Structures Joined to the Hippocampus

The hippocampus is prolonged by the subiculum (the "bed" of the hippocampus), which, from an anatomical point of view, forms part of the parahippo-campal gyrus. The end of the stratum radiatum of CA1 is considered to mark the division between the cornu Ammonis and the subiculum (Figs. 7, 8) (Lorente de No 1934; Blackstad 1956; Braak 1980). The subiculum itself is divided into several segments (Fig. 5; Powell and Hines 1975; Williams 1995): (1) the prosubiculum, which continues CA1 (and whose existence is not accepted by all), (2) the subiculum proper, partly hidden by the gyrus dentatus, (3) the presubiculum, whose small, superficial pyramidal neurons are packed in clusters, making it characteristically maculate (see Figs. 113B, 114B; Braak 1980; Amaral et al. 1984), and (4) the parasubiculum, which passes around the margin of the parahippo-campal gyrus to the entorhinal area on the medial aspect of the gyrus. The entorhinal area (Brod-mann's area 28) is itself poorly demarcated (Amaral et al. 1987). Although its presence in the uncus and anterior end of the parahippocampal gyrus (Figs. 4, 16,18) is generally accepted, its posterior extension along the parahippocampal gyrus is uncertain. This posterior extension is thought to be marked in humans where the entorhinal area is well developed (Jacobs et al. 1979; Braak 1980; Hyman et al. 1986). Its special structure will be described later together with its functions (see p. 26, 28).

The amygdala, which belongs to the limbic lobe, is often described together with the hippocampus as far as its function is concerned. Its structure, as described by Braak and Braak (1983) and Amaral et al. (1992), is shown in Fig. 14. The cortical and medial nuclei are olfactory centers, whereas the basal, lateral, and central nuclei have limbic functions (Aggle-ton 1992), which are described on p. 30.

From an anatomical point of view, the limbic lobe maybe divided into limbic and intralimbic gyri. According to its structure, however, the limbic lobe is usually divided into the allocortex, including the hippocampus (cornu Ammonis and gyrus dentatus), the proximal part of the subiculum, and the in-dusium griseum (the amygdala is often included in this group), and the periallocortex, made up of the transitional cortex between the allocortex and isocortex, including the cingulate and parahippocam-pal gyri (Schwerdtfeger 1984; Chronister and White 1975; Jacobs et al. 1979; Braak 1980; Van Hoesen 1982; Swanson 1983; Kier et al. 1995). (Text continued on p. 26)

Lobe Frontal Cironconvolution

Fig. 1. A Drawing and B dissection showing the inferomedial 5, calcarine sulcus; 6, occipital lobe (cuneus); 7, parietal lobe, aspect of the right hemisphere. Bar, 10 mm medial aspect (precuneus); 8, cingulate gyrus; 9, frontal lobe,

1, hippocampus, only partly visible on the inferomedial sur- medial aspect (superior frontal gyrus); 10, corpus callosum;

face of the temporal lobe; 2, parahippocampal gyrus (T5); 11, fornix; 12, third ventricle 3, fusiform gyrus (T4); 4, inferior temporal gyrus (T3);

Fig. 1. A Drawing and B dissection showing the inferomedial 5, calcarine sulcus; 6, occipital lobe (cuneus); 7, parietal lobe, aspect of the right hemisphere. Bar, 10 mm medial aspect (precuneus); 8, cingulate gyrus; 9, frontal lobe,

1, hippocampus, only partly visible on the inferomedial sur- medial aspect (superior frontal gyrus); 10, corpus callosum;

face of the temporal lobe; 2, parahippocampal gyrus (T5); 11, fornix; 12, third ventricle 3, fusiform gyrus (T4); 4, inferior temporal gyrus (T3);

Small Intestine
Fig. 1 B
Parahippocampal Gyrus Mri

Fig. 2. A, B Coronal section of the brain. A Head section. Bar, 10 mm. B 3T MRI view, ^-weighted image 1, hippocampus; 2, parahippocampal gyrus; 3, fusiform gyrus; 4, inferior temporal gyrus; 5, middle temporal gyrus; 6, superior temporal gyrus; 7, lateral fissure; 8, postcentral gyrus; 9, central sulcus; 10, precentral gyrus; 11, superior

Fig. 2. A, B Coronal section of the brain. A Head section. Bar, 10 mm. B 3T MRI view, ^-weighted image 1, hippocampus; 2, parahippocampal gyrus; 3, fusiform gyrus; 4, inferior temporal gyrus; 5, middle temporal gyrus; 6, superior temporal gyrus; 7, lateral fissure; 8, postcentral gyrus; 9, central sulcus; 10, precentral gyrus; 11, superior frontal gyrus; 12, cingulate gyrus; 13, corpus callosum; 14, lateral ventricle; 14' caudate nucleus; 15, thalamus; 16, putamen; 17, temporal (inferior) horn of the lateral ventricle; 18, red nucleus; 19, substantia nigra; 20, pons; 21, tentorium cerebelli; 22, ambient cistern

Fig. 2. B 3T MRI view

Fig. 3. Intraventricular aspect of the hippocampus. The temporal horn has been opened and the choroid plexuses removed. Bar, 6.5 mm

I, hippocampal body; 2, head and digitationes hippocampi (internal digitations); 3, hippocampal tail; 4, fimbria; 5, crus of fornix; 6, subiculum; 7, splenium of the corpus callosum; 8, calcar avis; 9, collateral trigone; 10, collateral eminence;

II, uncal recess of the temporal horn

Calcarine Avis

Fig. 4. A Drawing and B dissection showing a sagittal section, right hemisphere. The limbic lobe is separated from the isocortex by the limbic fissure and may be divided into two gyri: the limbic and intralimbic gyri. The line a-a indicates the plane of the section on Fig. 5. Bar, 7.7 mm Limbic fissure: 1, anterior paraolfactory sulcus (subcallosal sulcus); 2, cingulate sulcus; 3, subparietal sulcus; 4, anterior calcarine sulcus; 5, collateral sulcus; 6, rhinal sulcus. Limbic gyrus: 7, subcallosal gyrus; 8, posterior paraolfactory sulcus; 9, cingulate gyrus; 10, isthmus; 11, parahippocampal gyrus,

Fig. 4. A Drawing and B dissection showing a sagittal section, right hemisphere. The limbic lobe is separated from the isocortex by the limbic fissure and may be divided into two gyri: the limbic and intralimbic gyri. The line a-a indicates the plane of the section on Fig. 5. Bar, 7.7 mm Limbic fissure: 1, anterior paraolfactory sulcus (subcallosal sulcus); 2, cingulate sulcus; 3, subparietal sulcus; 4, anterior calcarine sulcus; 5, collateral sulcus; 6, rhinal sulcus. Limbic gyrus: 7, subcallosal gyrus; 8, posterior paraolfactory sulcus; 9, cingulate gyrus; 10, isthmus; 11, parahippocampal gyrus, posterior part; 11', parahippocampal gyrus, anterior part (piriform lobe). Piriform lobe: 12, entorhinal area; 13, ambient gyrus; 14, semilunar gyrus; 15, prepiriform cortex. Intralimbic gyrus: 16, prehippocampal rudiment; 16', paraterminal gyrus; 17, indusium griseum. Hippocampus: 18, gyrus denta-tus; 19, cornu Ammonis; 20, gyri of Andreas Retzius; 21, fimbria (displaced upwards, arrows); 22, uncal apex; 23, band of Giacomini; 24, uncinate gyrus; 25, anterior perforated substance; 26, anterior commissure; 27, fornix; 28, corpus callo-sum

Fig. 4. B

Fig. 5. A Development of the gyrus dentatus (dotted area) and of the cornu Ammonis (hatched area) towards B their definitive disposition. Arrows indicate the hippocampal sulcus (superficial part). (Modified after Williams 1995) 1, cornu Ammonis; 2, gyrus dentatus; 3, hippocampal sulcus (deep or vestigial part); 4, fimbria; 5, prosubiculum; 6, sub-iculum proper; 7, presubiculum; 8, parasubiculum; 9, ento-

Fig. 5. A Development of the gyrus dentatus (dotted area) and of the cornu Ammonis (hatched area) towards B their definitive disposition. Arrows indicate the hippocampal sulcus (superficial part). (Modified after Williams 1995) 1, cornu Ammonis; 2, gyrus dentatus; 3, hippocampal sulcus (deep or vestigial part); 4, fimbria; 5, prosubiculum; 6, sub-iculum proper; 7, presubiculum; 8, parasubiculum; 9, ento-

rhinal area; 10, parahippocampal gyrus; 11, collateral sulcus; 12, collateral eminence; 13, temporal (inferior) horn of the lateral ventricle; 14, tail of caudate nucleus; 15, stria terminalis; 16, choroid fissure and choroid plexuses; 17, lateral geniculate body; 18, lateral part of the transverse fissure (wing of ambient cistern); 19, ambient cistern; 20, mesencephalon; 21, pons; 22, tentorium cerebelli

Fig. 6. Site of CA1 and CA3 in rats and humans (see p. 8). Arrowheads show the hippocampal sulcus. The arrow indicates the inversion of arrangements in the hippocampus in these two species

CA1, superior region; CA3, inferior region; Th, thalamus

Fig. 6. Site of CA1 and CA3 in rats and humans (see p. 8). Arrowheads show the hippocampal sulcus. The arrow indicates the inversion of arrangements in the hippocampus in these two species

CA1, superior region; CA3, inferior region; Th, thalamus

Subiculum Layers

Fig. 7. A, B Diagram and 9.4T MRI view ofthe structure ofthe hippocampus (coronal section) CA1-CA4, fields of the cornu Ammonis. Cornu Ammonis: 1, alveus; 2, stratum oriens; B, stratum pyramidale; 3', stratum lucidum; 4, stratum radia-tum; 5, stratum lacunosum; 6, stratum moleculare; 7, vestigial hippocampal sulcus (note a residual cavity, 7'). Gyrus den-tatus: B, stratum moleculare; 9, stratum granulosum;

1G, polymorphic layer; 11, fimbria; 12, margo denticulatus; 13, fimbriodentate sulcus; 14, superficial hippocampal sulcus; 15, subiculum; 16, choroid plexuses; 17, tail of caudate nucleus; 1B, temporal (inferior) horn ofthe lateral ventricle

Stratum Oriens
B

Fig. 8. Coronal section of the hippocampal body after intravascular India ink injection. The layers of the hippocampus (see Fig. 7) can be distinguished due to differences in their vascular density. The stratum moleculare of the cornu Am-monis (8) and that of the gyrus dentatus (9) are separated by the vestigial hippocampal sulcus (10). Note the high vascular density of the subiculum (11) in comparison to that ofthe adjacent stratum radiatum of CA1 (7), Bar, 1.5 mm

Fig. 8. Coronal section of the hippocampal body after intravascular India ink injection. The layers of the hippocampus (see Fig. 7) can be distinguished due to differences in their vascular density. The stratum moleculare of the cornu Am-monis (8) and that of the gyrus dentatus (9) are separated by the vestigial hippocampal sulcus (10). Note the high vascular density of the subiculum (11) in comparison to that ofthe adjacent stratum radiatum of CA1 (7), Bar, 1.5 mm

Cornu Ammonis: 1 -4, CA1-CA4 (fields ofthe cornu Ammo-nis). Sublayers of CA1: 5, alveus; 6, stratum pyramidale; 7, strata radiatum and lacunosum; 8, stratum moleculare. Gyrus dentatus: 9, stratum moleculare; 10, vestigial hippocampal sulcus; 11, subiculum; 12, margo denticulatus; 13, superficial hippocampal sulcus; 14, fimbriodentate sulcus; 15, fimbria; 16, choroid plexuses; 17, tail of caudate nucleus; 18, temporal (inferior) horn of the lateral ventricle

Gyrus Dentatus

Fig. 9. Enlargement of the dentata area. The gyrus dentatus leculare. Cornu Ammonis: 4, stratum moleculare; 5, stratum and CA4 together form the area dentata. Silver impregnation, lacunosum; 6, stratum lucidum; 7, alveus; 8, fimbria; 9, fim-

Bodian. Bar, 590 |im briodentate sulcus; 10, margo denticulatus; 11, superficial

CA1-CA4, fields of the cornu Ammonis. Gyrus dentatus: hippocampal sulcus 1, polymorphic layer; 2, stratum granulosum; 3, stratum mo-

Fig. 9. Enlargement of the dentata area. The gyrus dentatus leculare. Cornu Ammonis: 4, stratum moleculare; 5, stratum and CA4 together form the area dentata. Silver impregnation, lacunosum; 6, stratum lucidum; 7, alveus; 8, fimbria; 9, fim-

Bodian. Bar, 590 |im briodentate sulcus; 10, margo denticulatus; 11, superficial

CA1-CA4, fields of the cornu Ammonis. Gyrus dentatus: hippocampal sulcus 1, polymorphic layer; 2, stratum granulosum; 3, stratum mo-

Hippocampal Structure

Fig. 10. A, B Structure of the hippocampus. A Silver impregnation (Bodian). B Intravascular India ink injection, showing the varying density of the vascular network in different hippocampal layers. Note high vascular density in the stratum moleculare of the cornu Ammonis (1). Bar, 600 |im Cornu Ammonis: A, alveus; SO, stratum oriens; SPy, stratum pyramidale; SR, stratum radiatum; SL, stratum lacunosum;

Fig. 10. A, B Structure of the hippocampus. A Silver impregnation (Bodian). B Intravascular India ink injection, showing the varying density of the vascular network in different hippocampal layers. Note high vascular density in the stratum moleculare of the cornu Ammonis (1). Bar, 600 |im Cornu Ammonis: A, alveus; SO, stratum oriens; SPy, stratum pyramidale; SR, stratum radiatum; SL, stratum lacunosum;

SM, stratum moleculare; HS, vestigial hippocampal sulcus. Gyrus dentatus: SM1, stratum moleculare, external two thirds; SM2, stratum moleculare, inner third; SG, stratum granulosum; PL, polymorphic layer; CA4, field of the cornu Ammonis. 1, Stratum moleculare; 2, external part of stratum moleculare of the gyrus dentatus; 3, inner part, highly vascularized; 4, stratum granulosum, poorly vascularized

Fig. 12. Neuronal types in the gyrus dentatus. Silver impregnation, Bodian. Bar, 85 |im

1, stratum moleculare, external part; 2, stratum moleculare, inner part; 3, stratum granulosum; 4, polymorphic layer

Fig. 11. Neuronal types in the cornu Ammonis. Silver impregnation, Bodian. Bar, 52 |im

CA1-CA4, fields of the cornu Ammonis

Fig. 12. Neuronal types in the gyrus dentatus. Silver impregnation, Bodian. Bar, 85 |im

1, stratum moleculare, external part; 2, stratum moleculare, inner part; 3, stratum granulosum; 4, polymorphic layer

Stratum Pyramidal Structure

Fig. 13. Overview of the principal connections of pyramidal (A) and granular (B) neurons

CA, cornu Ammonis; GD, gyrus dentatus. 1, axon of a pyramidal neuron; 2, Schaffer collateral; 3, basket cell; 4, basal dendrite; 5, apical dendrite; 6, apical dendrite of a granular neuron; 7, axon (mossy fiber) of a granular neuron; 8, connections of a basal dendrite of a pyramidal neuron with other pyramidal neurons and with septal and commissural fibers; 9, mossy fibers (stratum lucidum into CA3); 10, septal and commissural fibers; 11,12, Schaffer collaterals; 13,14, perfo rant path; 15, commissural fibers; 16, septal fibers. Layers of the cornu Ammonis: alveus, stratum oriens (STR. ORIENS), stratum pyramidale (STR. PYR.), stratum lucidum (STR. LUC.), stratum radiatum (STR. RAD.), stratum lacunosum (STR. LAC.), stratum moleculare (STR. MOL.), vestigial hippocampal sulcus (HIP. SUL.). Layers of the gyrus dentatus: stratum moleculare, external two thirds (STR. MOL. 2/3), stratum moleculare, inner third (STR. MOL. 1/3), stratum granulosum (STR. GR.), polymorphic layer (POLY. LAY.)

Stratum Pyramidal Structure

Fig. 14. A, B Structure of the amygdala. A Drawing of a coronal section. B Intravascular India ink injection. Bar, 1.8 mm 1, lateral nucleus; 2, basal nucleus; 3, accessory basal nucleus; 4, cortical nucleus; 5, medial nucleus; 6, central nucleus; 7, anterior perforated substance; 8, anterior commissure, lateral part; 9, putamen; 10, claustrum; 11, uncal recess of the temporal horn; 12, ambient gyrus

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    What structures are surrounding the hippocampus?
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