The brain of the tree pangolin ( Manis tricuspis ). IV. The hippocampal formation

Ajao

et al. 2019

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The diencephalon (dorsal thalamus, ventral thalamus, and epithalamus) and the hypothalamus, play central roles in the processing of the majority of neural information within the central nervous system. Given the interactions of the diencephalon and hypothalamus with virtually all portions of the central nervous system, the comparative analysis of these regions lend key insights into potential neural, evolutionary, and behavioral specializations in different species. Here, we continue our analysis of the brain of the tree pangolin by providing a comprehensive description of the organization of the diencephalon and hypothalamus using a range of standard and immunohistochemical staining methods. In general, the diencephalon and hypothalamus of the tree pangolin follow the organization typically observed across mammals. No unusual structural configurations of the ventral thalamus, epithalamus, or hypothalamus were noted. Within the dorsal thalamus, the vast majority of typically identified nuclear groups and component nuclei were observed. The visual portion of the tree pangolin dorsal thalamus appears to be organized in a manner not dissimilar to that seen in most nonprimate and noncarnivore mammals, and lacks certain features that are present in the closely related carnivores. Within the ventral medial geniculate nucleus, a modular organization, revealed with parvalbumin neuropil immunostaining, is suggestive of specialized auditory processing in the tree pangolin. In addition, a potential absence of hypothalamic cholinergic neurons is suggestive of unusual patterns of sleep. These observations are discussed in an evolutionary and functional framework regarding the phylogeny and life history of the pangolins.

Section: Introductionmentioning

confidence: 83%

The brain of the tree pangolin (Manis tricuspis). V. The diencephalon and hypothalamus

Imam

Ajao

et al. 2019

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“…Our analysis revealed no clear indications of the presence of either the CA2 or CA4 fields in both species of carnivore studied. Previous investigations of the cornu Ammonis region in other carnivores, such as the domestic dog, and closely related species, such as the tree pangolin, have hinted at the possible presence of the CA2 field (Amayasu et al, 1999; Hof et al, 1996; Imam et al, 2019), but this field is reported to be absent in the domestic cat (Hirama et al, 1997), and was not noted in the red fox (Amrein & Slomianka, 2010). Despite this, the CA2 region is regularly reported as a distinct field in the laboratory rat/mouse and primates, and has been associated specifically with social memory (e.g., Botcher et al, 2014; Dudek, Alexander, & Farris, 2016; Hitti & Siegelbaum, 2014; Kohara et al, 2014; Tzakis & Holahan, 2019).…”

Section: Discussionmentioning

confidence: 99%

“…In the current study, immunostaining for vesicular glutamate transporter 2 clearly revealed two of these sublamina of the molecular layer of the dentate gyrus in the banded mongoose, but this immunostain did not reveal these sublamina in the domestic ferret. In the African elephant, up to four sublaminae of the molecular layer were revealed with calretinin immunostaining (Patzke et al, 2014), while in the tree pangolin vesicular glutamate transporter 2, calbindin and calretinin immunostaining revealed the presence of three sublaminae (Imam et al, 2019), matching that observed in laboratory rodents (Witter, 2007). In most mammals the granule cell layer is considered a single entity with no sublamina (Witter, 2007), but in the present study vesicular glutamate transporter 2 immunostaining revealed the presence of three sublaminae in the banded mongoose (outer, middle, and inner) but not the domestic ferret.…”

Section: The Sublamination Of the Dentate Gyrusmentioning

confidence: 99%

“…The CA region and dentate gyrus intertwine, while the subicular complex and entorhinal cortex are generally found on the ventral surface of the cerebral hemisphere (Amayasu, Shoumura, Ichinohe, Yu, & Yonekura, 1999; Duvernoy et al, 2013; Hirama, Shoumura, Ichinohe, You, & Yonekura, 1997; Hof, Rosenthal, & Fiskum, 1996). While the CA region can be divided into four fields (CA1–CA4), the presence of the CA2 and CA4 regions is variably reported, and their presence debated, across mammals (e.g., Amaral & Lavenex, 2007; Jones & McHugh, 2011; Mercer, Trigg, & Thomson, 2007); however, this controversy is primarily based on studies of laboratory rodents and various species of primates (e.g., Botcher, Falck, Thomson, & Mercer, 2014), while the presence or absence of the CA2 and CA4 fields appears less contentious in less commonly studied species (e.g., Amayasu et al, 1999; Imam, Bhagwandin, Ajao, Ihunwo, & Manger, 2019). The dentate gyrus, which shares borders with the CA3 field, is one region of the brain where adult neurogenesis occurs, and this has been reported in a range of mammalian species (e.g., Chawana et al, 2013; Epp, Barker, & Galea, 2009; Patzke et al, 2015; van Praag et al, 2002), with the cetaceans being the only noted exception to date (Patzke et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

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The hippocampal formation of two carnivore species: The feliform banded mongoose and the caniform domestic ferret

Pillay

Bertelsen

et al. 2020

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Employing cyto-, myelo-, and chemoarchitectural staining techniques, we analyzed the structure of the hippocampal formation in the banded mongoose and domestic ferret, species belonging to the two carnivoran superfamilies, which have had independent evolutionary trajectories for the past 55 million years. Our observations indicate that, despite the time since sharing a last common ancestor, these species show extensive similarities. The four major portions of the hippocampal formation (cornu Ammonis, dentate gyrus, subicular complex, and entorhinal cortex) were readily observed, contained the same internal subdivisions, and maintained the topological relationships of these subdivisions that could be considered typically mammalian. In addition, adult hippocampal neurogenesis was observed in both species, occurring at a rate similar to that observed in other mammals. Despite the overall similarities, several differences to each other, and to other mammalian species, were observed. We could not find evidence for the presence of the CA2 and CA4 fields of the cornu Ammonis region. In the banded mongoose the dentate gyrus appears to be comprised of up to seven lamina, through the sublamination of the molecular and granule cell layers, which is not observed in the domestic ferret. In addition, numerous subtle variations in chemoarchitecture between the two species were observed. These differences may contribute to an overall variation in the functionality of the hippocampal formation between the species, and in comparison to other mammalian species. These similarities and variations are important to understanding to what extent phylogenetic affinities and constraints affect potential adaptive evolutionary plasticity of the hippocampal formation.

“…Here we expand our systematic analysis of the brain of the tree pangolin (Imam, Ajao, Bhagwandin, Ihunwo, & Manger, ; Imam et al, ; Imam et al, ; Imam, Bhagwandin, Ajao, Ihunwo, & Manger, ; Imam, Bhagwandin, Ajao, & Manger, ) by providing a detailed account of the architecture of the tree pangolin brainstem and cerebellum (diencephalic prosomere 1 through to rhombomere 11) using Nissl and myelin staining in conjunction with a range of immunohistochemical stains.…”

Section: Introductionmentioning

confidence: 99%

The brain of the tree pangolin (Manis tricuspis). VI. The brainstem and cerebellum

Imam

Ajao

et al. 2019

Self Cite

The brainstem (midbrain, pons, and medulla oblongata) and cerebellum (diencephalic prosomere 1 through to rhombomere 11) play central roles in the processing of sensorimotor information, autonomic activity, levels of awareness and the control of functions external to the conscious cognitive world of mammals. As such, comparative analyses of these structures, especially the understanding of specializations or reductions of structures with functions that have been elucidated in commonly studied mammalian species, can provide crucial information for our understanding of the behavior of less commonly studied species, like pangolins. In the broadest sense, the nuclear complexes and subdivisions of nuclear complexes, the topographical arrangement, the neuronal chemistry, and fiber pathways of the tree pangolin conform to that typically observed across more commonly studied mammalian species. Despite this, variations in regions associated with the locus coeruleus complex, auditory system, and motor, neuromodulatory and autonomic systems involved in feeding, were observed in the current study. While we have previously detailed the unusual locus coeruleus complex of the tree pangolin, the superior olivary nuclear complex of the auditory system, while not exhibiting additional nuclei or having an altered organization, this nuclear complex, particularly the lateral superior olivary nucleus and nucleus of the trapezoid body, shows architectonic refinement. The cephalic decussation of the pyramidal tract, an enlarged hypoglossal nucleus, an additional subdivision of the serotonergic raphe obscurus nucleus, and the expansion of the superior salivatory nucleus, all indicate neuronal specializations related to the myrmecophagous diet of the pangolins.