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J Comp Neurol. 2016 Jul 1;524(10):2036-58. doi: 10.1002/cne.23930. Epub 2016 Feb 18.

Organization of the sleep-related neural systems in the brain of the river hippopotamus (Hippopotamus amphibius): A most unusual cetartiodactyl species.

Author information

1
School of Anatomical Sciences, Faculty of Health Sciences, University of the Witwatersrand, Parktown 2193, Johannesburg, Republic of South Africa.
2
Department of Anatomy, Des Moines University, Des Moines, Iowa, 50312.
3
Center for Zoo and Wild Animal Health, Copenhagen Zoo, 2000, Fredericksberg, Denmark.
4
Department of Psychiatry, University of California, Los Angeles, Neurobiology Research 151A3, Veterans Administration Sepulveda Ambulatory Medical Center, North Hills, California, 91343.

Abstract

This study provides the first systematic analysis of the nuclear organization of the neural systems related to sleep and wake in the basal forebrain, diencephalon, midbrain, and pons of the river hippopotamus, one of the closest extant terrestrial relatives of the cetaceans. All nuclei involved in sleep regulation and control found in other mammals, including cetaceans, were present in the river hippopotamus, with no specific nuclei being absent, but novel features of the cholinergic system, including novel nuclei, were present. This qualitative similarity relates to the cholinergic, noradrenergic, serotonergic, and orexinergic systems and is extended to the γ-aminobutyric acid (GABA)ergic elements of these nuclei. Quantitative analysis reveals that the numbers of pontine cholinergic (259,578) and noradrenergic (127,752) neurons, and hypothalamic orexinergic neurons (68,398) are markedly higher than in other large-brained mammals. These features, along with novel cholinergic nuclei in the intralaminar nuclei of the dorsal thalamus and the ventral tegmental area of the midbrain, as well as a major expansion of the hypothalamic cholinergic nuclei and a large laterodorsal tegmental nucleus of the pons that has both parvocellular and magnocellular cholinergic neurons, indicates an unusual sleep phenomenology for the hippopotamus. Our observations indicate that the hippopotamus is likely to be a bihemispheric sleeper that expresses REM sleep. The novel features of the cholinergic system suggest the presence of an undescribed sleep state in the hippopotamus, as well as the possibility that this animal could, more rapidly than other mammals, switch cortical electroencephalographic activity from one state to another. J. Comp. Neurol. 524:2036-2058, 2016.

KEYWORDS:

Cetacea; Cetartiodactyla; RRID AB_10000321; RRID AB_10000323; RRID AB_10000340; RRID AB_10000343; RRID AB_2079751; RRID AB_91545; brain evolution; hippopotami; mammalian sleep; unihemispheric sleep

PMID:
26588600
DOI:
10.1002/cne.23930
[Indexed for MEDLINE]

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