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Perspectives PERSPECTIVES Anterior hippocampus anatomy OPINION In humans, the hippocampus is cradled by the parahippocampal gyrus, which is Anterior hippocampus: the anatomy positioned beneath it. The anterior part of the parahippocampal gyrus bends over and rests upon itself, forming the uncus. of perception, imagination and The various gyri that are visible on the surface of the brain (BOX 1) cover both episodic memory the amygdala and the anterior portion of the hippocampus. Beneath this surface, Peter Zeidman and Eleanor A. Maguire the hippocampus is divided into cytoar- chitectonically defined subfields. These are Abstract | The brain creates a model of the world around us. We can use this commonly thought of as being arranged representation to perceive and comprehend what we see at any given moment, in a canonical circuit, which can be but also to vividly re‑experience scenes from our past and imagine future (or even visualized in the cross-section of the main fanciful) scenarios. Recent work has shown that these cognitive functions — body of the hippocampus (FIG. 1). In this perception, imagination and recall of scenes and events — all engage the anterior circuit, neurons in the entorhinal cortex (EC), which is part of the neighbouring hippocampus. In this Opinion article, we capitalize on new findings from functional parahippocampal gyrus, project to the neuroimaging to propose a model that links high‑level cognitive functions to dentate gyrus (DG), which in turn drives specific structures within the anterior hippocampus. subfield CA3 then CA2, CA1 and the subiculum. The subiculum and CA1 then project back to the EC. Also visible in this The hippocampus is critical for learning, However, we are only beginning to plane are regions related to, but distinct memory and cognition. It is one of understand the precise anatomy of this from, the subiculum: the prosubiculum, the most studied brain structures in brain region in humans10, and consequently the presubiculum and the parasubiculum. neuroscience, and efforts to understand little is known about the specific structures The prosubiculum is situated between its functions continue apace. In particular, within the anterior hippocampus CA1 and the subiculum. However, despite there is considerable interest in functional that contribute to these important many differences between its connectivity differences between neural populations cognitive functions. and that of the subiculum12, these two located at different points along its anterior– In this article, we focus on the human regions are not normally separated in posterior axis1–5. A recent literature review3 anterior hippocampus. We summarize human neuroimaging because their showed that, in addition to the gradients current knowledge of its anatomy and borders are not visible with MRI. The of gene expression and connectivity that highlight a striking consistency in the presubiculum and the parasubiculum are vary along the length of the hippocampus, functional MRI (fMRI) literature, which situated between the subiculum and the the anterior portion of the hippocampus suggests that specific substructures EC. These regions can be delineated with (also known as the head, ventral or within the anterior hippocampus make high-resolution MRI10, which offers new temporal region) can be distinguished critical contributions to episodic memory, opportunities to study their functions from the intermediate and posterior imagination and visual scene perception. in humans. sections (also known as the tail, dorsal or Claims that the hippocampus (and the Understanding the arrangement of the septal regions) by sharp changes in these medial temporal lobes more generally) subfields in the anterior hippocampus functional characteristics. performs functions beyond memory (such requires awareness of their three-di- Owing to its complex anatomy, the as visual perception) are heavily contested11, mensional shape. The main body of the anterior hippocampus (particularly that particularly because it is difficult to design hippocampus bends medially in its anterior of humans) has proved to be difficult experiments that unequivocally control for portion (FIG. 1a) to form the extraventricular to study6. It has an intricate structure memory encoding and retrieval. We propose part of the anterior hippocampus, which with unique cellular morphology and is a model of anterior hippocampal function is positioned within the uncus. As a result, positioned at the junction between the that takes into account the importance CA1 and the subiculum must bend around parahippocampal gyrus, the amygdala of anatomical detail and refers to known a wider radius than the other subfields13. and the posterior hippocampus. It has connectivity across species; this model Thus, the most anterior portion of the widespread connectivity, and hippocampal may help to clarify recent discussions of hippocampus is dominated by CA1 and lesions that include damage to the anterior functional differences in the long axis of the the subiculum (FIG. 1b), whereas the more hippocampus have a deleterious effect hippocampus1–4 as well as the relationship posterior part of the uncus contains only on learning, memory and navigation7–9. between visual perception and memory. the DG, CA2 and CA3 (FIG. 1d). After the NATURE REVIEWS | NEUROSCIENCE ADVANCE ONLINE PUBLICATION | 1 ©2016 Mac millan Publishers Li mited. All ri ghts reserved. PERSPECTIVES medial turn within the uncus, the subfields mossy fibres project from the DG to Importantly, there are differences in bend upwards, ascending vertically towards CA3, and upon reaching distal CA3 the hippocampal anatomy of different the amygdala (FIG. 1b,c), which changes they change direction to extend 3–5 mm species. The uncus is particularly highly their orientation from the coronal to the in the anterior direction17. By contrast, developed in primates, and the degree to axial plane. associational and local connections within which it is homologous to its counterpart Subfields within the uncus have cellular the DG — which may have excitatory and in rodents is uncertain10,13. There are also ‘peculiarities’ (REF. 14): for example, CA1 inhibitory roles, respectively16 — extend differences in connectivity. Whereas rodents in the uncus — referred to as CA1’ — has bidirectionally along much of the length have commissural connections along the smaller and more densely packed neurons of the hippocampus. The DG in the uncus length of the hippocampus, in monkeys than CA1 in the body of the hippocampus13 is connected to the anterior DG in the these connections are largely restricted to (note that CA1’ is labelled uncal subiculum main body of the hippocampus through anterior regions, particularly the uncus18. in an alternative nomenclature15). The these associational projections16. The In monkeys, cells in the DG of the uncus vertical part of the uncus has particularly connection from CA3 to CA1 (the Schaffer project via the white matter of the fimbria differentiated cytoarchitecture — for collaterals) and connections within CA3 or fornix, before crossing hemispheres via instance, vertical CA1’ contains more also have longitudinal projections through the ventral hippocampal commissure19, densely packed pyramidal cell bodies than most of the hippocampus17. Once again, returning along the same pathway in horizontal CA1’ or CA1 of the hippocampal the uncus is distinct, with the targets of the opposite hemisphere to terminate body10. The functional implications of these projections of the uncal CA3 (CA3’) being in the contralateral uncus. Other regions cellular differences are unknown. largely confined to CA3’ and CA1’. The associated with the hippocampus — the Although the subfields are usually human hippocampus can therefore be presubiculum, the EC and the posterior studied in slices perpendicular to the divided into subfields in the main body parahippocampal cortex — connect across hippocampal long axis (the coronal plane of the hippocampus that are connected in hemispheres via the dorsal hippocampal in humans; see FIG. 1b–e), connections cross-section and longitudinally, as well as commissure. These findings point to a also extend through the length of the modified subfields that comprise the uncus striking role for the anterior hippocampus hippocampus16,17. In the coronal plane and have more limited connectivity with in connecting the hippocampi of each and with a slight anterior inclination, the anterior hippocampus. hemisphere. It has been suggested that Box 1 | A tour of the anterior hippocampus The anterior hippocampus may be understood in terms of its uncal sulcus. Moving posteriorly along the uncus (towards the right cytoarchitecture (see the main text) or in terms of the features that are of the figure), the gyrus ambiens becomes the uncinate gyrus, which visible on the surface of the brain, which are summarized here based on contains the hippocampal–amygdaloid transition area (HATA) previous observations10,13,94. See part a of the figure for context. Dashed (FIG. 1b,c). Next, the uncus becomes the band of Giacomini and finally lines labelled b–e correspond to the coronal slices shown in FIG. 1. the intralimbic gyrus, getting progressively smaller towards the Starting in the parahippocampal gyrus and moving anteriorly (towards posterior. The point at which the intralimbic gyrus is no longer visible the left of the figure), the gyrus becomes the entorhinal cortex (EC). in coronal section is a landmark for the posterior-most slice of the Its approximate position is indicated
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