Hippocampal pyramidal cells: the reemergence of cortical lamination

Abstract

The increasing resolution of tract-tracing studies has led to the definition of segments along the transverse axis of the hippocampal pyramidal cell layer, which may represent functionally defined elements. This review will summarize evidence for a morphological and functional differentiation of pyramidal cells along the radial (deep to superficial) axis of the cell layer. In many species, deep and superficial sublayers can be identified histologically throughout large parts of the septotemporal extent of the hippocampus. Neurons in these sublayers are generated during different periods of development. During development, deep and superficial cells express genes (Sox5, SatB2) that also specify the phenotypes of superficial and deep cells in the neocortex. Deep and superficial cells differ neurochemically (e.g. calbindin and zinc) and in their adult gene expression patterns. These markers also distinguish sublayers in the septal hippocampus, where they are not readily apparent histologically in rat or mouse. Deep and superficial pyramidal cells differ in septal, striatal, and neocortical efferent connections. Distributions of deep and superficial pyramidal cell dendrites and studies in reeler or sparsely GFP-expressing mice indicate that this also applies to afferent pathways. Histological, neurochemical, and connective differences between deep and superficial neurons may correlate with (patho-) physiological phenomena specific to pyramidal cells at different radial locations. We feel that an appreciation of radial subdivisions in the pyramidal cell layer reminiscent of lamination in other cortical areas may be critical in the interpretation of studies of hippocampal anatomy and function.

Quantitative ultrastructural analysis of basket and axo-axonic cell terminals in the mouse hippocampus

“…Some properties of CA1 pyramidal cells depend on the vertical soma-position inside the layer (Slomianka et al, 2011), and, although we did not plan to test such differences, our samples were taken from different sublayers to have a better representation, and we did not notice any differences in perisomatic innervation.…”

On the Value of Reptilian Brains to Map the Evolution of the Hippocampal Formation

“…In reptiles, a more elementary terminology is used for cortical regions, medial, dorsal, and lateral cortex, each with only a single layer of principal cells. Can we find a region homologous to the mammalian hippocampal formation within the reptilian cortex, especially when considering the multilayered architecture of several hippocampal regions such as CA1 and the subiculum [Slomianka et al, 2011]? Surveying the literature and recent reviews, the answer seems to be yes.…”

“…For example, smaller neuronal populations such as mossy cells or the CA2 region, recent objects of renewed interest [Dudek et al, 2016;Scharfman, 2016], have no proposed reptilian equivalents. Also, most regions of the mammalian medial pallium, at least between CA1 and the entorhinal cortex [Slomianka et al, 2011], contain multiple cellular layers. Because reptilian cortex contains only one principal cell layer, the interpretation of layer-specific markers remains difficult [Puelles et al, 2017].…”

Trading new neurons for status: Adult hippocampal neurogenesis in eusocial Damaraland mole-rats

“…In fact, Damaraland mole-rats harbours similar numbers of granule cells than laboratory mice (Calhoun et al, 1998, Abusaad et al, 1999, Fabricius et al, 2008) despite a body weight up to six times higher than that of laboratory mice. Like other mole-rats, Damaraland mole-rats show a prominent CA3 layer and lamination of the CA1 layer (Slomianka et al, 2011). Calbindin and parvalbumin staining of the Damaraland mole-rat is similar to that of the solitary Cape mole-rat, the deep calbindin+ pyramidal cells present in the CA3 of naked mole-rats are however absent in the Damaraland mole-rat (Amrein et al, 2014).…”

“…Since neurogenesis declines with age, species with long life spans typically show low rates of neurogenesis as adults (Amrein et al, 2011). However, life spans are not uniform amongst the different castes of a mole-rat colony, breeding animals may live twice as long as their non-breeding counterparts (Dammann et al, 2011).…”