The Human Periallocortex: Layer Pattern in Presubiculum, Parasubiculum and Entorhinal Cortex. A Review

Abstract

The cortical mantle is not homogeneous, so that three types of cortex can be distinguished: allocortex, periallocortex and isocortex. The main distinction among those three types is based on morphological differences, in particular the number of layers, overall organization, appearance, etc., as well as its connectivity. Additionally, in the phylogenetic scale, this classification is conserved among different mammals. The most primitive and simple cortex is the allocortex, which is characterized by the presence of three layers, with one cellular main layer; it is continued by the periallocortex, which presents six layers, although with enough differences in the layer pattern to separate three different fields: presubiculum (PrS), parasubiculum (PaS), and entorhinal cortex (EC). The closest part to the allocortex (represented by the subiculum) is the PrS, which shows outer (layers I–III) and inner (V–VI) principal layers (lamina principalis externa and lamina principalis interna), both separated by a cell poor band, parallel to the pial surface (layer IV or lamina dissecans). This layer organization is present throughout the anterior-posterior axis. The PaS continues the PrS, but its rostrocaudal extent is shorter than the PrS. The organization of the PaS shows the layer pattern more clearly than in the PrS. Up to six layers are recognizable in the PaS, with layer IV as lamina dissecans between superficial (layers I–III) and deep (V–VI) layers, as in the PrS. The EC presents even more clearly the layer pattern along both mediolateral and rostrocaudal extent. The layer pattern is a thick layer I, layer II in islands, layer III medium pyramids, layer IV as lamina dissecans (not present throughout the EC extent), layer V with dark and big pyramids and a multiform layer VI. The EC borders laterally the proisocortex (incomplete type of isocortex). Variations in the appearance of its layers justify the distinction of subfields in the EC, in particular in human and nonhuman primates. EC layers are not similar to those in the neocortex. The transition between the periallocortical EC and isocortex is not sharp, so that the proisocortex forms an intervening cortex, which fills the gap between the periallocortex and the isocortex.

Cytoarchitecture and myeloarchitecture of the entorhinal cortex of the common marmoset monkey (Callithrix jacchus)

“…The deep layers V and VI are more developed in the caudal levels (EI, ECC, and ECl) than in the rostral levels (EO, ER, and EL) in the marmoset, with large size and darkly stained cells, a high density of myelin, and the absence of sublayers. In others monkeys, up to three sublayers are described in Layer V: two superficial cellular Layers (Va and Vb) in rats (Witter et al, ) and a deeper, fiber‐rich layer (Vc) in monkeys (Amaral et al, ) and humans (Insausti et al, ). In our preparations, we did not subdivide the deep layers because the lamination pattern was not evident.…”

“…Based on the organization of the afferent and efferent connections, together with the distributions of AChE and heavy metals and Golgi‐impregnated preparations, Amaral et al () defined seven subdivisions in the monkey EC. Eight subdivisions have been described in the human EC: olfactory, rostral, lateral rostral and caudal, medial intermediate, intermediate, caudal, and caudal limiting (Insausti et al, ; Insausti et al, ). Our parcellation is thus largely consistent with that originally described in M. fascicularis .…”

“…Along its extent, the EC presents a clear six-layered pattern. The number and names of the layers have changed over the years, but the common notion of six layers predominates (Insausti et al, 2017). Cortical outputs and intrinsic circuits between neurons located in the different layers contribute to the information processing carried out by the EC (Piguet, Chareyron, Banta Lavenex, Amaral, & Lavenex, 2018;Witter & Moser, 2006).…”

“…The entorhinal cortex (EC) is a prominent structure that occupies the ventromedial portion of the rostral temporal lobe. The EC is part of the periallocortex, together with the hippocampus, presubiculum, and parasubiculum (Brodmann, 1909;Insausti, Muñoz-López, Insausti, & Artacho-Pérula, 2017), and is regarded as a fundamental point between the hippocampal formation and several other cortical areas (Insausti, Marcos, Arroyo-Jiménez, Blaizot, & Martínez-Marcos, 2002;Witter, Doan, Jacobsen, Nilssen, & Ohara, 2017). Brodmann (1909) first divided the primate EC portion of Broadmann's area 28 into a rostral-lateral region (or A28b) and a caudal-medial region (or A28a), based on specific difference in the lamination patterns.…”

Differences in functional connectivity along the anterior-posterior axis of human hippocampal subfields

“…Together with the recent observation that even different regions of the pre/parasubiculum may facilitate distinct forms of mental imagery (Dalton et al, 2018), the current findings provide persuasive evidence that neuroimaging investigations of the hippocampus should, at the very least, differentiate between the pre/parasubiculum and the subiculum proper when investigating contributions of this complex region to human cognition. Indeed, Insausti et al (2017) recently suggested that the concept of a 'subicular cortex' may be incorrect considering it combines the differentiable subicular allocortex (comprising 3 layers) and the pre/parasubicular periallocortex (comprising 6 layers). Our results provide support for this distinction at a functional level.…”