Microvascular Anatomy of the Hippocampal Formation
S l o b o d a n M a r i n k o v i d , M . D . , P h . D . , M i l a n Mi l i s av l j ev id , M . D . , a n d Las lo Pugkag , M . D . , P h . D .
Institute of Anatomy, University Medical School, Belgrade, Yugoslavia
Marinkovi~ S, Milisavljevid M, Pugkag L. Microvascular anatomy of the hippocampal formation. Surg Neurol 1992;37:339-49.
The hippocampal vessels were examined in 25 forebrain hemispheres injected with india ink or methylmethacry- late. There were two to seven hippocampal arteries, which measured 200-800/am in diameter. The anterior hippo- campal artery (AHA), which was present in 88.2% of the hemispheres, most often originated from the posterior ce- rebral and the anterior temporal arteries, that is, within the rostral hippocampo-parahippocampal arterial com- plex. It arose from the anterior choroidal artery in 29.4% of the hemispheres. The AHA extended between the un- cus and the parahippocampal gyrus, and it supplied the head of the hippocampus. The middle hippocampal artery was constant. It most often arose from the posterior cere- bral and the common temporal arteries. The middle hippo- campal artery coursed just caudal to the uncus, in close relationship with the lateral posterior choroidal artery, and it usually supplied the middle part of the hippocampal formation. The posterior hippocampal artery, which ex- isted in 94.1% of the hemispheres, most often arose from the posterior cerebral and the splenial arteries. It irrigated the caudal part of the hippocampal formation. The anasto- moses connecting the posterior, middle, and the anterior hippocampal arteries were present in 29.4% of the hemi- spheres.
The hippocampal arteries gave rise to the straight ves- sels, which divided into the large and the small intrahippo- campal arteries. The highest density of the capillary net- work was noted in the pyramidal and molecular layers of the hippocampal formation. The clinical significance of the obtained microanatomical findings is discussed.
The hippocampal formation is one of the most important parts of the cortical portion of the limbic system [2 ,20-22] . There is a specific local activity of the hippo-
Address reprint requests to: Dr. Slobodan Marinkovi~, M.D., Institute of Anatomy, University Medical School, Dr. Subotida 4/2, 11000 Belgrade, Yugoslavia.
Received June 3, 1991; accepted August 28, 1991.
campal neurons [8] that correlates with the function of the neurons in some other regions of the brain. This interaction of the hippocampal and other neurons is made possible by connections of the hippocampal forma- tion with many cerebral regions, especially with the ento- rhinal area, the association neocortical regions, and cer- tain portions of the diencephalon and the brain stem [2,4,13,14,22,24,28]. Some of the mentioned regions send specific projections to the hippocampal formation: cholinergic (from the septal region), serotoninergic (from the nuclei ofraphe), noradrenergic (from the locus coeruleus), the dopaminergic (from the ventral tegmen- tal area), and so on [4,6,22]. These neuronal connec- tions, the local activity of the hippocampal neurons, and the local intrahippocampal neuronal circuits enable the crucial functioning of the hippocampal formation in the memory and the learning process [6,15,17,18,2 3,29].
Disorders of the function of, and pathologic changes in, the hippocampal neurons have been noted in many pathophysiologic and pathologic conditions, such as ce- rebral ischemia, hypoglycemia, "psychomotor epilepsy," schizophrenia, and Alzheimer's disease [1,6,7,23,31]. In some of these cases modern microneurosurgical proce- dures can be performed [23,25,31].
In spite of the obviously great functional role and clinical significance of the hippocampal formation, in the last seven decades only a few reports have appeared that deal with the hippocampal vasculature, which is the base for the normal function of the hippocampal formation, and in which disorders may have significant clinical impli- cations [9,10,19,23,30].
The aim of the present study was to examine the anatomic characteristics of the hippocampal arteries, the features of the hippocampal microvasculature, and the relationship between the extrahippocampal and the in- trahippocampal vessels.
M a t e r i a l s a n d M e t h o d s
The study was carried out in 25 forebrain hemispheres taken as soon as possible after death. In all the hemi- spheres, plastic catheters were placed in the internal carotid and the posterior cerebral arteries. The arterial system was perfused with isotonic saline solution. There-
after, in two hemispheres methylmethacrylate was in- jected to obtain casts of the hippocampal vessels. The arteries of the other 23 hemispheres were injected with a 10% mixture of india ink and gelatin. After fixation in 10% formaldehyde solution for 3 weeks, 17 hemi- spheres were microdissected under the stereoscopic mi- croscope to examine the extrahippocampal vessels. In the remaining six hemispheres the hippocampal forma- tion was removed and cut perpendicular to its longitudi- nal axis. Serial sections of the hippocampal formation were made. The thickness of the slices was 500 ~m. Between each two of them, a small slice was cut measur- ing 20/zm in thickness. The thick slices were cleared by Spalteholz's method with methylsalicylate and benzyl- benzoate [6]. The thin slices were dyed with cresil violet and luxol fast blue and then compared with the thicker ones to determine the sectors of the hippocampus and the layers of the hippocampus and the dentate gyrus. The intrahippocampal arteries were examined in the cleared sections of six hemispheres and in two vascular casts. Statistical analysis for the extrahippocampal arteries was carried out in the 17 hemispheres.
Resul ts
The hippocampal formation in the narrower sense com- prises the hippocampus, or Ammon's horn (cornu Am- monis [CA]), with its head, body, tail, and fimbria; the dentate gyrus; the subiculum, with the parasubiculum, presubiculum, subiculum proper, and prosubiculum; and the caudal prolongations of these structures, that is, the fasciolar gyrus, the fasciola cinerea, and the gyri of Retzius (Figure 1). The hippocampal formation, which is curved around the midbrain, extends from the uncus to the splenium of the corpus callosum.
The hippocampal formation receives the arterial blood vessels exclusively through its medial part, mainly through the free medial surface of the dentate gyrus (the so-called margo denticulatus) (see Figure 1). In our study the majority of the hippocampal arteries originated from the posterior cerebral artery (PCA). There were two to seven of them (mean 3.8), and they measured 200-800 k~m in diameter. Three sorts of these vessels can be distinguished: the anterior (rostral), the middle, and the posterior (caudal) (Figure 2).
The Anterior Hippocampal Artery The anterior hippocampal artery (AHA) was noted in 88.2% of the examined hemispheres (Table 1) (see Fig- ure 2). If absent, the artery was replaced by a strong rostral branch of the middle hippocampal artery (MHA) (see Figure 10), and/or by the hippocampal branch of the uncal branch of the anterior choroidal artery (AChA).
Figure 1. Dorsal view of a left ht~)pocampal formation after removal of the roof of the temporal horn (1) of the lateral ventricle, and partial removal of the crus cerebri (2) and the rostral portions of the brain stem and diencepha- lon. (3) Head, (4_) body, and (5) tail of the hippocampus," note the superficial veins of the hippocampus. (6) Atrium of the lateral ventricle. (7) Choroid plexus. (8_) Fimbria of the hippocampus, (9) Dentate gyrus (i.e., the margo denticulatus) and the subiculum proper. (10) Dorsal of the parahippocampal gyrus. H 1 l) Large MHA. (1_2) The uncus. (13) AChA. (14) Uncal recess.
Usually one AHA was present, rarely two of them. They ranged from 280 ~zm to 700/~m in diameter (see Table 1). The AHA usually arose within the so-called rostral hippocampo-parahippocampal arterial complex (Figures 3 and 4). The main components of the complex are the AHA and the anterior temporal artery (ATA). The large parahippocampal branches and, rarely, the MHA can also be included in the complex (see Figure 3).
The AHA most often originated from the ATA (see
Figure 2. Ventral view of the left hippocampal arteries after removal of the parahippocampal gyrus and the subiculum. (l) A H A arising close to the A T A (2). (3) M H A originating close to the M T A (4). (5 )PHAs arising close to the posterior temporal artery (6). (7) Distal segment of the PCA. (8_) Trochlear nerve. (9__) Crus cerebri. (I__0_0) The uncus. (1__L1) LPChA. (1___2) Fimbria of the hippocampus. (1__3_3) Pulvinar of the thalamus.
Microvascular Anatomy of Hippocampal Arteries Surg Neurol 341 1992;37 :339-49
T a b l e 1. Characteristics of the Hippocampa/ Arteries
Number: Diameter: Hippocampal Parent range range
arteries Frequency vessels (%) (mean) (mean)
Anterior 88.2c~ ATA (29.4) 0-2 280-700 ~m hippocampal ATA & PCA (5.9) (1.25) (476 tzm) artery PCA (23.5)
AChA (17.6) AChA & ATA (11.8)
Middle 100.0% PCA (29.4) 1-3 310-800 tzm hippocampal ATA (11.8) (1.29) (588/~m) artery ATA & LGA (5.9)
MTA (5.9) CTA (23.5) CTA & ATA (5.9) LPChA (11.8) LPChA & ATA (5.9)
Figure 4) and/or from the distal segment of the PCA (see Figure 5). The artery usually arose close to the uncal sulcus, that is, between the "hidden" ventral surface of the uncus and the dorsal surface of the parahippocampal gyrus (see Figures 3 and 5). The artery first continued laterally toward the rostral part of the dentate gyrus and the head of the hippocampus. It then abruptly changed its direction and continued along the dentate gyrus. When there were no hippocampal branches of the AChA, the AHA reached the junction of the uncus and
the hippocampal formation and turned sharply caudally, continuing along the rostral part of the dentate gyrus (see Figure 4). In these cases the AHA supplied most of the head of the hippocampus. However, when the AChA gave rise to small hippocampal branches or the second AHA, the hippocampal artery of the PCA reached the junction of the head and body of the hippocampus and then turned sharply rostrally along the dentate gyrus. The AHA sometimes divided into two terminal stems,
Figure 3. Rostral hippocampo-parahippocampal arterial complex. (I~ ATA (striped area). (2) AHA (dotted area). (3) Parahippocampal arteries (white). (4) Distal segment of the PCA. (5) Dorsal surface of the parahippo- campal gyrus. (6) Fimbria. (7) Margo denticulatus. (8) Unca/ branch (black) of the AChA (9). (1 O) T-he uncus, which is displaced slightly dorsally to open the uncal sulcus (l_l_l). (1__2_2) Right internal carotid artery. ~1_33 ) Middle cerebral artery. (14) Anterior cerebral artery. (1__~5 ) Posterior communicating artery. (1__6_6) Ventromedial surface of the parahippocampal gyrus.
"7" 3
Figure 4. Dorsal view of a right specimen after removal of the uncus. (l_J AHA arising from the ATA (2), which a/so gives rise to the MHA (3). (4) Distal segment (cut~ of the PCA. ~5) Dorsa/ surface of the parahippocampa/ gyrus. ~6~ Head of the hippocampus (cut~ with exposed straight arteries. (7 J Fimbria.
7
342 Surg Neurol Marinkovie et al 1992;37:339-49
8
Figure 5. A rare instance of the origin of the MHA (1)from the MTA (2); dorsomedial view. (3) ATA. (4) Distal segment (cut~ of the left PCA. (5) AHA, which gives rise to a large parahippocampal branch (6). (7) The uncus, which is slightly displaced dorsally. (8) Uncal branch of the AChA, which enters the uncal sulcus (9).
each of them taking opposite turns close to the head of the hippocampus.
The AChA gave rise to the AHA in 29.4% of the cases. In fact, the AChA gave rise to a large uncal branch, which entered the uncal sulcus and fissure (see Figure 3). The terminal part of the uncal branch represented the AHA, which supplied the rostral half of the head or, very rarely, the entire head of the hippocampus.
The A H A sometimes gave rise to small and large parahippocampal branches, subicular branches, uncal ar- tery, and straight hippocampal vessels.
Small parahippocampal branches were always present, while large ones were noted in 82.4% of the cases (see Figures 3, 5, and 6). Most of them left the uncal sulcus to supply the rostral part of the basal (ventromedial) surface of the parahippocampal gyrus, that is, the ento- rhinal area. The thin subicular branches took part in the irrigation of the subiculum. The uncal artery originated from the AHA in 47.1% of the cases. It usually supplied the ventral surface of the uncus. It rarely left the uncal sulcus to supply the medial surface of the uncus also. The straight hippocampal vessels will be described later.
Direct and indirect anastomoses involving the AHA were seen in almost all the cases examined. The largest anastomoses connected the AHA to the MHA as well as the uncal branch of the AHA to the same branch of the AChA. The latter anastomoses ranged from 50 txm to 220 /xm in diameter.
almost always in a close relationship with the largest lateral posterior choroidal artery (LPChA) (see Fig- ure 2).
There were one to three MHAs, which measured 310-800 /zm in diameter (see Table 1). They most often arose from the distal (P2) segment of the PCA (see Figure 2) or from the common temporal artery (CTA) (see Table 1). The M H A originated less frequently from the ATA (see Figure 4), and very rarely from the middle temporal artery (MTA) (Figure 5).
The MHA often had a close relationship to the largest LPChA (see Figure 2). The former vessel often arose close to the latter one or even from the latter itself (17.6%). The M H A was sometimes almost completely superimposed on the LPChA.
The MHA extended across the dorsal surface of the parahippocampal gyrus and the subiculum, within the wing of the ambient cistern. The artery almost always divided into rostral and caudal stems (Figure 6). The
Figure 6. Dorsal view of the vascular cast of the distal segment of the right PCA ~1). (2) MHA. (3) AHA. (4) Parahippocampal branches of the h ippocampa]-a rteries.
The Middle Hippocampal Artery The MHA is the most constant hippocampal artery. Irre- spective of its origin, the M H A was located near the caudal part of the uncus (see Figure 2). Besides, it was
Microvascular Anatomy of Hippocampal Arteries Surg Neurol 343 1992;37:339-49
Figure 7. Dorsal view of the vascular cast of a right MHA ~1), which divides into the rostral (2) and the caudal stem (3_J. Note the subicular ~4) and the small parahippocampal branches (5), as well as the straight hippocampal branches (between the two arrows).
T h e Pos ter ior H i p p o c a m p a l A r t e r y
The PHA was almost always present (see Figure 2). When absent, it was replaced by the caudal stem of the MHA. There were zero to three PHAs, which varied from 200 ~m to 800/.~m in diameter.
The PHA most often originated from the splenial (spleniothalamic) artery (SplA) (Figure 8), and the distal segment of the PCA (see Figure 2). Occasionally it arose from the lingual gyri artery (LGA) (see Table 1).
The PHA usually coursed across the most caudal part of the dorsal surface of the parahippocampal gyrus (see Figure 8). Some of the arteries coursed only laterally, toward the caudal part of the hippocampal formation, where they gave rise to the straight vessels in a fanlike manner. Some of these PHAs gave rise to the straight vessels shortly after their origin (see Figure 8). The other posterior hippocampal arteries first extended laterally
division took place close to the dentate gyrus, but in some cases more proximally, that is, close to the parent vessel. The rostral stem was almost always smaller than the caudal one (see Figure 6). It curved rostrally, close to the junction of the head and the body of the hippo- campus, where it often anastomosed with the AHA. When the AHA was absent, it was replaced by the rostral stem of the MHA. In these cases the rostral stem usually anastomosed with the uncal branch of the AChA.
The caudal stem was the true continuation of the MHA (see Figures 6, 7, and 10). It sharply turned cau- dally and extended along the margo denticulatus. It often followed a tortuous course (see Figure 10). The caudal stem very rarely replaced the PHA. It sometimes anasto- mosed with the most rostral PHA (see Figure 10).
The MHA sometimes gave rise to small and large parahippocampal branches, subicular branches, and straight vessels (Figure 7).
The small parahippocampal branches supplied the dorsal surface of the parahippocampal gyrus, which ex- tended, in a broader sense, from the medial margin of that gyrus to the subiculum proper. The large parahippo- campal branches arose less frequently from the MHA than from the AHA (see Figures 7 and 10). The subicular branches irrigated the subiculum. The straight hippo- campal arteries usually supplied the part of the hippo- campal formation that corresponded to the body of the hippocampus. They sometimes also perfused the border zone between the body and the head of the hippocam- pus, but rarely the head itself and very rarely the tail of the hippocampus.
Anastomoses were present among the MHA branches themselves, as well as between the MHA and the AHA and/or the PHA (see Figure 10).
Figure 8. Dorsal view of the SplA U) arising from the distal segment (2) of the right PCA. The SplA gives rise to the PHAs (3 J, some of which give rise to the long straight arteries. (4J Margo denticulatus after removal of the fimbria of the hippocampus.
344 Surg Neurol Marinkovie et al 1992;37:339-49
or laterocaudally and then abruptly turned caudally or caudiomedially along the caudal prolongation of the hip- pocampal formation (see Figures 8 and 10). Some of the arteries divided into two stems before taking the caudal turn. Finally, the straight vessels sometimes arose not only from the PHA but also directly from their parent vessels (from the SplA, for example).
The PHA supplied the tail of the hippocampus and the caudal prolongation of the hippocampal formation.
The Anastomoses
As already mentioned, anastomoses were often present among the hippocampal arteries themselves, as well as among their parahippocampal, subicular, straight, and uncal branches.
In addition to small anastomoses among the parahip- pocampal arteries, which measured 15-20 /~m or less in diameter, larger anastomoses also were sometimes present among these vessels. The anastomoses on the dorsal surface of the parahippocampal gyrus measured 3 0 - 9 0 / 2 m in diameter, and those on its ventromedial surface varied from 30/*m to 80/~m. Anastomoses were sometimes present among the parahippocampal branches of the AHA and the AChA, as well as the internal carotid and the middle cerebral arteries. Finally, in 11.8% of the cases the anastomotic channels were seen to connect the parahippocampal branches of the AHA to the ATA. One of these channels measured as much as 210/a,m in diameter.
Large anastomoses among the subicular branches oc- curred less frequently. They measured from 3 0 - 8 0 / , m in diameter.
Anastomoses were sometimes seen among the straight branches of the hippocampal arteries them- selves, then between them and the main stems of the hippocampal arteries, as well as among their branches to the fimbria of the hippocampus (see Figure 10).
Anastomoses between the hippocampal arteries and the AChA (usually by means of their uncal branches) were present in 52.9% of the cases. They varied from 50/zm to 220/~m in diameter.
Large anastomoses among the hippocampal arteries themselves were noted in 47.1% of the cases. Anasto- moses between the AHA and the MHA, which ranged from 30/~m to 180/a,m in diameter, were observed in 41.2% of the cases. Connecting vessels between the MHA and the PHA, which varied from 30/.~m to 100 /zm in diameter, were seen in 35.3% of the hemispheres. Finally, both sorts of anastomoses in the same hemi- sphere were noted in 29.4%.
In the latter cases a complete arterial arcade was formed along the hippocampal formation. In addition to this large primary arcade short secondary arcades were
Figure 9, The straight arteries (between the two arrows; arising from the left AHA (1~ and MHA ¢2). (3) Margo denticulatus, exposed by the removal of most of the fimbria (4~. (5) Hippocampus. (6~ The subiculum proper. (7_) Dorsal surface of the parahippocampal gyrus.
sometimes present among the subicular branches and/ or the straight arteries (see Figure 10).
The Straight Hippocampal Arteries
The straight arteries are the specific branches of the hippocampal arteries (see Figures 4, 7, 9, and 10). The majority of them ran more or less parallel to each other, across the free surface (the margo denticulatus) of the dentate gyrus. Usually between 30 and 40 straight arter- ies were present in each hemisphere. We observed 0.9-1.2 vessels (mean 0.96) per millimeter. The vessels varied from 30 ~m to 330 ~m in diameter (mean 133 /2m) (see Figure 10). The length of the straight arteries depends on the site of their origin and their penetration. Most of the arteries originated on the margo denticula- tus, but some of them may arise at the level of the subiculum. In general, the caudal straight arteries were longer than the rostral ones (see Figure 8).
The majority of the straight arteries gave rise to one or more collateral and/or terminal branches (see Figure 10). The main stems of the arteries and their branches may penetrate any part of the margo denticulatus, that is, the area between the hippocampal sulcus and the fimbriodentate sulcus (see Figures 9 and 10). Some of them also penetrated the subiculum proper, and the others coursed around the fimbria of the hippocampus (see Figure 10).
The Intrahippocampal Arteries
As noted above, the main stems and the collateral and terminal stems of the straight arteries penetrated the margo denticulatus and sometimes the subiculum proper
Microvascular Anatomy of Hippocampal Arteries Surg Neurol 345 1992;37:339-49
t J 10 f
,oo 10
280 / 12o
130 / 200
150 /
110
90
12
12
Figure 10. The straight hippocampal arteries. The diameters of most of them are labeled by the small numerals. (1) Distal segment (cut) of the left PCA. ~2) CTA. (3) ATA, which gives rise to the MHA (4). The latter artery anastomoses with the uncal branch (5) lcut) of the AChA. (6) Rostral part of the uncal sulcus (fissure) after removal of the uncus. (7_) SplA, which gives rise to the PHAs (8). (9) Dentate gyrus. (10) Fimbria of the hippocampus. Note the large (11) and several small arteries on the subiculum and the dorsal surface (12) of the parahippocampal gyrus.
and then took a curved course through the hippocampal formation (Figure 11). We divided these intrahippocam- pal arteries into the large and the small categories.
Usually two sorts of large arteries, ventral and dorsal, were present. Both of them ranged from 50/zm to 200 /zm in diameter.
The large ventral artery penetrated the medial half of the margo denticulatus and then traversed the ventrome- dial part of the dentate gyrus (Figure 12) or entered the hippocampal sulcus between the dentate gyrus and the subiculum. The artery then took a curved course through the medullary lamina (i.e., the intrahippocampal continu- ation of the hippocampal sulcus) between the dentate gyrus and the CA1 sector of the hippocampus. It gave rise to the lateral branches, which supplied most of the CA1 sector, and sometimes the prosubiculum or a part of the CA2 sector.
The large dorsal artery sometimes followed a course similar to that of the ventral one, but more often it ran between the dentate gyrus and the CA4 sector (see
Figures 11 and 12). It usually supplied the CA2 and the CA3 sectors and sometimes the most dorsal part of the CA1 sector and/or the dentate gyrus.
The small intrahippocampal arteries and arterioles, measuring 15-50/~m in diameter, were divided into the ventral, middle, and dorsal groups.
The small ventral branches originated not only from
Figure 11. Coronal section of the htppocampal formation (method of Spal- teholz). The branches of the straight hippocampal arteries penetrate the entire margo denticulatus, which extends from the hippocampal sulcus (1) to the fimbriodentate sulcus (2). (3) F imbria of the hippocampus. (4) Dentate gyruJ, which is separated from the hippocampus by the medullar lamina (5). Note the sectors of the hippocampus (CA1 through CA4).
346 Surg Neurol Marinkovid et al 1992;37:339-49
Figure 12. Drawing showing the general vascu- lar pattern of the hippocampal formation. Coronal section through a part of the formation that corres- ponds to the body of the hippocampus. (I_) Caudal stem of the MHA, which is displaced slightly medi- ally. The artery gives rise to the subicular branches Q), the parahippocampal vessels (3), and the straight arteries (4). (5) The subiculum proper. (6) Prosubiculum. (7) Margo denticulatus. (8) Den- tate gyrus. (9) Medullar lamina between the dentate gyrus and the hippocampus. (10) Large ventral intrahippocampal artery. CA I through CA4 repre- sent the sectors of the hippocampus. (11) Large dor- sal intrahippocampal artery. (12) Tempora/ horn of the lateral ventricle. (13) Alveus. (14) Ventricular surface of the hippocampus. (15) Fimbria of the hippocampus with its arteries.
the straight vessels but also directly from the hippocam- pal arteries. They usually supplied the subiculum proper and the prosubiculum (see Figure 12). The small middle arteries supplied the dentate gyrus. Finally, the small dorsal vessels, which penetrated the dorsal part of the margo denticulatus and the fimbriodentate sulcus, some- times supplied the CA3 and the CA4 sectors (see Figure 12) and rarely the CA2 sector. A subgroup of the dorsal vessels irrigated the fimbria.
the large ventral artery (see Figure 12). The most dorsal part of this sector was sometimes irrigated by the large dorsal artery. The CA2 sector was mainly supplied by the large dorsal artery (see Figures 11 and 12). The CA3 sector was perfused by the dorsal artery and by the small dorsal branches (see Figure 12). The CA4 sector was irrigated by the small dorsal branches (see Figures 11 and 12).
Most of the dentate gyrus was supplied by the small
The Arterial Supply of the Hippocampal Formation The hippocampal formation comprises the subiculum, the hippocampus (which has been cytoarchitectonically divided into four sectors), and the dentate gyrus. The ventricular surface of the hippocampus is covered by the white matter (the alveus), which forms most of the fimbria (see Figure 12).
The subiculum proper was supplied by the small ven- tral branches that originated from the straight vessels and the hippocampal arteries (see Figure 12). These branches formed a dense network within the subiculum (Figure 13).
The prosubiculum was perfused by the small branches of the straight arteries (see Figure 12) and sometimes by the branches of the large ventral artery.
The CA1 sector of the hippocampus was supplied by
Figure 13. Dense vascular network of the subiculum proper (1) on a coronal section of the hippocampal formation. Q) Medullar lamina. (3) Dentate gyrus. (4) Hippocampal sulcus. Method of Spalteholz.
Microvascular Anatomy of Hippocampal Arteries Surg Neurol 347 1992;37:339-49
Figure 14. Dense capillary network of the pyramidal (1) and the molecular layers (2) of the hippocampus, as well as the molecular layer (3) of the dentate gyrus. (4) Medullary lamina. Coronal section of the hippocampal formation. Method oiC Spaltebo]z.
(short and long) middle arteries. The short arteries and arterioles perfused the medioventral part, and the long ones the laterodorsal part, of that gyrus (see Figures 11 and 12). The most dorsal part of the gyrus was sometimes irrigated by the collateral branches of the large dorsal intrahippocampal artery.
The lateral and the dorsal parts of the alveus received the thin vessels from the branches of the large intrahip- pocampal arteries (see Figure 12). The dorsomedial part of the alveus was supplied by the small dorsal branches, which partially supplied the fimbria (see Figure 12).
The fimbria of the hippocampus had two sorts of small dorsal vessels. Some of these vessels penetrated the ven- tral surface of the fimbria (see Figure 12). The other vessels coursed around the medial margin of the fimbria, where they divided into two thin branches in opposite directions (see Figures 10 and 12). Occasionally there was a longitudinal anastomosis among the adjacent branches (see Figure 10). The branches then abruptly changed their course and traversed the dorsal surface of the fimbria (see Figures 10 and 12).
As to the intrahippocampal capillaries, we found the most dense capillary network within the pyramidal layer and within the molecular layers of both the hippocampus and the dentate gyrus (Figure 14).
Discuss ion
As noted above, there are only several reports about the hippocampal vasculature. These reports can be divided into two groups according to their main topic.
Extrahippocampal Vessek
The reports in the first group mainly deal with the extra- hippocampal vessels [9,19,23,34]. The data in these re-
ports are more or less in agreement with our results. Thus, according to the authors cited the number of hip- pocampal arteries varies from one to six, as compared with the finding of two to seven in our study. Data on the diameters of the hippocampal arteries, their origin, and their division into three groups practically cannot be found in the literature.
The dominant vessel of the hippocampal formation is the MHA. When strong it may replace either the AHA or the PHA. In these cases the MHA supplies most of the hippocampal formation.
There are various findings in the literature concerning the contribution of the AChA to the blood supply of the hippocampal formation. Some authors [9,19] have not mentioned such a possibility. In contrast, some other authors have noted hippocampal branches of the AChA in as much as 87% of the cases [12]. According to our results, however, the AChA took part in the supply of the head of the hippocampus in 58.8% of the cases. In one half of these cases, the AChA gave rise to a few small branches that supplied the most rostral and medial part of the head. In the other half of the specimens the AChA gave rise to a true anterior hippocampal artery, which irrigated a large part or, rarely, the entire head of the hippocampus as well as the rostral part of the dentate gyrus. In all these cases, the hippocampal vessels origi- nated from the uncal branch of the AChA.
In addition to the AChA the hippocampal vessels may originate directly from the distal segment of the PCA or from its collateral branches, especially from the temporal ones. We noted two special sorts of origination of the hippocampal vessels. First, origination of the AHA from the ATA together with the large parahippocampal arter- ies. We named the common origin of these vessels the "rostral hippocampo-parahippocampal arterial com- plex." This complex may supply the head of the hippo- campus, the most rostral parts of the dentate gyrus and the subiculum, the rostral part of the dorsal and ventro- medial surface of the parahippocampal gyrus (especially the entorhinal area), the neighboring part of the tempo- ral lobe, and finally the uncus. The second characteristic origin was seen in relation to the PHAs. These vessels often arose from the SplA and sometimes from the LGA. We discovered the latter vessel a few years ago [16]. It was proved in the present study that the LGA was more often present than we had previously described. What we would like to point out, however, is the following: I1) The PHA, together with the MHA and the AHA, supplies the hippocampal formation, which is especially important for spatial memory [6]. (2) The LGA irrigates the lingual (medial occipitotemporal) gyrus, which is par- tially occupied by the visual cortex [2]. (3) The SplA supplies the splenium of the corpus callosum, which contains the visual commissural fibers [2]. This all could
348 Surg Neurol Marinkovid et al 1992;37:339-49
mean that there is a common blood supply for the brain regions involved in similar functions.
It is clear from our study that the hippocampal arteries may supply not only the hippocampal formation but also the portions of the parahippocampal gyrus and the uncus. The uncal artery is hardly mentioned in the litera- ture [ 19]. This artery was present in 47.1% of our speci- mens. It often anastomosed with the uncal branch of the AChA.
Large and small anastomoses among the hippocampal arteries were often present in our study. Large connect- ing channels among all the hippocampal arteries were noted in 29.4% of the hemispheres. This is consistent with the finding of Muller and Shaw [19] that anasto- motic channels among the AHA, MHA, and the PHA formed a complete arterial arcade. In addition, smaller arcades also may occur. This made Heiman [9] compare such a vascular pattern to the arterial arcades along the intestine. Such a comparison, however, is not quite cor- rect, because the hippocampal arcades are less frequent and less continuous than the paraintestinal and the para- colic arcades. Anyway, in some cases with a complete primarily hippocampal arcade there was also, on the one hand, an anastomosis of the AHA and the ACHA and, on the other hand, an anastomosis between the SplA (which gave rise to a posterior hippocampal artery) and the pericallosal branch of the anterior cerebral artery. In these cases a true arterial ring was actually present that supplied almost the entire limbic lobe.
Intrahippocampal Vessels The second group of reports deals with the intrahippo- campal vessels [6,10,30]. Our findings are more or less in agreement with the results of these studies.
As noted above, the straight arteries, which are branches of the hippocampal arteries, may give rise to large ventral and dorsal intrahippocampal arteries, as well as small ventral, middle, and dorsal branches. In addition, some small ventral branches may also originate directly from the hippocampal arteries. These intrahip- pocampal vessels supply the hippocampal formation in a segmental manner. The vascular segments are more or less wedge-shaped, with apexes corresponding to each straight artery and bases usually located at the level of the ventricular surface of the hippocampus. Individual variations in the size of the segments can be noted in various parts of the hippocampus.
Of the six layers and sublayers of the hippocampus (the alveus, the stratum oriens, the pyramidal layer, the stratum radiatum, the stratum lacunosum, and the mo- lecular layer) we found the highest density of the capil- lary network within the pyramidal and the molecular layers. As to the three layers of the dentate gyrus (the
molecular layer, the stratum granulosum, and the poly- morphic layer) the largest number of capillaries were present within the molecular layer. This is in agreement with the fact that the highest density of the capillaries exists in the regions with the largest number of synapses [6]. The smallest number of capillaries were found in the alveus, the stratum radiatum, and lacunosum of the hippocampus, and the stratum granulosum of the dentate gyrus [6].
It is well known that there are differences in resistance to ischemia in certain regions of the hippocampal forma- tion [6,30]. Thus, the most sensitive part is the CA1 sector, also known as Sommer's sector. The other por- tions of the hippocampus, especially the CA2 and the CA3 (Spielmeyer's sector), are known as the resistant sector. There are certain microvascular anatomical facts that could be, at least partially, the basis of these differ- ences. First, the CA1 sector is supplied by one large (ventral) artery. In contrast, the resistant part is irrigated not only by one large (dorsal) artery but also by several smaller vessels. Second, the CA1 sector has a smaller number of microvessels than the other hippocampal sec- tors. In spite of this, however, it seems that the specific characteristics of the metabolism and the membrane re- ceptors of the CA1 pyramidal neurons are the main reason for their higher sensitivity to ischemia [6].
The hippocampal formation can be affected by many disorders and diseases. Some of them are of special neu- rosurgical interest. This is especially true of aneurysms of the distal segment of the posterior cerebral artery, arteriovenous malformations in the hippocampal region, and some forms of epilepsy.
Saccular or fusiform aneurysms of the distal segment of the PCA are often situated in the ambient cistern [3,5,11,26,32], exactly where most of the hippocampal arteries have their origin. Hence, these aneurysms may compress, stretch, or embolize the hippocampal arteries. The resulting ischemia can cause memory disturbance [7].
Arteriovenous malformations (AVMs) are sometimes located in the hippocampal or the adjacent parahippo- campal region [27,33]. The hippocampal arteries could be the feeding vessels of some of these AVMs.
Intractable "psychomotor epilepsy," that is, complex partial seizures with a focus in the hippocampal forma- tion, indicates neurosurgical intervention [23,25,31]. Several microsurgical approaches to the hippocampal formation can be used in these cases: the transsulcal approach (through the superior temporal sulcus); the inferior temporal approach (through the inferior tempo- ral gyrus); and the retroinsular transventricular approach (through the retrosylvian part of the circular sulcus) [23,31]. Before resection of the hippocampal formation and a portion of the parahippocampal gyrus, their arter-
Microvascular Anatomy of Hippocampal Arteries Surg Neurol 349 1992;37:339-49
ies must be coagulated. From our examination we con- cluded that identification of the hippocampal arteries should not represent any difficulty. Thus, the AHA, after entering the uncal sulcus, extends between the uncus and the parahippocampal gyrus (see Figure 3). Cauteriza- tion of this vessel may also exclude from the circulation some of the rostral parahippocampal arteries and occa- sionally the uncal branch. The MHA lies just caudal to the uncus and has a close relationship with the large LPChA (see Figure 2). Finally, the PHA often arises from the SplA, whose proximal part usually makes a very characteristic curve (see Figure 8). The LGA, which also may give rise to the posterior hippocampal vessels, must be spared during surgery, since its damage could cause a quadrantanopsia [ 16].
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