lamina propria of the papilla incisiva, respec-tively. The first one (arrow) is located just above the basal laminamaking direct contact with the keratinocytes of the stratum basale.The second is formed by a bundle of nerve terminals (★) andmostly covered by terminal glial cells. Both types contain accumu-lations of mitochondria. ×5400&/fig.c:

Fig. 7 Free nerve ending (★) surrounded by a simple sheath ofterminal glial cells (S) and amorphous electron dense material.Two or three layers of perineural cells (P) encapsulate the com-plex. ×3200&/fig.c:

Fig. 8 Bundle of free nerve endings in the lamina propria belowthe epithelium of the first ruga palatina. Terminals (arrows) can berecognized by their accummulation of mitochondria. They arecovered by terminal glial cells with their basal lamina. ×5400&/fig.c:

Fig. 9 Ruffini corpuscle in the lamina propria of the second rugapalatina in cross section. The corpuscle consists of nerve terminals(arrows) sheathed by terminal glial cells anchored between bun-dles of collagen fibres. Thin lamellae of perineural cells (C) formcylinders separating the nerve terminals from the surrounding con-nective tissue. The nerve terminals are supplied by myelinated ax-ons (A) with a diameter of about 3 to 5 µm. ×3250&/fig.c:

Fig. 10 Oblique section of a cylinder from a Ruffini corpuscle inthe lamina propria of the second ruga palatina. Nerve terminals areindicated by arrows. ×3250&/fig.c:

Fig. 11 Detail of nerve terminals from a Ruffini corpuscle. Nerveterminals are partly sandwiched between thin lamellae of terminalglial cells (★) leaving parts of the axolemma (arrows) in directcontact with the basal lamina and collagen fibrils. ×14500&/fig.c:

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Merkel nerve endings

The basal layer of the epithelial thickenings containsMerkel nerve endings. Their number depends on thethickness of the epithelial pegs. In larger pegs up to 12Merkel nerve endings can be found. In smaller onesthere may be only individual Merkel nerve endings. EachMerkel nerve ending consists of a Merkel cell and a dis-coid nerve terminal. The Merkel cells are oval in shapewith the long axis oriented perpendicularly to the mucos-al surface. Their nuclei are lobulated and contain typicaldense core granules in that part of the cytoplasm facingthe nerve terminal. Desmosomal contacts with the sur-rounding keratinocytes are often seen. Between thesecontact sites protoplasmic protrusions extend either be-tween or are invaginated into neighbouring keratinocytes(Figs. 4, 5). The discoid nerve terminals are oriented par-allel to the longitudinal axis of the Merkel cells facingtheir labial side and are characterised by accumulation ofmitochondria. Synapse-like contacts can be seen be-tween the axolemma of the nerve terminal and the cyto-plasmic membrane of the Merkel cell (Fig. 4). Afferentaxons are myelinated with diameters of 4–5 µm. Afterlosing their myelin sheath the branches form terminalsinnervating up to 6 Merkel cells.

Sensory receptors in the lamina propria

Free nerve endings

Two types of free nerve endings can be found innervatedby thinly myelinated (Aδ-) and unmyelinated (C-) fibres.The endings of Aδ-fibres show typical thickenings andare only partly covered by processes of the terminal glialcell (Fig. 6). Very rarely they are embedded by masses ofbasal lamina-like material and wrapped within a perineu-ral capsule, resembling a very simple corpuscle (Fig. 7).The endings of unmyelinated fibres form groups of ter-minals (Fig. 8). The terminals are thin and covered byprocesses of the terminal glial cells. Only in serial sec-

tions can they be clearly recognised as terminals ratherthan passing axons.

Ruffini corpuscles

Ruffini corpuscles are found in the lamina propria of thepapilla incisiva and rugae palatinae (Figs. 9, 10). Theyare cylindrical in shape. The capsules of the cylinders areformed by flat perineural cells with both ends open. Col-lagen fibres of the lamina propria enter via these endsand run through the length of the cylinder to leave at theother end. These fibres are compartmentalised by thin la-mellar cells. The afferent axons are thick myelinated fi-bres (Aβ) with diameters of about 5 µm (Fig. 9) penetrat-ing the capsule at the long side of the cylinder. The peri-neurium of the nerve blends with the capsule of the cor-puscle. Within the cylinder the axon loses the myelinsheath and branches into several terminals. Each termi-nal is partly sandwiched between thin lamellae of termi-nal glial cells. Parts of the axolemma and sometimesslim processes are in direct contact with the basal laminaof the glial cell and collagen fibrils (Fig. 11). Sometimesseveral Ruffini corpuscles could be seen close together,oriented in different directions following the direction ofthe collagen fibre bundles.

Meissner corpuscles

Meissner corpuscles are located in the connective tissuebetween the epithelial pegs in the papilla incisiva andfirst two rugae palatinae and are supplied by one or twomyelinated afferent axons with diameters of 4–5 µm.Their size increases with the thickness of the papillarylayer of the lamina propria. They consist of several flat-tened nerve terminals surrounded by 1–5 flat cytoplas-mic lamellae of terminal glial cells. They lack a perineu-ral capsule and are generally located so close below theepithelium that the basal lamina of the terminal glial cellblends with the basal lamina of the epithelium (Fig. 12).The nerve terminals have a discoid shape oriented in par-allel to the epithelial surface. They resemble a stack ofcoins with lamellae of the terminal glial cell and materialof connective tissue between them (Figs. 13, 14). The cy-

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toplasm and nuclei of the glial cells are usually at theside of this stack.

Lamellated corpuscles

Small lamellated corpuscles are found individually orgrouped mostly in the connective tissue of the papilla in-cisiva. Occasionally they can be seen below the epitheli-um of the first two rugae palatinae. In contrast toMeissner corpuscles they are located well below the epi-thelial pegs, without direct contact to the basal lamina,and possess a thin capsule of two or three layers of peri-neural cells. Their longitudinal axis runs parallel to themucosal surface.

The lamellated corpuscles consist of a nerve terminal,an “inner core” and a capsule (Fig. 15). In the centre of

the two symmetric halves of the inner core, formed bythin cytoplasmic processes of a pair of terminal glialcells covered by basal laminae, is an oval shaped nerveterminal. Longitudinal clefts filled with basal membranematerial can be seen between the halves (Fig. 16). Theslim ends of the oval nerve terminal are oriented towardsthe clefts. The corpuscle is innervated by a myelinatedafferent axon of about 5 µm diameter. After losing themyelin sheath the unmyelinated terminal axon maybranch before forming the nerve terminals.

Discussion

The present study confirms that in primates a great vari-ety of sensory nerve endings can be found in the masti-catory mucosa that are likely to play an important role inchecking the food during the chewing process. This is inline with previous findings in smaller mammals. Wefound two morphologically distinct types of free nerveendings in the epithelium and two in the underlying con-nective tissue, Merkel cell nerve endings at the bases ofepithelial thickenings, Ruffini corpuscles in the deeperlayer of the lamina propria, Meissner corpuscles in thelamina propria with close contact to the basal lamina ofthe epithelium, and small lamellated corpuscles in theconnective tissue of the lamina propria. This suggests a

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Fig. 12 Small Meissner corpuscle in the lamina propria just be-low the epithelium. The basal lamina of the glial cell blends withthe basal lamina of the epithelium (arrow). Discoid nerve termi-nals (★) are surrounded by thin cytoplasmic processes of the ter-minal glial cell (S). ×5400&/fig.c:

Figs. 13, 14 Larger Meissner corpuscles in the lamina propria ofthe papilla incisiva. They are located so close to the epitheliumthat the basal laminae blend. Each corpuscle consists of flat nerveterminals (★) and terminal glial cells (S) with its thin cytoplasmicprocesses both running parallel to the epithelial surface. ×5400&/fig.c:

Fig. 15 Group of small lamel-lated corpuscles from the lami-na propria of the papilla incis-iva. In contrast to the Meissnercorpuscles shown in Figs. 11 to13 they are about 20 µm belowthe basal lamina and are encap-sulated by thin perineural cells(C). In the centre of the innercore formed by thin lamellae(L) of terminal glial cells is thenerve terminal (★). The sup-plying myelinated axon has adiameter of about 4 µm. ×2500&/fig.c:

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high degree of specialisation of the various types ofmechanoreceptors for different parts of the sensory pro-cess involved in masticatory control.

Free nerve endings

Free nerve endings were found in large numbers in thepapilla incisiva, with decreasing numbers in the aboraldirection. They are particularly concentrated in the ele-vated parts of the mucosa (papilla incisiva and rugaepalatinae). In the mucosa between the elevated parts onlya few free nerve endings can be seen. Two types withdifferent characteristics and location were seen in theepithelium. Those in the stratum spinosum were simpleenlargements of the peripheral end of the thinly myelin-ated afferent nerve fibre. In contrast, the second type waslocated exclusively in the stratum basale, making directcontact with keratinocytes containing accumulations ofmitochondria. In the skin, this type is believed to havemainly thermoreceptive functions (Hensel 1973), andthis is likely to be the case in the oral mucosa as well.However, we are not aware of studies employing electro-

physiological recordings from such receptors. Thosenerve endings in the stratum spinosum were described asprobable mechanoreceptors (Munger 1965) but may alsoact as polymodal nociceptors. In addition to those in theepithelium, in the lamina propria also two types of freenerve endings could be distinguished. Nerve endings ofafferent C-fibres showed minimal terminal enlargement,appearing in groups wrapped by processes of the termi-nal glial cell. Thus, in order to be sure that these wereendings rather than passing nerve fibres, serial sectionshad to be examined. In contrast, nerve endings of thinlymyelinated fibres had clear terminal enlargements andwere only partially covered by processes of the terminalglial cells. Functionally, the free nerve endings in theconnective tissue are most likely polymodal nociceptors(Kruger et al. 1981; Kruger and Halata 1996). However,some of the free nerve endings in the connective tissuemay be efferent autonomic fibres involved in vasomotorcontrol.

Merkel nerve endings

Merkel nerve endings were found in large numbers inepithelial pegs throughout the hard palate. All Merkelcells found in this study were in contact with nerve ter-minals. It is striking that the location of Merkel cells inrelation to the nerve terminals seems to depend on the di-rection of the mechanical stimulus to be perceived. In theskin, the long axis of Merkel cells runs parallel to thesurface of the epidermis with the nerve terminal directed

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Fig. 16 Detail of an inner core from a small lamellated corpusclein the lamina propria of the papilla incisiva. In the centre of the in-ner core is the nerve terminal (★) with mitochondria. Pairs of ter-minal glial cell (S) with thin cytoplasmic processes (L) and basallamina form one half of the inner core, each separated by a longi-tudinal cleft (arrow) with collagen fibrils. A thin capsule (C) sur-rounds the inner core of the corpuscle. ×7360&/fig.c:

towards the basal lamina (Halata 1975; Halata 1993). Insinus hairs their long axis is parallel to the hair shaft,with the nerve terminal away from the basal lamina(Halata and Munger 1980). In the monkey hard palate,the alignment is perpendicular to the epithelial surfacewith the nerve terminal on the labial side of the Merkelcell, suggesting an optimal arrangement for the percep-tion of shear forces applied by the tongue. In contrast, inthe large papilla incisiva of the goat (lacking incisorteeth) Merkel cells and nerve endings are arranged paral-lel to the mucosal surface as in the skin (Schwegmann etal. 1993).

Merkel cell receptors are known to have slowly adapt-ing responses monitoring punctuate pressure (Iggo andMuir 1969). Characteristic features of Merkel cells haveled to the hypothesis that the Merkel cell acts as a mech-anoelectric transducer employing synaptic transmissionto the nerve terminal (Iggo and Findlater 1984). Thesefeatures could also be seen in the present study: proto-plasmic protrusions extending between or invaginatinginto neighbouring keratinocytes, dense core granules andsynapse-like contacts. However, there is still controversyabout the precise role of Merkel cells within the mech-ano-electric transduction process (Mills and Diamond1995; Ogawa 1996; Senok et al. 1996; Senok andBaumann 1997). In contrast to findings by Tachibanaand her group (Tachibana et al. 1991; Tachibana et al.1997; Tachibana et al. 1998), we could not find evidencefor the presence of so called “transitional” Merkel cellswithout contact to nerve terminals. All Merkel cellsfound in our study had contact with nerve terminals.

Ruffini corpuscles

Ruffini corpuscles were found in the deeper layer of thelamina propria of the papilla incisiva and rugae palati-nae. They are specially designed to monitor stretch andcan be found ubiquitously in the connective tissue under-lying the mucosa and skin or in joint capsules. The nerveterminals are always adjusted to the structure of the sur-rounding tissue. Larger accumulations of nerve terminalsare often wrapped by a capsule consisting of either fibro-blasts or perineural cells (Halata 1988). In contrast, Ruf-fini corpuscles in the periodontium of teeth (Itoh et al.1981; Byers 1985; Millar et al. 1989) and those associat-ed with hairs (Halata and Munger 1980) mainly lacksuch a capsule, which appears to have no effect on theirfunction. They respond with a slowly adapting nerve dis-charge (Chambers et al. 1972). The connection with bun-dles of collagen fibres of the lamina propria makes themideally suited for this task. In contrast to Ruffini corpus-cles found in joint capsules (Halata 1988), those in theoral mucosa and in the periodontium have a thin perineu-ral capsule that is lacking completely in some places.The usual spindle shape of Ruffini corpuscles is morediscoid in the palate. In view of the rather thin layer offirm connective tissue between the mucosa and bone ofthe hard palate (2.5 to 3 mm) any movement within this

layer is likely to be fairly limited. The presence ofRuffini corpuscles in this location suggests that shearforces do result in lateral movement of the mucosaagainst the hard palate of such dimensions that it needsto be monitored. The ultrastructural differences betweenRuffini corpusles in the connective tissue of the hard pal-ate and those in the locomotion apparatus may be an ad-aptation to the kind of shear forces occurring in this lo-cation.

Meissner corpuscles

Meissner corpuscles were found only in the papilla incis-iva and the first two rugae palatinae. They are located inthe lamina propria just below the basal lamina betweenthe epithelial pegs and do not possess a perineural cap-sule. Their size depends on the height of the neighbour-ing epithelial pegs. They are always supplied by one sin-gle axon, in contrast to those in skin of the monkey fin-ger tip, which can have up to three supplying nerve fi-bres and an egg-cup shaped perineural capsule in thelower part (Halata 1993). In the skin they function asrapidly adapting mechanoreceptors (Cauna 1956; Iggoand Andres 1982) monitoring changes in pressure. It islikely that the response characteristics are the same inthis location. The positioning just below the epitheliumand the orientation of lamellae parallel to the surfacemakes them ideally suited for the task of supplementingthe responses of slowly adapting receptors (i.e. Merkelnerve endings) to the level of pressure on the mucosawith additional and independent information about rapidchanges in pressure occurring during the chewing pro-cess.

Lamellated corpuscles

Lamellated or Pacini-like corpuscles were found in rath-er small numbers in the lamina propria, mainly in the pa-pilla incisiva. Often they were found in groups suppliedby one axon. Their longitudinal axis runs parallel to themucosal surface and the perineural capsule is thinnerthan in other locations (Zelena 1994). They are known tobe very rapidly adapting, especially suited for the per-ception of vibration stimuli (Loewenstein 1971). Closesimilarities exist to those described in the mucosa of thecat tongue (Spassova 1974), also called “Krause’s end-bulbs”.

The density of receptors in the mucosa of the hardpalate and in the papilla incisiva suggests that these dif-ferent receptors play an important role in sensing the me-chanical properties of food before swallowing as well asthe position of the tongue within the mouth. In man thelatter information is likely to be important for the articu-lation of speech. Usually such a rich supply of mechano-receptors is only found in the skin of the fingertips. Herethe active movement for the monitoring of surface prop-erties plays an important functional role. The hard palate

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does not move itself, but the movement of the tongue orfood along these receptors is recorded.

&p.2:Acknowledgements This study was supported in part by a grantfrom Deutsche Forschungsgemeinschaft (Ha 477/633/93). Wewish to thank Dr. Brian Cooper, Department of Oromaxillar Sur-gery, State University of Florida, Gainesville Fla., USA, for pro-viding the monkey palate. The excellent technical skills in prepar-ing the sections and photographs by Mrs. B. Knuts, Mrs. B. Lücht,Mr. S. Schillemeit and Dr. A. Spaethe is very much appreciated.We also wish to thank Mrs. M. Lück for the schematic drawing ofFig. 1.

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