Reflections on the Structural-Functional Evolution of the Hippocampus: What Is the Big Deal about a Dentate Gyrus

Abstract

The vertebrate hippocampal formation has been central in discussions of comparative cognition, nurturing an interest in understanding the evolution of variation in hippocampal organization among vertebrate taxa and the functional consequences of that variation. Assuming some similarity between the medial pallium of extant amphibians and the hippocampus of stem tetrapods, we propose the hypothesis that the hippocampus of modern amniotes began with a medial pallium characterized by a relatively undifferentiated cytoarchitecture, more direct thalamic and olfactory sensory inputs, and a broad role in associative learning and memory processes that nonetheless included the map-like representation of space. From this modest beginning evolved the cognitively more specialized hippocampal formation of birds and the hippocampus of mammals with its confounding dentate gyrus. Much has been made of trying to identify a dentate homologue in birds, but there are compelling reasons to believe no such structural homologue/functional equivalent exists. The uniqueness of the mammalian dentate then raises the question of what might be the functional consequences of a hippocampus with a dentate compared to one without. One might be tempted to speculate that the presence of a dentate gyrus facilitates so-called pattern separation, but birds with their suspected dentate-less hippocampus display excellent hippocampal-dependent pattern separation relying on space. Perhaps one consequence of a dentate is a hippocampus better designed to process a broader array of stimuli beyond space to more robustly support episodic memory. What is clear is that any meaningful reconstruction of hippocampal evolution and the eventual identification of any subdivisional homologies will require more data on the neurobiological and functional properties of the nonmammalian hippocampus, particularly those of amphibians and reptiles.

Of Horse-Caterpillars and Homologies: Evolution of the Hippocampus and Its Name

“…All amniotes share some features, such as the presence of double pyramidal cells (neurons with dendritic trees that extend both superficially and deep to the cell body layer), while some features are shared among some but not all amniotes, and some, possibly including the presence or at least elaboration of a distinct dentate gyrus, may be unique to only one clade -mammals in the case of the dentate gyrus [Striedter, 2016;Bingman and Muzio, 2017]. Among the variable features are the number of architectonically distinct subdivisions, the patterns of efferent projections -such as whether a particular region projects to the septum or other subcortical targets or not, the extent to which the cell bodies conform to a strictly trilaminar morphology or are more scattered, and the degree to which the system of axon collaterals is developed.…”

“…Although amphibians have a well-delineated medial pallium, the region most likely to be homologous to the amniote hippocampus lacks any suggestion of a trilaminar structure [Herrick, 1948;Wilczynski and Northcutt, 1983;Bingman and Muzio, 2017], i.e., a single cell body layer bordered on either side by a neuropil region containing incoming fiber tracts and the dendrites of the cell bodies. A second marked disparity is the lack of the double pyramidal cell morphology, i.e., neuron cell bodies that have both apical and basal dendritic trees, that diagnostically characterizes the amniote hippocampus [Tömböl, 1995;Luis de la Iglesia and Lopez-Garcia, 1997].…”

“…Previous studies in amphibians indicated only a secondary role at best for the telencephalon, including the medial pallium, in spatial orientation, it being focused instead on exerting a regulatory influence on the optic tectum [Patton and Grobstein, 1998]. However, in spite of the substantial morphological and connectional differences between the medial pallia of amphibians and amniotes, recent evidence in toads has demonstrated medial pallial participation in navigation by use of external geometric cues [Sotelo et al, 2016;Bingman and Muzio, 2017]. The function of spatial navigation by the hippocampal formation thus appears to be a shared feature across tetrapods.…”

The interoceptive hippocampus: mouse brain endocrine receptor expression highlights a dentate gyrus (DG)–cornu ammonis (CA) challenge– sufficiency axis

“…Preliminary inspection of the microarray-based Allan Human Brain Atlas (http://human.brain-map.org/) fully confirms selective endocrine receptor expression in human HPC, consistent with internal sensing deficits in HPC-ablated patient H.M. [3], but the human data (from elderly individuals) are not strictly comparable to the analyzed data from young mice (and are therefore not presented). There are also hints that DG/CA patterning may be less well conserved in human (not presented), but we note that strict conservation of this patterning across vertebrates is unlikely because, for example, birds and reptiles lack a morphological dentate gyrus (e.g., [56]). Indeed, there is no a priori reason why physical segregation of challenge versus sufficiency signaling should be necessary.…”

Comparing cognition by integrating concept learning, proactive interference, and list memory

“…Following from the previous section that the two corvid bird species performed somewhat better than monkeys in the early stages of learning a same/different abstract concept raises an intriguing issue about whether nutcrackers and/or magpies might share event-based proactive interference with nonhuman primates or time-based proactive interference with pigeons, the other bird species. If the outcome would be the former, with nutcrackers and/or magpies sharing event-based proactive interference with nonhuman primates, then it might shed some light on the role of the dentate gyrus of the primate hippocampal formation in episodic memory because birds do not have a dentate gyrus (e.g., Bingman & Muzio, 2017).…”