Vascularization of the hypophysial region of the normal and adenohypophysectomized toad

Zeitschrift fiir Zellforschung 83, 207---218 (1967)

Vascularization of the Hypophysial Region of the Normal and Adenohypophysectomized Toad*

ESTEBA~ M. RODR~GUEZ* * and RAMON S. Px~zzI**

Instituto de Histologia y Embriologia, Facultad de Ciencias M6dicas - - U-NC Mendoza - - Argentina

Received, in final form, June 2, 1967

Summary. The study of standarized sections of the hypophysial regions, and in vivo observations showed the presence of communicating vessels between the capillary network of the median eminence and the large capillaries of the neurointermediate junction. Moreover, direct branches from the hypophysial artery are described which give off branches, at the level of the neural stalk, to the median eminence and to the large capillaries of the neurointermediate junction.

A second portal system similar to the one described by CRuz has been observed. Its primary plexus originates in several encephalic regions, and its secondary plexus is distributed through the neural lobe and thence to the pars intermedia. The course of flow in this system is a descending one. The arterial contribution to this system appears to arise from branches from the basilar and retroinfundibular arteries. - - There are small venous-type vessels between the large capillaries of the neurointermediate junction and the posterodorsal region of the pars distalis. - - After adenohypophysectomy, the blood which normally goes towards the pars distalis, flows towards the pars intermedia, following the path of the communicating vessels between the median eminence and the pars intermedia.

The first authors to recognise the portal na tu re of the vessels t ha t connect the median eminence to the pars distalis were PorA and FIELDING (1930). They be- lieved tha t the course of this portal system was an ascending one, i. e. from the pars distalis towards the hypotha lamus . HogssAY, BIASOTTI and SAMMARTII~O (1935) were the first to observe the descending course of the circulation, by direct ex- amina t ion of these vessels in live toads. The descending course was subsequent ly confirmed in other species by several authors (WIsLOCKI and KING, 1936 ; MO~ATo, 1939 ; G~ErN and HARRIS, 1949).

According to GREE~ (1947) and CRUZ (1959) this portal system is the sole vascular supply to the pars distalis; whereas HoussAY (1949) descibed a direct ar ter ial con t r ibu t ion to the posterodorsal region, arising either from the re t ro infundibular communica t ing ar te ry or else directly from the anastomot ic branches of the basilar artery. GREEN (1947) also described small communica t ions between the pars distalis and the pars intermedia. He did no t men t ion the direction of circulat ion of these vessels.

* This paper was presented at the VII Reunion de la Asociaci6n Latinoamericana de Ciencias Fisiol6gicas (A.L.A.C.F.), Mar del Plata, Argentina, 1966. It was carried out under the auspices of the Consejo Nacional de Investigaciones Cientfficas y T6cnicas de la Repdblica Argentina and the Rockefeller Foundation (School grant RF-58028).

* * Fellows of the Consejo Nacional de Investigaciones Cientffieas y T6enicas de la Re- pfiblica Argentina. - - The authors wish to thank Prof. B. A. HoussAY and Drs. J. H. TRA- MEZZA~r~ and J. L,A POI~TE for their criticism, to Prof. M. H. BURGOS and Dr. F. SAC~BDOTE for their help.

208 E.M. RoImiGtrEZ and R. S. PIEzzI:

Vascularization of Hypophysial Region 209

Some of the vessels of the median eminence, instead of ending in the pars distalis, end in the large capillaries of the neurointermediate junction (GRE~, 1947 ; L]~Ys, 1962). Furthermore, according to the latter author, the vessels which penetrate the pars intermediate and reach the pars distalis emerge from those large capillaries. According to ETXI~ (1962) the vessels that reach the neurointermediate junction do not come from the median eminence but from small arteries situated in the zone of the neural stalk, which could be branches of the hypophysial artery. Branches arising from this network of arteries of the stalk also penetrate the median eminence.

I t is in the vascularization of the neural lobe where observations have been less intelligible. According to HoussAY, BIASOTTI and SAMMARTI~O (1935) and t tovs- sAY (1949) the neural lobe is irrigated by a branch from the retroinfundibular communicating artery. According to GRE~I~ (1947), this lobe receives its supply from the anastomotic branches of the basilar artery. On the other hand, according to CR~GIE (1939), the blood supply to the neural lobe would be the one coming from the hypothalamus. According to this author, the vessels might be of an arterial type and the circulation a descending one. Finally. CRvz (1956 and 1959) recognized the venous nature of these vessels and described them as a second hypophysial portal system, whose primary plexus might be in the encephalon and the secondary plexus in the neurointermediate lobe.

We known of no references concerning the changes produced in the vaseularization of the hypophysial region of amphibians after partial or complete hypophysectomy. On the other hand, vascular changes of the hypophysial region have been studied in the rat after total hypophysectomy (MOLL, 1958). This author observed an increase in the number of capillaries in the infundibular region, which are drained by veins towards the neighbouring subdural sinuses.

Since there is no agreement as to the vascularization of the amphibian hypophysis, and a lack of information on the effects of adenohypophysectomy on this vaseularization, we are presenting our results obtained from serial sections and in vivo observations of the vessels of the hypophysis in the normal and adenohypophysectomized toad.

Fig. 1. Longitudinal section of the hypophysial region. At the mesencephalon (M): the dotted arrows point to those vessels that form the posterior mesencephalic and bulbar group and the full-line arrow points to the collecting vein of the hypothalamic group of the encephalo-posthypophysial portal system. At the neural lobe (N) : the dotted arrows point to the ending of the capillaries of the encephalo-posthypophysial portal system at the large capillaries of the neurointermediate junction (full-line arrows). At the pars intermedia (PI) : the dotted arrows point to the marginal capillaries. At the pars distalis (PD) : the arrows point to the "sinusoid capillaries" and at the median eminence (ME) the dotted arrow points to capillary vessels and the full-line arrow to arterioles. B communication branch of the basilar artery; RC retroinfundibular communicating artery; P g common venous stem of the encephalo-posthypophysial portal system; HA hypophysial artery; ESP endolymphatic sac plexus; I infundibulum; IR infundibular recess; IRR infundibular recess roof; MS median eminence stalk; PAS-orange stain

• 115

Fig. 2. Section near to the previous one. The collecting veins of the hypothalamic (HpV) and the anterior meseneephalie groups (AMV) are observed. M mesencephalon; RC retroinfundibular communicating artery; P V common venous stem;/V neural lobe; IR infundibular recess.

PAS-orange. • 120

210 E.M. RO~RICtU~Z and R. S. PtEZZI:

Fig. 3. Longitudinal section of the hypophysial region showing the inlet of the common venous stem (P V) of the eneephalo-posthypophysial portal system (arrows), in the neural lobe (N). RC retroinfundibular communicating artery; BC large capillaries of the neurointermediate junction; P I pars intermedia; N S neural stalk; I R infundibular recess. Paraldehyde-fuchsin

stain. X 480

Material and Methods Histological observations were carried out on 133 animals used in previous work (ROURI-

a~EZ, 1966; RODRmU~Z and PrszzI, 1967) 83 with the hypophysial region intact and 50 adenohypophysectomized. The in vivo observations were carried out by means of a 80X magnifying lens. To observe the vessels of the pars intermedia, the pars distalis was removed according to the technique of RODRIOUEZ and PI~zzI (1967). In order to observe the eneephalon- posthypophysial portal system and the retroinfundibular artery the following techniques were applied: 1. The infundibular recess was perforated at the stalk of the median eminence, per- mitting the exist of eerebrospinat fluid (Fig. 1). The thin lamina of the floor was applied to the roof of the infundibular recess. The vessels could then be observed directly through the trans- parent lamina. 2. By sectioning the stalk of the median eminence and using the neural stalk as a hinge, it was possible to place the median eminence out of the way on the pars distalis, so that the vessels of the encephalo-posthypophysial portal system could be observed through the roof of the infundibular recess (Fig. 1).

Results The winding hypophysial branches of the hypothalamic ar tery run sagit tal ly

on both sides of the midl ine; they always contact the pars tuberalis, bi lateral ly s i tua ted in f ront of the stalk of the median eminence (Fig. 5). The major i ty of branches of the hypophysial ar tery penetra te the median eminence forming the p r imary plexus of the hypothalamie-adenohyophysia l portal system. Some of the capillaries of the median eminence, ins tead of supplying the pars distalis, go through the neural stalk and end in the large capillaries of the neurointermediate junc t ion


Fig. 4. Longitudinal section of the hypophysis, showing the trajectory of a communicating vessel between the pars intermedia (PI) and the pars distalis (PD) (arrows). BC large capillaries of the neurointermediate junction; the dotted arrow points out a tangential section of one of

the branches; N neural lobe. PAS-orange. X 330

or penetrate into the parenchyma of the pars intermedia (Fig. 5). We do not know the direction of the flow in these communicating vessels.

In addition, the hypophysial arteries have one or two branches on either side which, instead of penetrating into the anterior region of the median eminence, like the majority, pass directly towards the neural stalk, clinging to the surface of the median eminence along its lateral regions. At the neural stalk it gives off branches towards the midline, so that in sagittal sections they are seen in transverse section in the angle formed by the neural stalk and the pars intermedia (Fig. 5). These small arteries give off branches that form capillary nets within the median eminence contributing to the capillary network of the primary plexus of the hypothalamie- adenohypophysial portal system. Other branches of these direct arteries take a reverse course and, following the neural stalk, end at the capillaries of the neurointermediate junction (Fig. 5).

Encephalo-posthypophysial portal system The primary plexus of this system is distributed about an ample zone of the

encephalon, drained by numerous veins which, in turn, empty into one or two venous stems, The course of flow of this portal system is descendant, that is to say, from the encephalon towards the hypophysis. The places where the primary plexus originates can be divided into three groups.

1. Hypothalamic group. The capillaries of this group are distributed in the region of the preoptic nucleus. The veins that drain this group go caudally and ventrally, towards the angle formed by the roof of the infundibular recess and the floor of the diencephalon (Figs. 2 and 5). The venous branches that come to this angle are numerous, but here they join two or three veins on either side. From this point the veins follow a straight line, along the external surface of the roof of the infundibular recess, to flow finally into the common venous stem of the same side (Figs. 2 and 5).

15 Z. Zellforsch., Bd. 83

212 E.M. RODRiGUEZ and R. S. Pr~zzI:

2. Anterior mesencephalic group. I t originates in the anterior region of the mesencephalon, therefore including the floor of the anterior end of the aqueduct of Sylvius. The veins draining this zone proceed rostrally and ventrally, flowing into different levels of the collecting veins of the anterior group (Figs. 2 and 5).


Fig. 6. Longitudinal section of the hypophysial region of an adenohypophysectomized toad (60 days after operation), showing an increase in the vascularization (arrows) of the hypertro- fled pars intermedia (PI). The arrows at the neural lobe (N) point out the capillary branches of the common venous stem (PV) and the large capillaries of the neurointermediate junction. /~C retroinfundibular communicating artery; I infundibulum; ME median eminence; NS

neural stalk; IR infundibular recess. Mallory • 115

3. Posterior mesencephalic and bulbar group. The capillary branches of this group are s i tua ted in the region of the cerebral s tem from the posterior par t of the mesencephalon to the bulbo-medul la ry limit. The veins draining these capillaries descend vert ical ly and flow in to two collecting veins, one on either side, which proceed in close contact with the floor of the cerebral stem (Figs. 1 and 5). As these collecting veins approach the common venous stem on their side, they increase in

Fig. 5. Semi-schematic representation of the vascularization of the hypophysial region oi the toad. C cerebellum; SA aqueduct of Sylvius; M mesencephalon; H hypothalamus; IR infundibular recess; I infundibulum; P T pars tuberalis ; ME median eminence; N neural lobe; P I pars intermedia; PD pars distalis. The refilled vessels are a portal type and the linear ones are arteries. Vessels: 1 hypothalamic group of the primary plexus of the encephalo-posthypophysial portal system; 2 anterior mesencephalic group; 3 posterior mesencephalic and bulbar group; d common venous stem; 5 capillarization at the neural lobe; 6 large capillaries of the neurointermediate junction; 7 superficial capillaries of the pars intermedia ; 8 pars intermedia- pars distalis communicating vessel; 9 basilar artery communicating branch; 10 retroinfundibular communicating artery; 11 hypothalamic branch of the retroiiffundibular communicating artery; 12 hypophysial artery; 13 median eminence capillary loops; 14 hypothalamo-adenohypophysial portal veins; 15 sinusoid capillaries of pars distalis; 16 pars distalis collecting veins; 17 endolymphatie sac plexus; 18 communicating capillaries between median eminence and pars intermedia; 19 direct branch of the hypophysial artery giving off a branch to the

median eminence and another to the large capillaries of the neurointermediate junction

15"

214 E.M. RODRIGUEZ and R. S. PIEZZI:

Fig. 7. Longitudinal section of the median eminence (ME) 30 days after adenohypophyseeto- my, showing a swelling of its capillaries (DC) and the presence of a thick collecting vessel (C V), which after a tortuous trajectory (full-line arrows), flows into a dilated superficial capillary (dotted arrow) of the pars intermedia (MC). MS median eminence stalk; NS neural stalk; IR infundibular recess; N neural lobe; BC a large capillary of the neurointermediate junction.

Paraldehyde-fucbsin. • 170

size. At the retroinfundibular communicat ing artery, these veins take a descending course and flow into the common venous stem (Fig. 5).

There are one or two common venous stems, which are si tuated between the retroinfundibular communicat ing ar tery and the thin roof of the infundibular recess (Figs. 1, 2 and 5). The venous stems penetrate the neural lobe through its anterosuperior angle, producing m a n y branches within the neural lobe (Figs. 3 and 5). The greater proport ion of these branches end in the great capillaries of the neuro intermediate junct ion (Figs. 1,5 and 6). Those tha t do not end in these large capri- laries go towards the dorsolateral region, where veins are formed, which ul t imately drain into the hypophysia l veins. We have never observed branches of the portal vein going directly to the pars intermedia without passing through the neural lobe.

I t is impor tan t to recall t ha t the great capillaries of the neurointermediate junct ion receive contr ibution from three sources: 1. Capillaries coming from the median eminence, 2. Small arteries coming from the direct branches of the hypophysial artery, 3. Mostly of the capillaries tha t form the secondary plexus of the encephalo-posthypophysial portal system. From this zone of confluence, branches lead out dorsally and ventral ly around to the opposite, distal side of the pars intermedia, where they come to lie superficially, but always within the glandular tissue (Figs. 1 and 5).

A few vessels f rom the pars intermedia tha t pass through the pars distahs, on a level with the dorsal border of both regions, m a y be observed in each animal


Fig. 8. Neurointermediate lobe 30 days after adenohypophysectomy, showing a swelling of the vessels and a greater vascularization of the pars intermedia (PI). N neural lobe; BC large capillaries of the neurointermediate junction; MC superficial capillaries of the pars intermedia;

HV hypophysial vein. Paraldehyde-fuchsin. • 170

(Figs. 4 and 5). In the pars distalis these vessels are surrounded by typical adenohypophysial cells. We have been unable to observe them in live animals and, therefore, cannot tell what course the circulation takes in them.

The branches of the division of the basilar ar tery give off branches at right angles tha t supply the same regions that give rise to the second and third groups of the encephalo-posthypophysial portal system. Due to the closely neighbouring connections, and to the fact tha t it is practically the sole arterial contribution to these regions, we assume that these branches of the basilar ar tery supply the arterial blood to a great par t of this portal system (Fig. 5). The arterial contribution of the hypothalamic group is probably made up by branches originating from the ends of the retroinfundibular communicating artery. These branches reach the hypothalamie region at the same angle where the portal veins of this group leave (Fig. 5).

Vascularisation o/the hypophysis o/adenohypophysectomized toads

The removal of the pars distalis brings about some changes in the vascularization of the remaining parts of the hypophysis, which can be observed on the 15th day after operation, but are quite clear-cut from the 30th day on.

216 E.M. RODRIGU~Z and R. S. PIEZZr:

Fig. 9. Semi-diagrammatic representation of the vascularization of the hypophysis after adenohypophysectomy. I infundibulum; M E median eminence; N neural lobe; P I pars intermedia; Vessels: 1 encephalo-posthypophysial portal system; 2 hypophysial artery; 3 median eminence capillaries ; 4 collecting vessel at the median eminence; 5 large capillaries of the neurointermediate junction; 6 superficial capillaries of the pars intermedia; 7 neural lobe

vein; 8 hypophysial vein; 9 retroinfundibular artery

The blood capillaries of the median eminence become greatly enlarged (Figs. 7 and 9). They flow into large vessels at the most superficial part of the median eminence. These take a winding course towards the neural stalk to end either in the large capillaries of the neurointermediate junction or communicate directly with the capillaries of the pars intermedia, which are branches of the former (Figs. 7 and 9). The capillaries of the neurointermediate junction generally become dilated (Fig. 9). The capillaries which branch off from them and penetrate the pars intermedia increase in number and size and give off branches which proceed from the ventral surface into the depth of the glandular tissue (Figs. 6, 8 and 9). The veins which drain the neurointermediate lobe also become quite dilated (Figs. 8 and 9). These veins belong to the plexus of the endolymphatic sac, and end in the subdural sinuses as under normal conditions.

Discussion

Our observations agree with those of HoussAY, BIASOTTI and SAMMARTINO (1935), GREEN (1947), CRUZ (1959), and L]~NYs (1962) with regard to the characteristics of the hypothalamic-adenohypophysial portal system. Nevertheless, neither GREEN (1947) nor CRuz (1959) nor we ourselves have found the arterial branch which, according to HOUSSAY (1949), supplies the posterodorsal region of the pars


distaffs. On the other hand, we have found in tha t zone of the pars distalis venous- type vessels which connect it with the pars intermedia. These communicating vessels might explain the absence of necrosis of the posterodorsal region of the pars distaffs after the hypophysial arteries are severed (LAzCANo-GoNzALEZ, 1935).

We agree with GREEN (1947) and LENYS (1962) with regard to the communicating vessels between median eminence and pars intermedia, and also with ETKIN (1962) with regard to the presence of an arterial network in the zone of the neural stalk, because we have found (a) loops from the median eminence to the pars intermedia and (b) arteries from the stalk which give off branches to both regions.

With respect to the distribution of the pr imary plexus and the arrangement of the draining veins and of the venous stem of the encephalo-posthypophysial portal system, our observations coincide with those of CRUZ (1959). This author states that the secondary plexus is distributed in the neurointermediate lobe, but not how. We believe it is important for future interpretations of the functions of this region to describe the characteristics of this secondary capillary plexus. For example, the fact tha t the pars intermedia receives no direct branches from the portal vein, and tha t the ones it does receive must first have passed through the neural lobe via the large capillaries of the neurointermediate junction, does seem important to us, for the blood tha t the pars intermedia receives contains sub- stances liberated from the neuroseeretory endings of the neural lobe.

The pars intermedia, by means of its vascular connections, is connected: 1. with the median eminence and, therefore, with the hypothalamic neuroseeretory axons coming to it; 2. with the neural lobe and its neurosecretory axons; 3. with all the nervous centers, including the hypothalamus, in which the encephalo-posthypophysial portal system originates; 4. with the rest of the body through the direct arterial branches of the hypophysial artery. All these connections, especially the first three, may help to clarify the mechanism of the hypothalamus-pars intermedia antagonism. The encephalic centers having the greatest concentration of noradrenaline are the hypothalamus and the mesencephalic-bulbar region (see DoNoso and STEFANO, 1966). In addition, FuxE, H(SKFELT and I~ILSSON (1965), by means of fluorescence and electron microscope techniques, described the presence of monoamines in several bulbar nuclei. Adrenergic-type endings have also been described in the anterior hypothalamus by P]SLLEGRINO DE IRALDI, DUGGAK and DE ROB~RTIS (1963) and RODI~mUEZ (unpublished). From all these centers, in which monoamines have been described, vessels start that reach the neurointermediate lobe. Could this be taken to explain I turriza 's hypothesis (personal communication) whereby the inhibitory action on the pars intermedia is exercised through monoamines ?

MOLL (1958) observed tha t in the ra t after total hypophysectomy the portal veins, deprived of the organ in which they branch into capillaries again, drain their contents into the neighbouring subdural sinuses.

After adenohypophysectomy, large vessels which collect the blood from the median eminence and empty into the pars intermedia are seen. These vessels have the same pat tern as the small communicating capillaries which are normally found between both regions. These communicating vessels are no longer seen after adenohypophysectomy. Therefore, it is easily concluded tha t the blood, tha t nor-

218 E.M. RODRIGUEZ and R. S. PIEzzI: Vascularization of Hypophysial Region

mal ly flows towards the pars distalis, when the pars distalis is r emoved should

flow towards the pars in te rmedia taking the course of the communicat ing vessels and causing them to enlarge. This in te rpre ta t ion also explains the increase in

number and d iameter of the pars in termedia vessels and the di la tat ion of the large

capillaries of the neuroin termedia te junct ion and of the collecting veins of the

neuro in te rmedia te lobe. F r o m this we infer t ha t the blood entering the median eminence through the

hypophysia l a r te ry finally makes its way to the subdural sinuses but, instead of

passing through the pars distalis, i t t raverses the pars intermedia.

References CRAIGIE, E. H.: Vascular connection of the hypophysis in the leopard frog (Rana pipiens).

Anat. Rec. 74, 6 1 ~ 9 (1939). C~uz, A. R.:Sur l'existence de deux syst~mes portes dans l'hypophyse des amphibiens anoures.

C. R. Acad. Sei. (Paris) 242, 189--190 (1956). - - Sur l'existence d'un syst~me porte dans la neuro-hypophyse des amphibiens anoures

Acta anat. (Basel) 36, 153--168 (1959). DoNoso, A. O., and F. J. E. STEFANO: Cerebral changes in the noradrenaline content during

cortical spreading depression in the rat. Acta physiol, lat.-amer. (in press). ETKIN, W.: Hypothalamie inhibition of pars intermedia activity in the frog. Gem comp

Endocr., Suppl. 1, 148--159 (1962). FuxE, K., T. HSKFELT, and O. NILSSON: A fluorescence and electron-microscopic study on

certain brain regions rich in monoamine terminals. Amer. J. Anat. llT, 3 3 ~ 6 (1965). GREEN, J. D. : Vessels and nerves of amphibian hypophyses. A study of the living circulation

and the histology of the hypophysial vessels and nerves. Anat. Rec. 99, 21--53 (1947). - - , and G. W. HARRIS: Observation of the hypophysis-portal vessels of the living rat. J.

Physiol. (Lond.) 108, 359--361 (1949). HoussAY, B.A.: Hypophyseal functions in the toad Bufo arenarum Hensel. Quart. Rev.

Biol. ~4, 1--27 (1949). - - A. BIASOTTI y R. SAMMARTINO: Modificaciones produeidas per las lesiones infundibulo-

tuberianas en el sapo. Rev. Soc. argent. Biol. 11, 318--330 (1935). LASCA~o-Go~ZALEZ, J. M.: Infartos hipofisarios por lesiones tuberianas en el sapo. Rev. Soc.

argent. Biol. 11, 309--313 (1935). LENYS, D. : Etude morphologique des relations neurovasculaires hypothalamo-hypophysaires.

Th~se Medicine, Nancy 1962. MOLL, J.: The effect of hypophysectomy on the pituitary vascular system of the rat. J. Morph.

10~, 1--21 (1958). MORATO, M. J. X.: The blood supply of the hypophysis. Anat. Rec. 74, 297--320 (1939). PELLEGRINO DE IRALDI, A., n . F. DUGGAN, and E. DE ROBERTIS: Adrenergic synaptic vesicles

in the anterior hypothalamus of the rat. Anat. Rec. 145, 521--531 (1963). POPA, G. T., and U. FIELDING: A portal circulation from the pituitary to the hypothalamic

region. J. Anat. (Lond.) 65, 88--91 (1930). RODRIGUEZ, E.M.: Differences between median eminence and neural lobe in amphibians

Z. Zellforsch. 74, 308--316 (1966). - - , and R. S. PIEzzI: The effects of adenohypophysectomy on the hypothalamo-hypophysial

neurosecretory system and the adrenal gland of the toad Bufo arenarum Hensel. Z. Zell- forsch. 80, 93---107 (1967).

WISLOCKI, G. B., and L. S. KING: The permeability of the hypophysis and hypothalamus to vital dyes with a study of the hypophyseal vascular supply. Amer. J. Anat. 58, 4 2 1 ~ 7 2 (1936).

ESTEBAN M. RODRiGUEZ Department of Pharmacology, Medical School, University of Bristol Bristol 8, England

Vascularization of the hypophysial region of the normal and adenohypophysectomized toad

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