The Cerebral Cortex of the Pygmy Hippopotamus, Hexaprotodon liberiensis (Cetartiodactyla, Hippopotamidae): MRI, Cytoarchitecture, and Neuronal Morphology

Butti, Camilla; Fordyce, R. Ewan; Raghanti, Mary Ann; Gu, Xiaosi; Bonar, Christopher J.; Wicinski, Bridget; Wong, Edmund; Roman, Jessica; Brake, Alanna; Eaves, Emily; Spocter, Muhammad A.; Tang, Cheuk Y.; Jacobs, Bob; Sherwood, Chet C.; Hof, Patrick R.

doi:10.1002/ar.22875

Cited by 42 publications

(75 citation statements)

References 111 publications

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“…They showed the phylogenetic relatedness of this mammal to both cetaceans and artiodactyls (cetartiodactyls). In most of the aquatic members (including the hippopotamus), layer IV is missing in the primary neocortical areas [Kern et al, 2011;Butti et al, 2014Butti et al, , 2015Knopf et al, 2016], but in terrestrial artiodactyls the situation seems to be somewhat ambiguous (see above). The overall morphology of the cerebral cortex is similar in cetartiodactyls [Butti et al, 2014[Butti et al, , 2015.…”

Section: Neurobiology and Evolutionmentioning

confidence: 99%

“…In most of the aquatic members (including the hippopotamus), layer IV is missing in the primary neocortical areas [Kern et al, 2011;Butti et al, 2014Butti et al, , 2015Knopf et al, 2016], but in terrestrial artiodactyls the situation seems to be somewhat ambiguous (see above). The overall morphology of the cerebral cortex is similar in cetartiodactyls [Butti et al, 2014[Butti et al, , 2015. In this context, the structural comparison of the neocortex in dolphins, hippos, and terrestrial artiodactyls will make an important contribution to neurobiology [Kruska and Röhrs, 1974].…”

Section: Neurobiology and Evolutionmentioning

confidence: 99%

“…The brain of one member of the latter group, the pygmy hippopotamus ( Choeropsis [syn . Hexaprotodon ] liberiensis ) [Wilson and Mittermeier 2011], characterized by a semiaquatic lifestyle, was studied intensively by Butti et al [2014]. They showed the phylogenetic relatedness of this mammal to both cetaceans and artiodactyls (cetartiodactyls).…”

Section: Neurobiology and Evolutionmentioning

confidence: 99%

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Qualitative and Quantitative Analysis of Primary Neocortical Areas in Selected Mammals

et al. 2017

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The present study focuses on the relationship between neocortical structures and functional aspects in three selected mammalian species. Our aim was to compare cortical layering and neuron density in the projection areas (somatomotor, M1; somatosensory, S1; auditory, A1; and visual, V1; each in a wider sense). Morphological and design-based stereological analysis was performed in the wild boar (Sus scrofa scrofa) as a representative terrestrial hoofed animal (artiodactyl) and the common dolphin (Delphinus delphis) as a highly derived related aquatic mammal (cetartiodactyl). For comparison, we included the human (Homo sapiens) as a well-documented anthropoid primate. In the cortex of many mammals, layer IV (inner granular layer) is the main target of specific thalamocortical inputs while layers III and V are the main origins of neocortical projections. Because the fourth layer is indistinct or mostly lacking in the primary neocortex of the wild boar and dolphins, respectively, we analyzed the adjacent layers III and V in these animals. In the human, all the three layers were investigated separately. The stereological data show comparatively low neuron densities in all areas of the wild boar and high cell counts in the human (as expected), particularly in the primary visual cortex. The common dolphin, in general, holds an intermediate position in terms of neuron density but exhibits higher values than the human in a few layers. With respect to the situation in the wild boar, stereological neuron counts in the dolphin are consistently higher, with a maximum in layer III of the visual cortex. The extended auditory neocortical field in dolphins and the hypertrophic auditory pathway indicate secondary neurobiological adaptations to their aquatic habitat during evolution. The wild boar, however, an omnivorous quadruped terrestrial mammal, shows striking specializations as to the sensorimotor neurobiology of the snout region.

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Section: Neurobiology and Evolutionmentioning

confidence: 99%

Section: Neurobiology and Evolutionmentioning

confidence: 99%

Section: Neurobiology and Evolutionmentioning

confidence: 99%

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Qualitative and Quantitative Analysis of Primary Neocortical Areas in Selected Mammals

et al. 2017

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“…Artiodactyls express thousands of OR and some V1R (cows, 40 intact genes), but not functional V2R [Shi and Zhang, 2007], whereas cetaceans possess about 60 OR and very few V1R genes (mink whales, two intact genes; bottlenose dolphins, one gene) and lack V2R [Yim et al, 2014;Kishida et al, 2015a]. Unlike in cetaceans, a pair of large olfactory bulbs [Garrod, 1880;Butti et al, 2014] and peripheral vomeronasal organs [Estes, 1991;pers. obs.…”

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confidence: 99%

Histological Properties of Main and Accessory Olfactory Bulbs in the Common Hippopotamus

Kondoh

Watanabe²,

Nishihara³

et al. 2017

Brain Behav Evol

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The olfactory system of mammals comprises a main olfactory system that detects hundreds of odorants and a vomeronasal system that detects specific chemicals such as pheromones. The main (MOB) and accessory (AOB) olfactory bulbs are the respective primary centers of the main olfactory and vomeronasal systems. Most mammals including artiodactyls possess a large MOB and a comparatively small AOB, whereas most cetaceans lack olfactory bulbs. The common hippopotamus (Hippopotamus amphibius) is semiaquatic and belongs to the order Cetartiodactyla, family Hippopotamidae, which seems to be the closest extant family to cetaceans. The present study evaluates the significance of the olfactory system in the hippopotamus by histologically analyzing the MOB and AOB of a male common hippopotamus. The MOB comprised six layers (olfactory nerve, glomerular, external plexiform, mitral cell, internal plexiform, and granule cell), and the AOB comprised vomeronasal nerve, glomerular, plexiform, and granule cell layers. The MOB contained mitral cells and tufted cells, and the AOB possessed mitral/tufted cells. These histological features of the MOB and the AOB were similar to those in most artiodactyls. All glomeruli in the AOB were positive for anti-G_αi2, but weakly positive for anti-G_αo, suggesting that the hippopotamus vomeronasal system expresses vomeronasal type 1 receptors with a high affinity for volatile compounds. These findings suggest that the olfactory system of the hippopotamus is as well developed as that of other artiodactyl species and that the hippopotamus might depend on its olfactory system for terrestrial social communication.

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“…The variety of NPNFP-ir neuron subtypes exhibited by the manatee appears to be related to phylogeny; most mammalian taxa exhibit greater diversity in NPNFP-ir neuron morphology in the cortex than is observed in the boreoeutherian lineage (e.g. primates, rodents, carnivores and cetartiodactyls), where NPNFPir neurons tend to be more limited to pyramidal morphologies [Sherwood et al, 2009;Jacobs et al, 2011;Butti et al, 2014Butti et al, , 2015Jacobs et al, 2015].…”

Section: Npnfp-ir Neuronsmentioning

confidence: 99%

Neuron Types in the Presumptive Primary Somatosensory Cortex of the Florida Manatee (Trichechus manatus latirostris)

Reyes

Stimpson²,

Gupta³

et al. 2015

Brain Behav Evol

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Within afrotherians, sirenians are unusual due to their aquatic lifestyle, large body size and relatively large lissencephalic brain. However, little is known about the neuron type distributions of the cerebral cortex in sirenians within the context of other afrotherians and aquatic mammals. The present study investigated two cortical regions, dorsolateral cortex area 1 (DL1) and cluster cortex area 2 (CL2), in the presumptive primary somatosensory cortex (S1) in Florida manatees (Trichechus manatus latirostris) to characterize cyto- and chemoarchitecture. The mean neuron density for both cortical regions was 35,617 neurons/mm³ and fell within the 95% prediction intervals relative to brain mass based on a reference group of afrotherians and xenarthrans. Densities of inhibitory interneuron subtypes labeled against calcium-binding proteins and neuropeptide Y were relatively low compared to afrotherians and xenarthrans and also formed a small percentage of the overall population of inhibitory interneurons as revealed by GAD67 immunoreactivity. Nonphosphorylated neurofilament protein-immunoreactive (NPNFP-ir) neurons comprised a mean of 60% of neurons in layer V across DL1 and CL2. DL1 contained a higher percentage of NPNFP-ir neurons than CL2, although CL2 had a higher variety of morphological types. The mean percentage of NPNFP-ir neurons in the two regions of the presumptive S1 were low compared to other afrotherians and xenarthrans but were within the 95% prediction intervals relative to brain mass, and their morphologies were comparable to those found in other afrotherians and xenarthrans. Although this specific pattern of neuron types and densities sets the manatee apart from other afrotherians and xenarthrans, the manatee isocortex does not appear to be explicitly adapted for an aquatic habitat. Many of the features that are shared between manatees and cetaceans are also shared with a diverse array of terrestrial mammals and likely represent highly conserved neural features. A comparative study across manatees and dugongs is necessary to determine whether these traits are specific to one or more of the manatee species, or can be generalized to all sirenians.

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The Cerebral Cortex of the Pygmy Hippopotamus, Hexaprotodon liberiensis (Cetartiodactyla, Hippopotamidae): MRI, Cytoarchitecture, and Neuronal Morphology

Cited by 42 publications

References 111 publications

Qualitative and Quantitative Analysis of Primary Neocortical Areas in Selected Mammals

Qualitative and Quantitative Analysis of Primary Neocortical Areas in Selected Mammals

Histological Properties of Main and Accessory Olfactory Bulbs in the Common Hippopotamus

Neuron Types in the Presumptive Primary Somatosensory Cortex of the Florida Manatee <b><i>(Trichechus manatus latirostris)</i></b>

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