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

Anatomical Record

Volumn 297, Issue 4, 2014, Pages 670-700

  Butti, Camilla ^a   Ewan fordyce, R ^b   Ann Raghanti, Mary ^c   Gu, Xiaosi ^a,d   Bonar, Christopher J ^e   Wicinski, Bridget A ^a   Wong, Edmund W ^a   Roman, Jessica ^a   Brake, Alanna ^a   Eaves, Emily ^a   Spocter, Muhammad A ^f   Tang, Cheuk Y ^a   Jacobs, Bob ^g   Sherwood, Chet C ^h   Hof, Patrick R ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF OTAGO   (New Zealand)

^c KENT STATE UNIVERSITY   (United States)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e Dallas Zoological Society   (United States)

^f DES MOINES UNIVERSITY   (United States)

^g Department of Psychology   (United States)

^h GEORGE WASHINGTON UNIVERSITY   (United States)

Author keywords

Artiodactyls; Cetaceans; Cytoarchitecture; Hippopotamids; Mammalian evolution; Neocortex

Indexed keywords

CALRETININ;

ANIMAL TISSUE; ANTERIOR CINGULATE; ANTERIOR INSULA; ARCHICORTEX; ARTICLE; BRAIN CORTEX; BRAIN SIZE; CELL STRUCTURE; CEREBELLUM; CORPUS CALLOSUM; CYTOARCHITECTURE; ENTORHINAL CORTEX; FEMALE; FRONTAL CORTEX; GOLGI STAIN; HEXAPROTODON LIBERIENSIS; HIPPOCAMPUS; HISTOLOGY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; NERVE CELL; NEUROANATOMY; NISSL STAINING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; OCCIPITAL CORTEX; PALEOCORTEX; PARIETAL CORTEX; POSTERIOR CINGULATE; POSTERIOR INSULA; PREGENUAL CORTEX; PRIORITY JOURNAL; PYGMY HIPPOPOTAMUS; RETROSPLENIAL CORTEX; SMALL MAMMAL; SUBGENUAL CORTEX; TEMPORAL CORTEX;

ARTIODACTYLA; CETACEA; CETARTIODACTYLA; HEXAPROTODON; HEXAPROTODON LIBERIENSIS; HIPPOPOTAMIDAE; HIPPOPOTAMUS AMPHIBIUS; MAMMALIA;

ARTIODACTYLS; CETACEANS; CYTOARCHITECTURE; HIPPOPOTAMIDS; MAMMALIAN EVOLUTION; NEOCORTEX;

ANIMALS; ARTIODACTYLA; BIOLOGICAL EVOLUTION; CEREBRAL CORTEX; FEMALE; IMMUNOENZYME TECHNIQUES; MAGNETIC RESONANCE IMAGING; NEURONS;

EID: 84896314064     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.22875     Document Type: Article

References (136)

1. Agnarsson I, May-Collado LJ. 2008. The phylogeny of Cetartiodactyla: the importance of dense taxon sampling, missing data, and the remarkable promise of cytochrome b to provide reliable species-level phylogenies. Mol Phyl Evol 48:964-985.
2. Allman JM, Tetreault NA, Hakeem AY, Manaye KF, Semendeferi K, Erwin JM, Goubert V, Hof PR. 2010. The von Economo neurons in frontoinsular and anterior cingulate cortex of great apes and humans. Brain Struct Funct 214:495-517.
3. Alouf J. 1929. Die vergleichlende Cytoarchitektonik der Area striata. J Psychol Neurol 38:5-41.
4. Andressen C, Blümcke I, Celio MR. 1993. Calcium-binding proteins: selective markers of nerve cells. Cell Tissue Res 271:181-208.
5. Baimbridge KG, Celio MR, Rogers JH. 1992. Calcium-binding proteins in the nervous system. Trends Neurosci 15:303-308.
6. Boisserie J. 2005. The phylogeny and taxonomy of Hippopotamidae (Mammalia: Artiodactyla): a review based on morphology and cladistic analysis. Zool J Linn Soc 143:1-26.
7. Boisserie JR, Fisher RE, Lihoreau F, Weston EM. 2011. Evolving between land and water: key questions on the emergence and history of the Hippopotamidae (Hippopotamoidea, Cetancodonta, Cetartiodactyla). Biol Rev 86:975-975.
8. Breathnach AS. 1955. The surface features of the brain of the humpback whale (Megaptera novaeangliae). J Anat 89:343-354.
9. Breathnach AS. 1960. The cetacean central nervous system. Biol Rev 35:187-230.
10. Breathnach AS, Goldby F. 1954. The amygdaloid nuclei, hippocampus and other parts of the rhinencephalon in the porpoise (Phocaena phocaena). J Anat 88:267-291.
11. Butti C, Hof PR. 2010. The insular cortex: a comparative perspective. Brain Struct Funct 214:477-493.
12. Butti C, Raghanti MA, Sherwood CC, Hof PR. 2011. The neocortex of cetaceans: cytoarchitecture and comparison with other aquatic and terrestrial species. Ann NY Acad Sci 1225:47-58.
13. Butti C, Sherwood CC, Hakeem AY, Allman JM, Hof PR. 2009. Total number and volume of Von Economo neurons in the cerebral cortex of cetaceans. J Comp Neurol 515:243-259.
14. Campbell A. 1905. Histological studies on the localisation of cerebral function. Cambridge: University Press.
15. Condé F, Lund JS, Jacobowitz DM, Baimbridge KG, Lewis DA. 1994. Local circuit neurons immunoreactive for calretinin, calbindin D-28k or parvalbumin in monkey prefrontal cortex: distribution and morphology. J Comp Neurol 341:95-116.
16. Corbet GB. 1969. The taxonomic status of the pygmy hippopotamus, Choeropsis liberiensis, from the Niger Delta. J Zool 158:387-394.
17. Davila JC, Padial J, Andreu MJ, Real MA, Guirado S. 1997. Calretinin immunoreactivity in the cerebral cortex of the lizard Psammodromus algirus: a light and electron microscopic study. J Comp Neurol 382:382-393.
18. DeFelipe J. 1993. Neocortical neuronal diversity: chemical heterogeneity revealed by colocalization studies of classic neurotransmitters, neuropeptides, calcium-binding proteins, and cell surface molecules. Cereb Cortex 3:273-289.
19. DeFelipe J. 1997. Types of neurons, synaptic connections and chemical characteristics of cells immunoreactive for calbindin-D28K, parvalbumin and calretinin in the neocortex. J Chem Neuroanat 14:1-19.
20. Eltringham S. 1993a. The common hippopotamus (Hippopotamus amphibius). In: Oliver WLR, editor. Pigs, peccaries and hippos: status survey and action plan. IUCN, The World Conservation Union, Gland, Switzerland. p 71-87.
21. Eltringham S. 1993b. The pygmy hippopotamus (Hexaprotodon liberiensis). In: Oliver WLR, editor. Pigs, peccaries and hippos: status survey and action plan. IUCN, The World Conservation Union, Gland, Switzerland. p 87-94.
22. Eltringham S. 1999. The hippos: natural history and conservation. London: Academic Press.
23. Evrard HC, Forro T, Logothetis NK. 2012. Von Economo neurons in the anterior insula of the macaque monkey. Neuron 74:482-489.
24. Fajardo C, Escobar MI, Buritica E, Arteaga G, Umbarila J, Casanova MF, Pimienta H. 2008. Von Economo neurons are present in the dorsolateral (dysgranular) prefrontal cortex of humans. Neurosci Lett 435:215-218.
25. Fay JM. 2004. In the land of the surfing hippos. Natl Geogr Mag 206:100.
26. Ferrer I, Perera M. 1988. Structure and nerve cell organisation in the cerebral cortex of the dolphin Stenella coeruleoalba: a golgi study. With special attention to the primary auditory area. Anat Embryol 178:161-173.
27. Filimonoff IN. 1965. On the so-called rhinencephalon in the dolphin. J Hirnforsch 8:1-23.
28. Furutani R. 2008. Laminar and cytoarchitectonic features of the cerebral cortex in the Risso's dolphin (Grampus griseus), striped dolphin (Stenella coeruleoalba), and bottlenose dolphin (Tursiops truncatus). J Anat 213:241-248.
29. Garey LJ, Takacs J, Revishchin AV, Hamori J. 1989. Quantitative distribution of GABA-immunoreactive neurons in cetacean visual cortex is similar to that in land mammals. Brain Res 485:278-284.
30. Garrod AH. 1880. On the brain and other parts of the hippopotamus (H. amphibius). Trans Zool Soc Lond 11:11-17.
31. Gatesy J. 1997. More DNA support for a Cetacea/Hippopotamidae clade: the blood-clotting protein gene gamma-fibrinogen. Mol Biol Evol 14:537-543.
32. Gilbert CD. 1983. Microcircuitry of the visual cortex. Annu Rev Neurosci 6:217-247.
33. Gingerich PD. 2005. Cetacea. In: Rose KD, Archibald JD, editors. Placental mammals: origin, timing, and relationships of the major extant clades. Baltimore: Johns Hopkins University Press. p 234-252.
34. Gingerich PD, Uhen MD. 1998. Likelihood estimation of the time of origin of cetacean and the time of divergence of Cetacea and Artiodactyla. Paleo Electron 2:1-47.
35. Glezer, II, Hof PR, Leranth C, Morgane PJ. 1993. Calcium-binding protein-containing neuronal populations in mammalian visual cortex: a comparative study in whales, insectivores, bats, rodents, and primates. Cereb Cortex 3:249-272.
36. Glezer, II, Hof PR, Morgane PJ. 1992. Calretinin-immunoreactive neurons in the primary visual cortex of dolphin and human brains. Brain Res 595:181-188.
37. Glezer, II, Hof PR, Morgane PJ. 1998. Comparative analysis of calcium-binding protein-immunoreactive neuronal populations in the auditory and visual systems of the bottlenose dolphin (Tursiops truncatus) and the macaque monkey (Macaca fascicularis). J Chem Neuroanat 15:203-237.
38. Glezer, II, Morgane PJ. 1990. Ultrastructure of synapses and golgi analysis of neurons in neocortex of the lateral gyrus (visual cortex) of the dolphin and pilot whale. Brain Res Bull 24:401-427.
39. Glezer I. 2002. Neural morphology. In: Hoelzel AR, editor. Marine mammal biology: an evolutionary approach: Oxford: Blackwell Science. p 98-115.
40. Glezer I, Jacobs, MS, Morgane, PJ. 1988. Implications of the "initial brain" concept for brain evolution in Cetacea. Behav Brain Sci 11:75-116.
41. Gonchar Y, Burkhalter A. 1997. Three distinct families of GABAergic neurons in rat visual cortex. Cereb Cortex 7:347-358.
42. Grubb P. 1993. The Afro-tropical hippopotamuses-hippopotamidae-Hippopotamus and Hexaprotodon. In: Oliver WLR, editor. Pigs, peccaries and hippos: status survey and action plan. IUCN, The World Conservation Union, Gland, Switzerland. p 68-71.
43. Gruenberger H. 1970. On the cerebral anatomy of the Amazon dolphin Inia geoffrensis. Invest Cetacea 2:129-146.
44. Hakeem AY, Sherwood CC, Bonar CJ, Butti C, Hof PR, Allman JM. 2009. Von Economo neurons in the elephant brain. Anat Rec 292:242-248.
45. Hof PR, Bogaert YE, Rosenthal RE, Fiskum G. 1996a. Distribution of neuronal populations containing neurofilament protein and calcium-binding proteins in the canine neocortex: regional analysis and cell typology. J Chem Neuroanat 11:81-98.
46. Hof PR, Chanis R, Marino L. 2005. Cortical complexity in cetacean brains. Anat Rec 287:1142-1152.
47. Hof PR, Glezer, II, Condé F, Flagg RA, Rubin MB, Nimchinsky EA, Vogt Weisenhorn DM. 1999. Cellular distribution of the calcium-binding proteins parvalbumin, calbindin, and calretinin in the neocortex of mammals: phylogenetic and developmental patterns. J Chem Neuroanat 16:77-116.
48. Hof PR, Glezer, II, Nimchinsky EA, Erwin JM. 2000. Neurochemical and cellular specializations in the mammalian neocortex reflect phylogenetic relationships: evidence from primates, cetaceans, and artiodactyls. Brain Behav Evol 55:300-310.
49. Hof PR, Rosenthal RE, Fiskum G. 1996b. Distribution of neurofilament protein and calcium-binding proteins parvalbumin, calbindin, and calretinin in the canine hippocampus. J Chem Neuroanat 11:1-12.
50. Hof PR, Sherwood CC. 2005. Morphomolecular neuronal phenotypes in the neocortex reflect phylogenetic relationships among certain mammalian orders. Anat Rec 287:1153-1163.
51. Hof PR, Van der Gucht E. 2007. Structure of the cerebral cortex of the humpback whale, Megaptera novaeangliae (Cetacea, Mysticeti, Balaenopteridae). Anat Rec 290:1-31.
52. Innocenti GM, Manger PR, Masiello I, Colin I, Tettoni L. 2002. Architecture and callosal connections of visual areas 17, 18, 19 and 21 in the ferret (Mustela putorius). Cereb Cortex 12:411-422.
53. IUCN Red List of Threatened Species. 2013 (Version 2013.2). www.iucnredlist.org. Accessed 23 January 2014.
54. Jacobs B, Lubs J, Hannan M, Anderson K, Butti C, Sherwood CC, Hof PR, Manger PR. 2011. Neuronal morphology in the African elephant (Loxodonta africana) neocortex. Brain Struct Funct 215:273-298.
55. Jacobs MS, Galaburda AM, McFarland WL, Morgane PJ. 1984. The insular formations of the dolphin brain: quantitative cytoarchitectonic studies of the insular component of the limbic lobe. J Comp Neurol 225:396-432.
56. Jacobs MS, McFarland WL, Morgane PJ. 1979. The anatomy of the brain of the bottlenose dolphin (Tursiops truncatus). Rhinic lobe (Rhinencephalon): The archicortex. Brain Res Bull 4(Suppl 1):1-108.
57. Jacobs MS, Morgane PJ, McFarland WL. 1971. The anatomy of the brain of the bottlenose dolphin (Tursiops truncatus). Rhinic lobe (rhinencephalon). I. The paleocortex. J Comp Neurol 141:205-271.
58. Kellogg ME, Burkett S, Dennis TR, Stone G, Gray BA, McGuire PM, Zori RT, Stanyon R. 2007. Chromosome painting in the manatee supports Afrotheria and Paenungulata. BMC Evol Biol 7:6.
59. Kesarev VS, Malofeeva LI. 1969. Structural organization of the motor zone of the cerebral cortex in dolphins. Arkh Anat Gistol Embriol 56:48-55.
60. Kojima T. 1951. On the brain of the sperm whale (Physeter catodon L). Sci Rep Whales Res Inst Tokyo 6:49-72.
61. Kubota Y, Hattori R, Yui Y. 1994. Three distinct subpopulations of GABAergic neurons in rat frontal agranular cortex. Brain Res 649:159-173.
62. Ladygina TF, Mass AM, Supin A. 1978. Multiple sensory projections in the dolphin cerebral cortex. Zh Vyssh Nerv Deiat Im I P Pavlova 28:1047-1053.
63. Ladygina TF, Supin A. 1977. Localization of the sensory projection areas in the cerebral cortex of the dolphin, Tursiops truncatus. Zh Evol Biokhim Fiziol 13:712-718.
64. Lende R, Akdikmen, S. 1968. Motor field in cerebral cortex of the bottlenose dolphin. J Neurosurg 29:495-499.
65. Lende RA, Welker WI. 1972. An unusual sensory area in the cerebral neocortex of the bottlenose dolphin, Tursiops truncatus. Brain Res 45:555-560.
66. Lydekker R. 1915. Catalogue of the ungulate mammals in the British museum (Natural History). London: Order of Trustees.
67. Manger PR, Hemingway J, Haagensen M, Gilissen E. 2010. Cross-sectional area of the elephant corpus callosum: comparison to other eutherian mammals. Neuroscience 167:815-824.
68. Manger PR, Nakamura H, Valentiniene S, Innocenti GM. 2004. Visual areas in the lateral temporal cortex of the ferret (Mustela putorius). Cereb Cortex 14:676-689.
69. Manger PR, Prowse M, Haagensen M, Hemingway J. 2012. Quantitative analysis of neocortical gyrencephaly in African elephants (Loxodonta africana) and six species of cetaceans: comparison with other mammals. J Comp Neurol 520: 2430-2439.
70. Manger PR, Sum M, Szymanski M, Ridgway SH, Krubitzer L. 1998. Modular subdivisions of dolphin insular cortex: does evolutionary history repeat itself? J Cogn Neurosci 10:153-166.
71. Marin-Padilla M. 1990. Three dimensional organization of layer I of the human cerebral cortex: a Golgi study. J Comp Neurol 299:89-105.
72. Marino L. 2007. Cetacean brains: how aquatic are they? Anat Rec 290:694-700.
73. Marino L, Murphy TL, Deweerd AL, Morris JA, Fobbs AJ, Humblot N, Ridgway SH, Johnson JI. 2001a. Anatomy and three-dimensional reconstructions of the brain of the white whale (Delphinapterus leucas) from magnetic resonance images. Anat Rec 262:429-439.
74. Marino L, Murphy TL, Gozal L, Johnson JI. 2001b. Magnetic resonance imaging and three-dimensional reconstructions of the brain of a fetal common dolphin, Delphinus delphis. Anat Embryol 203:393-402.
75. Marino L, Rilling JK, Lin SK, Ridgway SH. 2000. Relative volume of the cerebellum in dolphins and comparison with anthropoid primates. Brain Behav Evol 56:204-211.
76. Marino L, Sherwood CC, Delman BN, Tang CY, Naidich TP, Hof PR. 2004a. Neuroanatomy of the killer whale (Orcinus orca) from magnetic resonance images. Anat Rec 281:1256-1263.
77. Marino L, Sudheimer K, McLellan WA, Johnson JI. 2004b. Neuroanatomical structure of the spinner dolphin (Stenella longirostris orientalis) brain from magnetic resonance images. Anat Rec 279:601-610.
78. Marino L, Sudheimer K, Pabst DA, McLellan WA, Johnson JI. 2003a. Magnetic resonance images of the brain of a dwarf sperm whale (Kogia simus). J Anat 203:57-76.
79. Marino L, Sudheimer K, Sarko D, Sirpenski G, Johnson JI. 2003b. Neuroanatomy of the harbor porpoise (Phocoena phocoena) from magnetic resonance images. J Morphol 257:308-347.
80. Marino L, Sudheimer KD, Murphy TL, Davis KK, Pabst DA, McLellan WA, Rilling JK, Johnson JI. 2001c. Anatomy and three-dimensional reconstructions of the brain of a bottlenose dolphin (Tursiops truncatus) from magnetic resonance images. Anat Rec 264:397-414.
81. Marino L, Sudheimer KD, Pabst DA, McLellan WA, Filsoof D, Johnson JI. 2002. Neuroanatomy of the common dolphin (Delphinus delphis) as revealed by magnetic resonance imaging (MRI). Anat Rec 268:411-429.
82. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G, Wu C. 2004. Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5:793-807.
83. Martinez-Guijarro FJ, Freund TF. 1992. Distribution of GABAergic interneurons immunoreactive for calretinin, calbindin D28K, and parvalbumin in the cerebral cortex of the lizard Podarcis hispanica. J Comp Neurol 322:449-460.
84. Maseko BC, Spocter MA, Haagensen M, Manger PR. 2012. Elephants have relatively the largest cerebellum size for mammals. Anat Rec 295: 661-672.
85. Milinkovitch M, Bérubé, M, Palsboll, PJ. 1998. Cetaceans are highly derived artiodactyls. In: JGM Thewissen, editor. The emergence of whales. New York: Plenum Press. p 113-131.
86. Montie EW, Schneider GE, Ketten DR, Marino L, Touhey KE, Hahn ME. 2007. Neuroanatomy of the subadult and fetal brain of the Atlantic white-sided dolphin (Lagenorhynchus acutus) from in situ magnetic resonance images. Anat Rec 290:1459-1479.
87. Montie EW, Schneider G, Ketten DR, Marino L, Touhey KE, Hahn ME. 2008. Volumetric neuroimaging of the atlantic white-sided dolphin (Lagenorhynchus acutus) brain from in situ magnetic resonance images. Anat Rec 291:263-282.
88. Morgane P, Jacobs M, McFarland W. 1980. The anatomy of the brain of the bottlenose dolphin (Tursiops truncatus). Surface configuration of the telencephalon of the bottlenose dolphin with comparative anatomical observations in four other cetaceans species. Brain Res Bull 5:1-107.
89. Morgane PJ, Glezer, II, Jacobs MS. 1988. Visual cortex of the dolphin: an image analysis study. J Comp Neurol 273:3-25.
90. Morgane PJ, Jacobs MS, Galaburda A. 1985. Conservative features of neocortical evolution in dolphin brain. Brain Behav Evol 26:176-184.
91. Morgane PJ, McFarland WL, Jacobs MS. 1982. The limbic lobe of the dolphin brain: a quantitative cytoarchitectonic study. J Hirnforsch 23:465-552.
92. Ngowyang G. 1932. Beschreibung einer Art von Spezialzellen in der Inselrinde - zugleich Bemerkungen über die v. Economoschen Spezialzellen. J Psychol Neurol 44:671-674.
93. Nikaido M, Rooney AP, Okada N. 1999. Phylogenetic relationships among cetartiodactyls based on insertions of short and long interpersed elements: hippopotamuses are the closest extant relatives of whales. Proc Natl Acad Sci USA 96:10261-10266.
94. Nimchinsky EA, Gilissen E, Allman JM, Perl DP, Erwin JM, Hof PR. 1999. A neuronal morphologic type unique to humans and great apes. Proc Natl Acad Sci USA 96:5268-5273.
95. Nimchinsky EA, Vogt BA, Morrison JH, Hof PR. 1995. Spindle neurons of the human anterior cingulate cortex. J Comp Neurol 355:27-37.
96. O'Leary MA, Patel BA, Coleman MN. 2012. Endocranial petrosal anatomy of Bothriogenys (Mammalia, Artiodactyla, Anthracotheriidae), and petrosal volume and density comparisons among aquatic and terrestrial artiodactyls and outgroups. J Paleontol 86:44-50.
97. Oelschläger HA, Oelschläger J. 2008. Brain. In: Perrin WF, Würsig B, Thewissen JGM, editors. Encyclopedia of marine mammals. San Diego, CA: Academic Press. p 134-149.
98. Oelschläger HHA, Oelschläger JS. 2002. Brain. In: Perrin WF, Würsig B, Thewissen JGM, editors. Encyclopedia of marine mammals. San Diego: Academic Press. p133-158.
99. Parmentier M, Lefort A. 1991. Structure of the human brain calcium-binding protein calretinin and its expression in bacteria. Eur J Biochem 196:79-85.
100. Payne BR. 1993. Evidence for visual cortical area homologs in cat and macaque monkey. Cereb Cortex 3:1-25.
101. Pilleri G. 1962. Zur Anatomie des Gehirnes von Choeropsis liberiensis Morton (Mammalia, Artiodactyla). Acta Zool 43:229-245.
102. Pilleri G, Peixun, C, Zuohua, S. 1980. Concise macroscopical atlas of the brain of the common dolphin (Delphinus delphis Linnaeus, 1758). Bern-Waldau, Switzerland: Brain Anatomy Institute.
103. Popov VV, Supin A. 1976. Detemination of the hearing characteristics of the dolphin by the evoked potential method. Fiziol Zh SSSR Im I M Sechenova 62:550-558.
104. Popov VV, Supin A. 1986. Evoked potentials of the dolphin auditory cortex recorded from the body surface. Dokl Akad Nauk SSSR 288:756-759.
105. Pravosudov VV, Kitaysky AS, Omanska A. 2006. The relationship between migratory behaviour, memory and the hippocampus: an intraspecific comparison. Proc Biol Sci 273:2641-2649.
106. Puelles L and Rubenstein JL. 2003. Forebrain gene expression domains and the evolving prosomeric model. Trends Neurosci 26:469-476.
107. Raghanti MA, Spurlock LB, Uppal N, Sherwood CC, Butti C, Hof PR. In press. Von Economo neurons. In: Toga AW, Zilles K, Amunts K, edItors. Brain mapping: an encyclopedic reference. Elsevier, Amsterdam.
108. Ramón y Cajal S. 1911. Histologie du systeme nerveux de l'homme et des vertébrés. Paris: Maloine.
109. Reep RL, Finlay BL, Darlington RB. 2007. The limbic system in mammalian brain evolution. Brain Behav Evol 70:57-70.
110. Résibois A, Rogers JH. 1992. Calretinin in rat brain: an immunohistochemical study. Neuroscience 46:101-134.
111. Revishchin AV, Garey LJ. 1989. Sources of thalamic afferent neurons, projecting into the suprasylvian gyrus of the dolphin cerebral cortex. Neirofiziol 21:529-539.
112. Rogers JH. 1989. Two calcium-binding proteins mark many chick sensory neurons. Neuroscience 31:697-709.
113. Rogers JH. 1992. Immunohistochemical markers in rat cortex: co-localization of calretinin and calbindin-D28k with neuropeptides and GABA. Brain Res 587:147-157.
114. Rose J. 1942. A cytoarchitectural study of the sheep cortex. J Comp Neurol 76:1-55.
115. Sanides F, Hoffmann J. 1969. Cyto- and myeloarchitecture of the visual cortex of the cat and of the surrounding integration cortices. J Hirnforsch 11:79-104.
116. Sanides F, Sanides D. 1972. The "extraverted neurons" of the mammalian cerebral cortex. Z Anat Entwickl Gesch 136:272-293.
117. Scheibel ME, Scheibel AB. 1978. The methods of Golgi. In: RT Robertson, editor. Neuroanatomical research techniques. New York: Academic Press. p 89-114.
118. Schwaller B, Buchwald P, Blumcke I, Celio MR, Hunziker W. 1993. Characterization of a polyclonal antiserum against the purified human recombinant calcium binding protein calretinin. Cell Calcium 14:639-648.
119. Schwerdtfeger WK, Oelschläger HA, Stephan H. 1984. Quantitative neuroanatomy of the brain of the La Plata dolphin, Pontoporia blainvillei. Anat Embryol 170:11-19.
120. Seeley WW, Merkle FT, Gaus SE, Craig AD, Allman JM, Hof PR. 2012. Distinctive neurons of the anterior cingulate and frontoinsular cortex: a historical perspective. Cereb Cortex 22:245-250.
121. Sherk H. 1986. Location and connections of visual cortical areas in the cat's suprasylvian sulcus. J Comp Neurol 247:1-31.
122. Sherwood CC, Stimpson CD, Butti C, Bonar CJ, Newton AL, Allman JM, Hof PR. 2009. Neocortical neuron types in Xenarthra and Afrotheria: implications for brain evolution in mammals. Brain Struct Funct 213:301-328.
123. Shimamura M, Yasue H, Ohshima K, Abe H, Kato H, Kishiro T, Goto M, Munechika I, Okada N. 1997. Molecular evidence from retroposons that whales form a clade within even-toed ungulates. Nature 388:666-670.
124. Sokolov VE, Ladygina TF, Supin A. 1972. Localization of sensory zones in the dolphin cerebral cortex. Dokl Akad Nauk SSSR 202:490-493.
125. Spaulding M, O'Leary MA, Gatesy J. 2009. Relationships of Cetacea (Artiodactyla) among mammals: increased taxon sampling alters interpretations of key fossils and character evolution. PLoS One 4:e7062.
126. Squire LR, Zola-Morgan S. 1991. The medial temporal lobe memory system. Science 253:1380-1386.
127. Stern S. 2009. Migrations and movement patterns. In: Perrin WF, Würsig B, Thewissen JGM, editors. Encyclopedia of marine mammals: Academic Press. p 726-730.
128. Striedter GF. 2005. Principles of Brain Evolution. Sunderland, MA: Sinauer Associates.
129. Tarpley RJ, Ridgway SH. 1994. Corpus callosum size in delphinid cetaceans. Brain Behav Evol 44:156-165.
130. Thewissen JGM, Cooper LN, Clementz MT, Bajpai S, Tiwari BN. 2007. Whales originated from aquatic artiodactyls in the Eocene epoch of India. Nature 450:1190-1194.
131. Uhen M. 2010. The origin(s) of whales. Annu Rev Earth Planet Sci 38:189-219.
132. von Economo C. 1926. Eine neue Art Spezialzellen des Lobus cinguli and Lobus insulae. Zschr Ges Neurol Psychiatr 100:706-712.
133. Zhou X, Xu S, Yang Y, Zhou K, Yang G. 2011. Phylogenomic analyses and improved resolution of Cetartiodactyla. Mol Phyl Evol 61:255-264.
134. Zilles K, Armstrong E, Moser KH, Schleicher A, Stephan H.1989. Gyrification in the cerebral cortex of primates. Brain Behav Evol 34:143-150.
135. Zimmermann L, Schwaller B. 2002. Monoclonal antibodies recognizing epitopes of calretinins: dependence on Ca2+-binding status and differences in antigen accessibility in colon cancer cells. Cell Calcium 31:13-25.
136. Zola-Morgan S, Squire, LR. 1993. Neuroanatomy of memory. Annu Rev Neurosci 16:547-563.