Fine structure and innervation of the avian adrenal gland

Z. Zellforsch. 145, 557--575 (1973) © by Springer-Vcrlag 1973

Fine Structure and Innervation of the Avian Adrenal Gland III. Non-Chol inerg ic N e r v e F ibe r s*

K. Unsicker

Department of Anatomy, University of Kiel, Kiel, Germany (Head: Prof. Dr. Drs. h.c.W. Bargmann)

Received June 8, 1973

Summary. Apart from cholinergie nerve fibers, which make up the main part of efferent fibers to the avian adrenM gland (Unsickcr, 1973b), adrenergie, purinergie and afferent nerve fibers occur. Adrencrgic nerve fibers arc much more rare than eholincrgic fibers. With the FMek-Hillarp fluorescence method they can be demonstrated in the capsule of the gland, in the perieapsular tissue and near blood vessels. By their green fluorescent varicosities they may be distinguished characteristically from undulating yellow fluorescent ramifications of smM1 nerve cells which are found in the ganglia of the adrenal gland and below the capsule. The varicosities of adrencrgic axons exhibit small (450 to 700 A in diameter) and large (900 to 1300 A in diameter) granular vesicles with a dense core which is usually situated exccntri- cMly. After the application of 6-hydroxydopaminc degenerative changes appear in the varicosities. Adrcnergic axons arc not confined to blood vessels but can be found as welt in close proximity of chromaffin cells. Probably adrenergie fibers arc the axons of large ganglion cells which are situated mainly within the ganglia of the adrenal gland and in the periphery of the organ and whose dendritic endings show small granular vesicles after treatment with 6-OHDA.

A third type of nerve fiber is characterized by varicosities eontMning dense-cored vesicles with a thin light halo, the mean diameter (1250 A) of which exceeds that of the morphologi- eMly similar granular vesicles in cholinergic synapses. Those fibers resemble neurosecrctory and purinergic axons and are therefore called p-type fibers. They cannot be stained with chromMum-hematoxylinc-phloxinc. Axon dilations showing aggregates of mitochondria, myelin bodies and dense-cored vesicles of different shape and diameter are considered to be afferent nerve endings. Blood vessels in the capsule of the gland are innervated by both cholinergic and adrencrgie fibers.

Key words: Avian adrenal gland - - Adrenergic nerve fibers - - p-Type nerve fibers - - 6-Hydroxydopamine Fluorescence microscopy - - Electron microscopy.

Introduction

In a previous work (Unsieker, 1973b) it has been shown tha t adrenal chrom-

affin cells of birds, as well as those of mammals , (Feldberg and Minz, 1933;

Feldberg et al., 1934; Koelle, 1950; Coupland, 1965; Lewis and Shute, 1969) are

innerva ted by preganglionic sympathe t ic nerve fibers. Compared to our detai led

morphologicM, biochemical and pharmacological knowledge of the eholinergic

innerva t ion of the adrenal gland informat ion on non-cholinergic fibers to t h a t organ is much more scarce.

In their paper on the adrenal medulla of the hedgehog Bargmann and Lindner

(1964) give an i l lustrat ion of an axon (p. 902) which might be an adrenergie one.

Giordano-Lanza (1966) argues as well tha t adrenergic terminals occur in the

* Supported by a grant from the "Deutsche Forsehungsgemeinsehaft" (Un 34/1).

558 K. Unsicker

adrenal medulla. I n the course of an investigation of the inncrvat ion of the hamster adrenal cortex we observed green-fluorescent nerve fibers in the capsule of the gland and in the glomerulosa zone (Unsicker, 1969). Piezzi (1966) reported the occurrence of two types of synapse on the chromaffin cells of the toad 's adrenal gland, which, however, according to Coupland (1972), are likely to correspond to true synapses and preterminal regions of cholinergic nerves. Moreover, experiments by Halasz and Szent£gothai (1959) and Niijima and Winter (1968) indicate tha t the adrenal glands contain mechano- and chemoreceptors, but their morphological correlates have not been identified as yet.

Apar t f rom adrenergic and afferent fibers this publication deals with a type of nerve fiber, which is non-cholinergic and non-adrenergic and which strongly resembles the p- type fibers described by Baumgar ten et al. (1970) in the mammalian large intestine and purinergic nerves of several vertebrate organs (Burnstock, 1972).

Materials and Methods

1. Animals Studied (for number, sex, maturity, and date of fixation see Unsicker, 1973a). Domestic Fowl, Domestic Goose, Peking Duck, Larus ridibundus (Black-headed Gull), Larus argentatus (Herring Gull), Larus marinus (Black-backed Gull), Rissa tridactyla (Kitti- wake), Uria aalge (Guillemot), Domestic Pigeon, Corvus ]rugilegus (Rook), Corvus monedula (Jackdaw), Turdus merula (Blackbird), Sturnus vulgaris (Starling), Domestic Sparrow, Fringilla coelebs (Chaffinch).

2. Methods. Paraffin sections of adrenal glands of the Domestic Fowl, Duck, Black-headed Gull, Black-backed Gull, Kittiwake, Guillemot, Pigeon, Rook, Starling, Sparrow, and Chaffinch were stained with chromalum hematoxylin-phloxin according to Gomori-Bargmann.

Semithin sections of araldite-embedded material were stained with azure II-methyleneblue. Adrenal glands of the Domestic Fowl, Duck, Pigeon, Starling, Sparrow, and Chaffinch were

treated by Falck and 0wman's (1965) method for the detection of catecholamines. For details see Unsicker (1973a).

Electron microscopic demonstration of acetylcholinesterase: after Lewis and Shute (1966). Animals studied: Domestic Fowl, Rook. Experiments with 6-hydroxydopamine: see Unsicker (1973a).

Adrenal glands of all above mentioned species were studied under the electron microscope. The animals were perfused with Macrodex®, phosphate-buffered glutaraldehyde, and phosphate buffer, and postfixed in an aqueous 2% OsO4-solution. The sections were stained with uranyl acetate lead citrate and observed through a Siemens 101 or a Zeiss EM 9A. Further details see Unsicker (1973a).

Observations

Fluorescence Microscopy

With the Falck-Hillarp method fluorescent fibers can be observed mainly in the capsule of the gland or in close relation to it (Fig. 1). Within the gland they can be seen only exceptionally, for example around large blood vessels. I t cannot be excluded tha t the strong fluorescence of chromaffin cells suppresses the weak fluorescence of nerve fibers which possibly occur. Green and yellow fluorescent fibers can be discerned: green fluorescent varicosities from a sparse plexus in the capsule or in the pericapsular tissue and are concentrated in the neighbourhood of blood vessels. Yellow fluorescent fibers exhibit no varicosities and can be shown to represent processes of small intensively fluorescent ganglion cells which lie in the ganglia or are scattered beneath the capsule (Unsicker, 1973 a).

Innervation of the Avian Adrenal Gland 559

Fig. 1. Sturnus vulgaris. Fluorescence microscopic demonstration of catecholamines. Green fluorescent varicosities (]A) in the capsular tissue of the adrenal gland. Note the absence

of such axons within the organ (o)

Electron Microscopy

Among the axons, which make up the large nerve t runks of the adrenal g land (Unsicker, 1973b) and which, for the main par t , can be considered to be cho]inergie fibers can be found which give no posi t ive react ion to ac ty lehol ines terase and exhib i t cer ta in morphological features (Fig. 8) which dis t inguish t hem from eholinergic axons. Their size varies f rom 0.3-1 ~m, bu t i t can be shown on longi tud ina l sections t h a t t hey m a y sudden ly di la te up to a d iamete r of 2 ~m or even more. I n the course of the i r th in sections these axons m a y exhibi t an uneonspicuous inner s t ruc ture consist ing of tubules and f i laments . The varicosi t ies which are ra re ly found wi thin the large nerve t runks , bu t more often in re la t ion to endocrine cells (Fig. 2), regular ly conta in two popula t ions of dense-cored vesicles. The smal ler ones have a d iamete r of 450-700 ~ (mean d iamete r 580 A). W i t h i n the electron- dense core no s t ruc turM detai ls can be discerned. Often the dense core lies in an excentr ie posit ion. Clear vesicles of the same size occur. Larger dense-cored vesicles measure 900-1300 A. As in the smaller vesicles, thei r dense cores only somet imes fill out the space bounded by a un i t membrane comple te ly and uniformly. The out- line of the dense core is not sharp ly demarca ted . Mi tochondr ia of the varicosi t ies correspond to the er is ta- type . In the v ic in i ty of blood vessels varieosi t ies are ext rem- ly a b u n d a n t and voluminous. They can be observed there toge ther wi th axons which conta in typ ica l synap t ie vesicles only. However , varicosi t ies m a y also be s i tua ted close to adrena l chromaff in (Fig. 2) and interrenM cells (ef. Unsicker , 1973e). I n such posi t ions thei r satel l i te sheaths m a y be i n t e r rup t ed or d i sappear completely . F ibers of this t ype are pa r t i cu la r ly numerous in the herr ing gull and in the chaffinch.

Ano the r t y p e of nerve fiber which also differs f rom cholinergic fibers is com- monly observed in subcapsular regions of the avian adrena l gland. I t is charac te r ized by large varicosi t ies which measure up to 1.5 ~m and which exhib i t large round dense-cored vesicles wi th a mean d iamete r of 1250 A and a dense core of low or

38 Z. ZeUforsch., Bd. 145

560 K. Uns icke r

Fig. 2 a - - c


medium electron density (Fig. 3). As a rule, there is only a thin light halo between the dense center and the unit membrane. Sometimes these profiles also contMn small spherical vesicles, which resemble synaptic vesicles of cholinergic terminals, and mitochondria. These fibers which give no positive reaction to acetylcholinesterase can be observed close to capillaries, chromaffin (Fig. 8) and interrenal cells (cf. Unsieker, 1973e).

Final ly axon dilations have to be mentioned which are up to several tzm thick and which can develop out of axons with a normal inner structure (Fig. 6). They are characterized by numerous densely packed mitochondria and/or aggregations of myelin bodies and dense-cored vesicles. These formations can be regularly found in the connective tissue of the capsule and give a positive reaction to acetylcholinesterase (Fig. 5b). A positive reaction to acetylcholinesterase can also be observed in naked thin axons which are si tuated in large groups without any satellite sheath in the neighbourhood of adrenaline- and noradrenaline-storing cells (Fig. 7). The axons do not exhibit special terminals and contain only neurotubules.

After application of 6-hydroxydopamine (6-OHDA) the following alterations can be observed within varicosities showing two different populations of dense- cored vesicles: the small dense-cored vesicles increase in number, clear vesicles diminish (Fig. 5 a); membranes of mitochondria become more dense, and bizarre osmiophflic inclusions develop within the axoplasm (Fig. 2 c). 30 minutes after a single injection of 6 -OHDA the axoplasm shows severe destructions, myelin figures and vacuoles have formed; the mitochondria are swollen or incorporate an electron-dense material. Similar, but not so severe changes can be seen in the terminal portions of the dendrites of large ganglion cells (Unsicker, 1973a) where under normal conditions small t ranslucent vesicles occur (Fig. 4a, b). The other types of nerve fibers described above remain unaffected after 6-OE[DA-treatment.

Discussion

A. Adrenergie Fibers

Apar t f rom cholinergic axons which dominate in the avian adrenal gland (Unsicker, 1973 b) as well as in the mammal ian adrenal medulla (Coupland, 1965), fibers have been identified which, for several reasons, must be regarded as axons of adrcnergic neurons:

1. Varicosities containing two different kinds or granular vesicles have been found in m a n y organs which are innervated by postganglionic sympathet ic nerve fibers (Richardson, 1964; Taxi, 1965; Grillo, 1966: t t6kfelt , 1969; Tranzer st al , 1969; Baumgar ten et al., 1970; Geffen and Livett , 1971).

Fig. 2a--c. Adrenergie axons (aa) in the adrenal gland of (a) Fringilla coelebs, (b) Larus marinus, (c) Domestic Fowl (a and b: before 6-OHDA-treatment; c: after 6-OHDA- treat- merit), a) The adrenergic axon contains small and large dense-cored vesicles as well as some clear vesicles. Boutons of cholinergic axons (ca). Compare dense-cored vesicles in adrenergic and cholinergic nerve fibers! NoradrenMine (NA)-storing cell. b) Varicosities of adrenergic axons in con~ct with g chromaffin cell. c) Degeneration of adrenergic ~erminals after 6-

OKDA-treatment. × 18 000

38*

562 K. Unsicker

Fig. 3 Domest ic Fowl. p - type fibers (P). Dense-cored vesicles are significantly larger t h a n those in eholinergic axons. Note the voluminous axon dilations x I and x2! Chromaffin cell (A).

× 30 000


2. Electron microscopical and pharmacological investigations have shown that the small dense-cored vesicles, perhaps the large dense-cored vesicles of such varicosities as well, contain noradrenaline (for ref. see HSkfelt, 1968; Thoenen, 1969; Geffen and Livett , 1971).

3. 6-OHDA causes destructions of adrenergic terminals in the autonomic nervous system which can be compared to the alterations observed by us (Tranzer and Thoenen, 1967; Haeusler et al., 1969; Baumgarten et al., 1970; Furness et al., 1970; Jonsson and Sachs 1970; Thoenen, 1971). Under the electron microscope one notices at first an increase of granular vesicles; later typical degenerative changes, e.g. condensation of granular vesicles, increased density of the eristae mitochondriales and formation of myelin figures, develop (Thoenen and Tranzer, 1968; Tranzer and Thoenen, 1968; Devine, 1969; chicken: Bennett et al., 1970).

4. Under the fluorescence microscope eatecholamine-containing varicosities can be demonstrated in the capsule of the gland and close to blood vessels, that is to say, in such places, where 6-OHDA-affected axons are easily found. The failure to demonstrate adrenergic terminals with the Falck-Hillarp method in the surroundings of chromaffin cells may be explained by the intensive fluorescence of these elements.

Adrenergic terminals sometimes come into contact with chromaffin cells. Though the distance between nerve and endocrine cell is not larger than 200 A, synaptie membrane specializations do not occur, as is the rule in adrenergic synapses at smooth muscle and endocrine cells (Brettschneider, 1962; Grfllo and Palay, 1962; Richardson, 1962, 1964; Merillees et al., 1963; Theamert, 1963; Watari, 1968; Klein, 1971).

Exoeytosis of granular vesicles which has been suggested by biochemists (A.D. Smith etal . , 1970; A.D. Smith, 1971a, b) was not observed. However, we have to take into account that exocytosis is a rare event even in chromaffin cells of the adrenal medulla (Grynszpan-Winograd, 1971) or in the posterior lobe of the pi tui tary (Nagasawa, 1970; Krisch et al., 1972), and that adrenergic terminals are found comparably seldom in the avian adrenal gland. The number of adrenergic fibers seems to vary in different bird species. The large amount of adrenergic terminals in the adrenal gland of the chaffinch is striking, even more, because blood vessels with smooth muscle cells cannot be observed within the gland. This may be regarded as a hint that among all functions which could be speculatively ascribed to adrenal intraglandular adrenergic terminals the regulation of blood vessels does not need to be considered seriously. Which function these terminals really have is unknown as yet. One might speculate that they exert some influence on chemoreceptors which are sensitive to catecho]amines and which have heen neurophysiological]y demonstrated in the mammalian adrenal gland (Niijima and Winter, 1968a). However, a morphological correlate has not been found as yet with certainty (see below). A direct influence of adrenergic terminals on the storage and/or release of A and NA can hardly be imagined (for adrenergic terminals and interrenal cells see Unsicker, 1973 e).

For several reasons it seems logical to consider large sympathetic ganglion cells occurring in and around the avian adrenal gland (Unsicker, 1973a) to be the perikarya of adrenal adrenergic fibers:

1. Authors of former investigations on the innervation of the adrenal gland agree tha t these ganglion cells are the cell bodies of sympathetic neurons.

564 K. Uns icker

Fig. 4 a - - c

Innerva t ion of the Avian Adrenal Gland 565

Fig. 5. a) Domestic Fowl. Four adrenergic varicosities on a blood vessel of the capsule 30 min after an injection of 6-0HDA. Nearly all vesicles contain a dense core. Some mitoehondri~ (mi) show incorporations of an electron-dense material. ( ~ ) vaeuolization of the axoplasm. Smooth muscle cells (gin). b) Corvus /rugilcgus. Axon dilation, which probably represents an afferent ending, after demonstrat ion of acetylcholinesterase ( ~ ). The axon coutains

numerous eytosome-like particles, myelin bodies and clear vesicles. × 18000

Fig, 4a - -c . Periadrenal ganglia of (a) Domestic Fowl before 6-0HDA-trea tment . (b) Larus ridibundus 30 min after an injection of 80 mg/kg 6-OHDA. a) axodendritic synapse (ad) on the spine of a large dendrite (d). Within the spine small clear vesicles can be seen ( ~ ). P~ough- surfaced E R (er). Neurotubules (t). Mitochondria (m). × 24000. b) After 6-OItDA-treatment dendritic vesicles exhibi t an electron-dense core ( ~ ). Dendrites can be recognized by their contacts with preganglionie axons (s) and/or the large amount of glycogen. Satellite cell (sz). × 18000. c) Domestic Fowl, Small ganglion cell with granules, which, according to their size, bu t not according to shape and density ( ~ ), resemble p-granules. This ganglion cell could be interpreted as well as an intermediate stage of a devclopillg ehromaffin cell (el.

Unsicker, 1973a). × 18000

566 K. Unsicker

Fig. 6 a and b. Corvus ]rugilegus. Axon dilations in the capsule of the adrenal gland, which probably represent afferent endings, a) (I) axon dilation with numerous mitochondria. ( / / ) large axon dilation with cytosome-like particles (cy), myelin bodies (my), clear (nb) and dense-cored vesicles (db). ×24000. b) Dilation in the course of an unconspicuous axon (ax).

× 5400


Fig. 7. Domestic Fowl. Numerous small axons (ax) in the periphery of a chromaffin cell complex (A). The axons do not exhibit an individual satellite sheath. × 24000 (cf. Unsicker,

1973b; Fig. 10)

2. Dendr i tes of large gangl ion cells ident i f iable b y thei r contac ts wi th preganglionic axons of ten conta in small , t r ans lucen t vesicles in which af ter 6 -OHDA- t r e a t m e n t a dense core appears (Fig. 4a , b). This phenomenon supports the view t h a t these dendr i t ic processes belong to adrenergic neurons. There are good reasons to assume t h a t small gangl ion cells (Unsieker, 1973a) are adrenergic as well, b u t i t is improbab le and was never observed t h a t these cells send out axons longer t h a n a hundred ~zm.

P r e s u m a b l y adrenergie axons join the large nerve t runks on thei r w a y into the in ter ior of the adrena l gland. Varieosit ies were somet imes found wi th in the large bundles. A common course of adrenergic and eholinergic fibers wi th in one nerve bundle has been r epor t ed several t imes (Tranzer and Thoenen, 1967; Clement i et al., 1969; Eh inger et al., 1969; Nilsson and Sporrong, 1970).

568 K. Unsicker

Fig. 8. Cholinergie, adrenergic, and peptidergie (or purinergic) innervation of adrenal chromaffin cells ( A 1 - A 1 1 ) in birds. The cell A 6 produces noradrenaline, the others contain adrenaline. The axons a x 1 - a x 8 form the "nerve stalk" of the cell complex, ax l, a x 2, ax (1, a x 5, and a x 7 are cholinergic axons; their synaptie endings contain synaptie and large dense-cored vesicles, ax 2 forms synaptie endings on A 2 - A 5 ; A g and A 5 are ilmervated by the same bouton. Chromaffin cells and bouton show complicated folds and indentations. a x 9, which is a cholinergie axon as well, innervates A 6 . The synaptic contacts are established at the cell body and at its dendritie process, ax 10 and ax 11 cannot be identified, ax 3 and a x 6 are adrenergic axons recognizable by their varieosities and two different populations of dense-cored vesicles. The terminals of adrenergic and peptidergie (purinergic) (ax 8) fibers

lack synaptie membrane specializations. Satellite cells (sz)

Large ganglion ceils of the avian adrenal gland and their axons have to be regarded as short adrenergie neurons. Short adrenergic neurons, which are situated within the effector organ or in the vicinity, have been demonst ra ted as well in the male and female genital t ract (Falek et a l . , 1965; SjSstrand, 1965; Owman and SjSberg, 1967; Sj6berg, 1968; and others).

However, testis an ovary, which, because of their ontogenesis, are closely related to the adrenal gland, are supplied by long adrenergie neurons (Sj6berg, 1968; Baumgar t en and Holstein, 1971).


For a long time adrenaline has been considered to be the main t ransmit ter of avian postganglionie sympathetic fibers (CMlinghara. and Cass, 1969; Everet t and Man, 1968; Iguarro and Shideman, 1968). Fluorimetrieal results, however, indicate that noradrenaline prevails ; this can also be concluded from the observations of Enemar et al. (1965) and Baumgarten and Holstein (1971). The green fluorescence of the fibers demonstrated by us and the alterations following 6-OHDA- t reatment speak in favour of noradrenaline as the main transmit ter - - a t least in the avian adrenal gland.

B. P-Type Fibers

The possibility of distinguishing a third type of nerve fiber beside cholinergic and adrenergie axons in the avian adrenal gland is based only on morphological criteria until now. The term , , p - type"= peptidergie or purinergie refers only to some ultrastruetural correspondence with neurons which are presumably or in fact peptidergic or purinergic. The morphological features of p-type fibers are varicosities with dense-cored vesicles, the mean diameter of which exceeds that of large dense-cored vesicles in cholinergie and adrenergic neurons, and which show only a thin light rim between dense core and vesicle membrane. These dense- cored vesicles highly resemble neurosecretory granules of vertebrates and everte- brates (Palay, 1955 ; Bargmann and Knoop, 1957 ; Bargmann, 1966 ; Seharrer and Weitzman, 1970). However, staining with chromMum hematoxyline-phloxine gives no clear results, as basal laminae and connective tissue fibers are stained as well, and the Herring body-like varieosities are too small for light mieroscopicM demonstration.

Within the peripheral autonomic nervous system axons which can be compared to p-fibers of the avian adrenal gland have been seen, for example, in the gut of different vertebrates (Baumgarten st al., 1970; Bennett and Rogers, 1967; Burn- stock and Iwayama, 1971; Hayer and Tafuri, 1959; Rogers and Burnstoek, 1966; Silva et al., 1968; Taxi, 1968) and in the amphibian lung (Robinson et al., 1971). (For further ref. see Burnstoek, 1972, chapter VI).

P- type fibers in the avian adrenal gland are not affected by 6-OHDA. The reaction of the granules to 5-hydroxydopa was not studied. As to their contents only speculations can be deliverd unless it is a purine nucleotide. Feldberg and Lewis (1964, 1965), Douglas et al. (1967), Poisner and Douglas (1966), and Stas- zewska-Barczak and Vane (1967) have shown that several peptides, as angiotensin and bradykinin, may be responsible for the release of eateeholamines from the adrenal medulla. Whether prostaglandines, which may exert some influence on the smooth muscles of gut (Kottegoda, 1969) and vas deferens (v. Euler and Hedquist, 1969) and may reduce the noradrenaline-output in the spleen after excitation of the splenic nerve (ttedqnist 1969a, b, c, 1970), or substance P (Franz et al., 196t; Itaefeli and Hiirliman, 1962; Stiirmer, 1963; Fischer, 1971, pp. 598- 600) have to be considered as a possible t ransmit ter of peripheral terminals is more than doubtful. Baumgarten et al. (1970) assume tha t p-type fibers in the plexus of Auerbaeh contain a protein or a polypeptide, "which is somehow connected with an amine mechanism". The increased density of the core after application of 5-hydroxydopa sustains this suspicion and makes one take into consideration a relationship between p-type fibers and 5-hydroxytryptamine-

570 K. Unsicker

neurons in the plexus myentericus (Gershon et al., 1965; Bfilbring and Gershon, 1967a, b). Small intensively yellow fluorescent nerve cells and fibers occur in the capsule of the avian adrenal gland and in periadrenal ganglia (Unsicker, 1973a). Perhaps these cells belong to a group of 5-HT cells, the axons of which correspond to p-type fibers on the ultrastruetural level. The preponderance of p-type fibers in subcapsular regions, where numerous yellow fluorescent fibers can be seen, may support such a hypothesis. Furthermore, it has been shown that 5-HT stimulates adrenal ehromaffin cells (Miller and Pes]~in, 1963; Poisner and Douglas, 1966; Douglas et al., 1967). On the ultrastructnral level a definite identification of perikarya, which may belong to p-type fibers, is difficult. Small ganglion cells containing granules which have the size of p-granules can be observed in the capsular region; however, these granules show a higher polymorphy and higher electron density than p-granules do (Fig. 4c).

Finally, when trying to give an interpretation of p-type fibers, we have to take into account that for a long time neurosecretion in the peripheral autonomic nervous system has been postulated (Pawlikowski, 1962, 1963; a.o.). However, it seems unlikely that there is a connexion between p-type fibers and peripheral neurosecretion, since all attempts to demonstrate the u]trastrnctural equivalents of what was stained by Pawlikowski have failed.

C. Afferent _Nerve Fibers

Axon dilations containing clusters of mitochondria and/or myelin-like struc- tures and dense-cored vesicles resemble degenerating and regenerating Herring bodies in the pituitary posterior lobe (Dellmann and Rodriguez, 1970) or degenerative alterations in the ligated ischiadic nerve (laellegrino de Iraldi and De Robertis~ 1968). On the other hand, Chiba and Yamanchi (1970) have shown that in the human myocardinm dilated axons occur which are filled with myelin-figures, lysosomes-like particles, dense-cored vesicles and/or aggregations of mitochondria. Chiba and Yamauchi (1970) consider these formations to be the "terminal portion of the cardiac afferents". This interpretation is in good agreement with the findings of other autors showing that dilated axons with closely packed mitochondria occur in such places where afferent endings must be expected (Salzer et al., 1964; Andres, 1966; ](olb etal., 1967; BSck, 1970; B6ck etal., 1970; Plenk and ]~aab, 1970; Terashima et al., 1970; B6ck, 19711 ; and others). In favour of a receptive function of the formations observed by us may speak the fact that they are situated mainly in or beneath the capsule of the organ. Mechanoreceptors have been identified with neurophysiological methods in the mammalian adrenal gland by Niijima and Winter (1968).

Large groups of thin axons which contain neurotubulcs only and are not isolated from each other or from chromaffin cells by Schwann cells may represent afferent endings as well.

D. Innervation o/ Blood Vessels

Small muscular vessels in the pericapsular tissue of the avian adrenal gland exhibit two different types of nerve endings. The first type is affected by 6-OHDA, the other one contains only small translucent vesicles and shows no alterations following 6-OHDA-treatment. Probably the two types of terminals are adrenergic


and cholincrgic. Such double innerva t ion of vessels has been shown, e. g., b y Schenk and E1 Bad~wi (1968). I n mammal s cholinergic vasodi la to r fibers have been demon- s t r a t ed several t imes (Folkow, 1955; t t e r t z m a n n , 1959; t t o l t on and ]%and, 1962; Bell, 1968, 1969a, b, c). The coeliac a r t e ry of the chicken and the pigeon is suppl ied b y ~ dense cholinergic and adrenergie plexus (Bennet t , 1969). Burns tock (1969) assumes t h a t in the course of evolut ion the adrenergic vasocons t r ic to r componen t has increased while the cholinergic vasocons t r ic tor component has diminished. Thus i t seems l ikely t h a t in birds as well as in m a m m a l s cholinergic fibers have t a k e n up a d i la tor ac t ion on blood vessels.

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Priv.-Doz. Dr. K. Unsicker Anatomisches Institut der Universit~t D-2300 Kiel Neue Universit~t, Eingang F 1 Federal Republic of Germany

39a Z. Zellforsch., Bd. 145

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Fine structure and innervation of the avian adrenal gland