The neocortex of cetartiodactyls: I. A comparative Golgi analysis of neuronal morphology in the bottlenose dolphin (Tursiops truncatus), the minke whale (Balaenoptera acutorostrata), and the humpback whale (Megaptera novaeangliae)

Brain Structure and Function

Volumn 220, Issue 6, 2015, Pages 3339-3368

  Butti, Camilla ^a   Janeway, Caroline M ^b   Townshend, Courtney ^b   Wicinski, Bridget A ^a   Reidenberg, Joy S ^a   Ridgway, Sam H ^c   Sherwood, Chet C ^d   Hof, Patrick R ^a   Jacobs, Bob ^b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b Department of Psychology   (United States)

^c NATIONAL MARINE MAMMAL FOUNDATION   (United States)

^d GEORGE WASHINGTON UNIVERSITY   (United States)

Author keywords

Brain evolution; Cetacean neocortex; Golgi method; Neuronal morphology

Indexed keywords

ANIMAL TISSUE; ARTICLE; BALAENOPTERA; BALAENOPTERA ACUTOROSTRATA; CONTROLLED STUDY; FEMALE; FRONTAL CORTEX; GOLGI STAIN; HUMPBACK WHALE; MALE; MEGAPTERA NOVAEANGLIAE; MORPHOLOGY; MOTOR CORTEX; NEOCORTEX; NERVE CELL; NEURONAL MORPHOLOGY; NONHUMAN; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SUPRASYLVIAN GYRUS; TEMPORAL CORTEX; TURSIOPS TRUNCATUS; VISUAL CORTEX; ANATOMY AND HISTOLOGY; ANIMAL; BOTTLENOSE DOLPHIN; COMPARATIVE STUDY; CYTOLOGY; DENDRITE; GOLGI COMPLEX; MINKE WHALE; PHYSIOLOGY; ULTRASTRUCTURE;

ANIMALS; BOTTLE-NOSED DOLPHIN; DENDRITES; GOLGI APPARATUS; HUMPBACK WHALE; MALE; MINKE WHALE; NEOCORTEX; NEURONS; PYRAMIDAL CELLS;

EID: 84942367921     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-014-0860-3     Document Type: Article

References (165)

1. Anderson K, Bones B, Robinson B, Hass C, Lee H, Ford K, Roberts TA, Jacobs B (2009) The morphology of supragranular pyramidal neurons in the human insular cortex: a quantitative Golgi study. Cereb Cortex 19:2131–2144
2. Ascoli GA, Alonso-Nanclares L, Anderson SA, Barrionuevo G, Benavides-Piccione R, Burkhalter A, Buzsaki G, Cauli B, Defelipe J, Fairen A, Feldmeyer D, Fishell G, Fregnac Y, Freund TF, Gardner D, Gardner EP, Goldberg JH, Helmstaedter M, Hestrin S, Karube F, Kisvarday ZF, Lambolez B, Lewis DA, Marin O, Markram H, Munoz A, Packer A, Petersen CC, Rockland KS, Rossier J, Rudy B, Somogyi P, Staiger JF, Tamas G, Thomson AM, Toledo-Rodriguez M, Wang Y, West DC, Yuste R (2008) Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 9:557–568
3. Au WW, Nachtigall PE (1997) Acoustics of echolocating dolphins and small whales. Mar Freshw Behav Physiol 29:127–162
4. Au WW, Branstetter BK, Benoit-Bird KJ, Kastelein RA (2009) Acoustic basis for fish prey discrimination by echolocating dolphins and porpoises. J Acoust Soc Am 126:460
5. Barasa A (1960) Form, size and density of the neurons in the cerebral cortex of mammals of different body sizes. Z Zellforsch Mikrosk Anat 53:69–89
6. Betz W (1881) Ueber die feinere Structur der Gehirnrinde des Menschen. Zentralbl Med Wiss 19:193–195
7. Bianchi S, Bauernfeind AL, Gupta K, Stimpson CD, Spocter MA, Bonar CJ, Manger PR, Hof PR, Jacobs B, Sherwood CC (2011) Neocortical neuron morphology in Afrotheria: comparing the rock hyrax with the African elephant. Ann N Y Acad Sci 1225:37–46
8. Bok S (1959) Histonomy of the cerebral cortex. Histonomy of the cerebral cortex, Amsterdam
9. Boothe RG, Greenough WT, Lund JS, Wrege K (1979) A quantitative investigation of spine and dendrite development of neurons in visual cortex (area17) of Macaca nemestrina monkeys. J Comp Neurol 186:473–489
10. Bota M, Swanson LW (2007) The neuron classification problem. Brain Res Rev 56:79–88
11. Braak H, Braak E (1976) The pyramidal cells of Betz within the cingulate and precentral gigantopyramidal field in the human brain: a Golgi and pigmentarchitectonic study. Cell Tissue Res 172:103–119
12. Buell S (1982) Golgi–Cox and rapid Golgi methods as applied to autopsied human brain tissue: widely disparate results. J Neuropathol Exp Neurol 41:500–507
13. Butler AB (2008) Evolution of brains, cognition, and consciousness. Brain Res Bull 75:442–449
14. Butti C, Hof PR (2010) The insular cortex: a comparative perspective. Brain Struct Funct 214:477–493
15. 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
16. Butti C, Raghanti MA, Sherwood CC, Hof PR (2011) The neocortex of cetaceans: cytoarchitecture and comparison with other aquatic and terrestrial species. Ann N Y Acad Sci 1225:47–58
17. Butti C, Ewan Fordyce R, Ann Raghanti M, Gu X, Bonar CJ, Wicinski BA, Wong EW, Roman J, Brake A, Eaves E, Spocter MA, Tang CY, Jacobs B, Sherwood CC, Hof PR (2014) The cerebral cortex of the pygmy hippopotamus, Hexaprotodon liberiensis (Cetartiodactyla, Hippopotamidae): MRI, cytoarchitecture, and neuronal morphology. Anat Rec 297:670–700
18. Chan-Palay V, Palay SL, Billings-Gagliardi SM (1974) Meynert cells in the primate visual cortex. J Neurocytol 3:631–658
19. Chklovskii DB (2004) Synaptic connectivity and neuronal morphology: two sides of the same coin. Neuron 43:609–617
20. Connor RC (2007) Dolphin social intelligence: complex alliance relationships in bottlenose dolphins and a consideration of selective environments for extreme brain size evolution in mammals. Philos Trans R Soc Lond B Biol Sci 362:587–602
21. Cupp CJ, Uemura E (1980) Age-related changes in the prefrontal cortex of Macaca mulatta: quantitative analysis of dendritic branching patterns. Exp Neurol 69:143–163
22. de Lima AD, Voigt T, Morrison JH (1990) Morphology of the cells within the inferior temporal gyrus that project to the prefrontal cortex in the macaque monkey. J Comp Neurol 296:159–172
23. de Ruiter JP (1983) The influence of post-mortem fixation delay on the reliability of the Golgi silver impregnation. Brain Res 266:143–147
24. Deacon TW (1990) Rethinking mammalian brain evolution. Am Zool 30:629–705
25. 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
26. DeFelipe J, Lopez-Cruz PL, Benavides-Piccione R, Bielza C, Larranaga P, Anderson S, Burkhalter A, Cauli B, Fairen A, Feldmeyer D, Fishell G, Fitzpatrick D, Freund TF, Gonzalez-Burgos G, Hestrin S, Hill S, Hof PR, Huang J, Jones EG, Kawaguchi Y, Kisvarday Z, Kubota Y, Lewis DA, Marin O, Markram H, McBain CJ, Meyer HS, Monyer H, Nelson SB, Rockland K, Rossier J, Rubenstein JL, Rudy B, Scanziani M, Shepherd GM, Sherwood CC, Staiger JF, Tamas G, Thomson A, Wang Y, Yuste R, Ascoli GA (2013) New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat Rev Neurosci 14:202–216
27. Druga R (2009) Neocortical inhibitory system. Folia Biol 55:201–217
28. Elias H, Schwartz D (1969) Surface areas of the cerebral cortex of mammals determined by stereological methods. Science 166:111–113
29. Elston GN, Rosa MG (1998a) Complex dendritic fields of pyramidal cells in the frontal eye field of the macaque monkey: comparison with parietal areas 7a and LIP. NeuroReport 9:127–131
30. Elston GN, Rosa MG (1998b) Morphological variation of layer III pyramidal neurones in the occipitotemporal pathway of the macaque monkey visual cortex. Cereb Cortex 8:278–294
31. Elston GN, Oga T, Fujita I (2009) Spinogenesis and pruning scales across functional hierarchies. J Neurosci 29:3271–3275
32. Elston GN, Oga T, Okamoto T, Fujita I (2010a) Spinogenesis and pruning from early visual onset to adulthood: an intracellular injection study of layer III pyramidal cells in the ventral visual cortical pathway of the macaque monkey. Cereb Cortex 20:1398–1408
33. Elston GN, Okamoto T, Oga T, Dornan D, Fujita I (2010b) Spinogenesis and pruning in the primary auditory cortex of the macaque monkey (Macaca fascicularis): an intracellular injection study of layer III pyramidal cells. Brain Res 1316:35–42
34. Elston GN, Oga T, Okamoto T, Fujita I (2011) Spinogenesis and pruning in the anterior ventral inferiotemporal cortex of the macaque monkey: an intracellular injection study of layer III pyramidal cells. Front Neuroanat 5:42
35. Eriksen N, Pakkenberg B (2007) Total neocortical cell number in the mysticete brain. Anat Rec 290:83–95
36. Ferrer I (1987) The basic structure of the neocortex in insectivorous bats (Miniopterus sthreibersi and Pipistrellus pipistrellus). A Golgi study. J Hirnforsch 28:237–243
37. 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
38. Ferrer I, Fábregues I, Condom E (1986a) A Golgi study of the sixth layer of the cerebral cortex. I. The lissencephalic brain of Rodentia, Lagomorpha, Insectivora and Chiroptera. J Anat 145:217–234
39. Ferrer I, Fábregues I, Condom E (1986b) A Golgi study of the sixth layer of the cerebral cortex. II. The gyrencephalic brain of Carnivora, Artiodactyla and Primates. J Anat 146:87–104
40. 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
41. Gabi M, Collins CE, Wong P, Torres LB, Kaas JH, Herculano-Houzel S (2010) Cellular scaling rules for the brains of an extended number of primate species. Brain Behav Evol 76:32–44
42. Garey LJ, Winkelmann E, Brauer K (1985) Golgi and Nissl studies of the visual cortex of the bottlenose dolphin. J Comp Neurol 240:305–321
43. 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
44. Garland EC, Noad MJ, Goldizen AW, Lilley MS, Rekdahl ML, Garrigue C, Constantine R, Daeschler Hauser N, Poole MM, Robbins J (2013) Quantifying humpback whale song sequences to understand the dynamics of song exchange at the ocean basin scale. J Acoust Soc Am 133:560–569
45. Gatesy J (1997) More DNA support for a Cetacea/Hippopotamidae clade: the blood-clotting protein gene gamma-fibrinogen. Mol Biol Evol 14:537–543
46. Geisler G, Uhen MD (2003) Morphological support for a close relationship between hippos and whales. J Vert Paleontol 23:991–996
47. Germroth P, Schwerdtfeger WK, Buhl EH (1989) Morphology of identified entorhinal neurons projecting to the hippocampus. A light microscopical study combining retrograde tracing and intracellular injection. Neuroscience 30:683–691
48. Gingerich PD, Uhen MD (1998) Likelihood estimation of the time of origin of cetacean and the time of divergence of Cetacea and Artiodactyla. Paleo-Electronica 2:1–47
49. Gingerich PD, Haq M, Zalmout IS, Khan IH, Malkani MS (2001) Origin of whales from early artiodactyls: hands and feet of Eocene Protocetidae from Pakistan. Science 293:2239–2242
50. Glezer I (2002) Neural morphology. In: Hoezel AR (ed) Marine mammal biology: an evolutionary approach. Blackwell Science Ltd, Malden, pp 98–115
51. 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
52. Glezer II, Jacobs MS, Morgane PJ (1988) Implications of the “initial brain” concept for brain evolution in Cetacea. Behav Brain Sci 11:75–116
53. 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
54. 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
55. Glezer I, Hof PR, Morgane PJ (1995) Cytoarchitectonics and immunocytochemistry of the inferior colliculus of midbrain in cetaceans. FASEB J 9:A247
56. 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
57. Hanson A, Grisham W, Sheh C, Annese J, Ridgway S (2013) Quantitative examination of the bottlenose dolphin cerebellum. Anat Rec 296:1215–1228
58. Harrison KH, Hof PR, Wang SS (2002) Scaling laws in the mammalian neocortex: does form provide clues to function? J Neurocytol 31:289–298
59. Hart BL, Hart LA, Pinter-Wollman N (2008) Large brains and cognition: where do elephants fit in? Neurosci Biobehav Rev 32:86–98
60. Hassiotis M, Ashwell KW (2003) Neuronal classes in the isocortex of a monotreme, the Australian echidna (Tachyglossus aculeatus). Brain Behav Evol 61:6–27
61. Herculano-Houzel S (2007) Encephalization, neuronal excess, and neuronal index in rodents. Anat Rec 290:1280–1287
62. Herculano-Houzel S, Mota B, Lent R (2006) Cellular scaling rules for rodent brains. Proc Natl Acad Sci USA 103:12138–12143
63. Herculano-Houzel S, Collins CE, Wong P, Kaas JH (2007) Cellular scaling rules for primate brains. Proc Natl Acad Sci USA 104:3562–3567
64. Herman LM, Tavolga WN (1980) The communication systems of cetaceans. In: Herman LM (ed) Cetacean behavior: mechanisms and functions. Wiley, New York, pp 149–209
65. Herman LM, Peacock MF, Yunker MP, Madsen CJ (1975) Bottle-nosed dolphin: double-slit pupil yields equivalent aerial and underwater diurnal acuity. Science 189:650–652
66. Hof PR, Sherwood CC (2005) Morphomolecular neuronal phenotypes in the neocortex reflect phylogenetic relationships among certain mammalian orders. Anat Rec 287:1153–1163
67. 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
68. Hof PR, Glezer II, Archin N, Janssen WG, Morgane PJ, Morrison JH (1992) The primary auditory cortex in cetacean and human brain: a comparative analysis of neurofilament protein-containing pyramidal neurons. Neurosci Lett 146:91–95
69. Hof PR, Glezer II, Revishchin AV, Bouras C, Charnay Y, Morgane PJ (1995) Distribution of dopaminergic fibers and neurons in visual and auditory cortices of the harbor porpoise and pilot whale. Brain Res Bull 36:275–284
70. 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
71. Hof PR, Glezer II, Nimchinsky EA, Erwin JM (2000a) Neurochemical and cellular specializations in the mammalian neocortex reflect phylogenetic relationships: evidence from primates, cetaceans, and artiodactyls. Brain Behav Evol 55:300–310
72. Hof PR, Nimchinsky EA, Young WG, Morrison JH (2000b) Numbers of Meynert and layer IVB cells in area V1: a stereologic analysis in young and aged macaque monkeys. J Comp Neurol 420:113–126
73. Hof PR, Chanis R, Marino L (2005) Cortical complexity in cetacean brains. Anat Rec 287:1142–1152
74. Huggenberger S (2008) The size and complexity of dolphin brains—A paradox? J Mar Biol Assoc UK 88:1103–1108
75. Jacobs B, Scheibel AB (1993) A quantitative dendritic analysis of Wernicke’s area in humans. I. Lifespan changes. J Comp Neurol 327:83–96
76. Jacobs B, Scheibel AB (2002) Regional dendritic variation in primate cortical pyramidal cells. In: Schuz A, Miller R (eds) Cortical areas: unity and diversity (Conceptual advances in brain research series). Taylor & Francis, London, pp 111–131
77. 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
78. 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 1:1–108
79. 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
80. Jacobs B, Driscoll L, Schall M (1997) Lifspan dendritic and spine changes in areas 10 and 18 of human cortex: a quantitative Golgi study. J Comp Neurol 386:661–680
81. Jacobs B, Schall M, Prather M, Kapler E, Driscoll L, Baca S, Jacobs J, Ford K, Wainwright M, Treml M (2001) Regional dendritic and spine variation in human cerebral cortex: a quantitative Golgi study. Cereb Cortex 11:558–571
82. 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
83. Jacobs B, Harland T, Kennedy D, Schall M, Wicinski B, Butti C, Hof PR, Sherwood CC, Manger PR (2014a) The neocortex of cetartiodactyls. II. Neuronal morphology of the visual and motor cortices in the giraffe (Giraffa camelopardalis). Brain Struct Funct. doi:10.1007/s00429-014-0830-9
84. Jacobs B, Johnson NL, Wahl D, Schall M, Maseko BC, Lewandowski A, Raghanti MA, Wicinski B, Butti C, Hopkins WD, Bertelsen MF, Walsh T, Roberts JR, Reep RL, Hof PR, Sherwood CC, Manger PR (2014b) Comparative neuronal morphology of the cerebellar cortex in afrotherians, carnivores, cetartiodactyls, and primates. Front Neuroanat 8:24
85. Kawaguchi Y (1995) Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J Neurosci 15:2638–2655
86. Kern A, Siebert U, Cozzi B, Hof PR, Oelschläger HH (2011) Stereology of the neocortex in odontocetes: qualitative, quantitative, and functional implications. Brain Behav Evol 77:79–90
87. Kesarev VS (1971) The inferior brain of the dolphin. Soviet Sci Rev 2:52–58
88. Kesarev VS (1975) Homologization of the cerebral neocortex in cetaceans. Arkhiv Anat Gistol Embriol 68:5–13
89. Kesarev VS, Malofeeva LI (1969) Structural organization of the motor zone of the cerebral cortex in dolphins. Arkh Anat Gistol Embriol 56:48–55
90. Kesarev VS, Malofeeva LI, Trykova OV (1977) Structural organization of the cetacean neocortex. Arkh Anat Gistol Embriol 73:23–30
91. Kisvarday ZF, Gulyas A, Beroukas D, North JB, Chubb IW, Somogyi P (1990) Synapses, axonal and dendritic patterns of GABA-immunoreactive neurons in human cerebral cortex. Brain 113:793–812
92. Kraus C, Pilleri G (1969a) Quantitative Untersuchungen über die Grosshirnrinde der Cetaceen. Investig Cetacea 1:127–150
93. Kraus C, Pilleri G (1969b) Zur Feinstrucktur der großen Pyramidenzellen in der V Cortexschicht der Cetacean Delphinus delphis und Balaenoptera borealis. Investig Cetacea 1:89–99
94. Kraus C, Pilleri G (1969c) Zur Histologie der Grosshirnrinde von Balaenoptera borealis Lesson (Cetacea, Mysticeti). Investig Cetacea 1:151–170
95. 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
96. Ladygina TF, Mass AM, Supin A (1978) Multiple sensory projections in the dolphin cerebral cortex. Zh Vyssh Nerv Deiat Pavl 28:1047–1053
97. Le Gros Clark WE (1942) The cells of Meynert in the visual cortex of the monkey. J Anat 76:369–376
98. Lopez-Mascaraque L, De Carlos JA, Valverde F (1986) Structure of the olfactory bulb of the hedgehog (Erinaceus europaeus): description of cell types in the granular layer. J Comp Neurol 253:135–152
99. Lund JS, Lewis DA (1993) Local circuit neurons of developing and mature macaque prefrontal cortex: Golgi and immunocytochemical characteristics. J Comp Neurol 328:282–312
100. Manger PR (2006) An examination of cetacean brain structure with a novel hypothesis correlating thermogenesis to the evolution of a big brain. Biol Rev Camb Philos Soc 81:293–338
101. Manger PR (2013) Questioning the interpretations of behavioral observations of cetaceans: is there really support for a special intellectual status for this mammalian order? Neuroscience 250:664–696
102. Manger P, 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
103. Manger PR, Fuxe K, Ridgway SH, Siegel JM (2004) The distribution and morphological characteristics of catecholaminergic cells in the diencephalon and midbrain of the bottlenose dolphin (Tursiops truncatus). Brain Behav Evol 64:42–60
104. Manger PR, Cort J, Ebrahim N, Goodman A, Henning J, Karolia M, Rodrigues SL, Strkalj G (2008) Is 21st century neuroscience too focussed on the rat/mouse model of brain function and dysfunction? Front Neuroanat 2:5
105. 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
106. Marino L (2002) Convergence of complex cognitive abilities in cetaceans and primates. Brain Behav Evol 59:21–32
107. 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
108. 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
109. 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
110. 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
111. 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
112. 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
113. 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
114. 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
115. Marino L, Connor RC, Fordyce RE, Herman LM, Hof PR, Lefebvre L, Lusseau D, McCowan B, Nimchinsky EA, Pack AA, Rendell L, Reidenberg JS, Reiss D, Uhen MD, Van der Gucht E, Whitehead H (2007) Cetaceans have complex brains for complex cognition. PLoS Biol 5:e139
116. Marino L, Butti C, Connor RC, Fordyce RE, Herman LM, Hof PR, Lefebvre L, Lusseau D, McCowan B, Nimchinsky EA, Pack AA, Reidenberg JS, Reiss D, Rendell L, Uhen MD, Van der Gucht E, Whitehead H (2008) A claim in search of evidence: reply to Manger’s thermogenesis hypothesis of cetacean brain structure. Biol Rev Camb Philos Soc 83:417–440
117. Masland RH (2004) Neuronal cell types. Curr Biol 14:R497–R500
118. Mendizabal-Zubiaga JL, Reblet C, Bueno-Lopez JL (2007) The underside of the cerebral cortex: layer V/VI spiny inverted neurons. J Anat 211:223–236
119. Meyer G (1987) Forms and spatial arrangement of neurons in the primary motor cortex of man. J Comp Neurol 262:402–428
120. Meynert T (1867) Der Bau der Grosshirnrinde und seine örtlichen Verschiedenheiten nebst einem pathologisch anatomischen Corollarium. Vierteljahrsch Psychiatr 198–217
121. Milinkovitch M, Bérubé M, Palsboll PJ (1998) Cetaceans are highly derived artiodactyls. In: Thewissen JGM (ed) The emergence of whales. Plenum Press, New York, pp 113–131
122. Miller MW (1988) Maturation of rat visual cortex: IV. The generation, migration, morphogenesis, and connectivity of atypically oriented pyramidal neurons. J Comp Neurol 274:387–405
123. 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
124. 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
125. 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
126. Morgane PJ, McFarland WL, Jacobs MS (1982) The limbic lobe of the dolphin brain: a quantitative cytoarchitectonic study. J Hirnforsch 23:465–552
127. Morgane PJ, Jacobs MS, Galaburda A (1985) Conservative features of neocortical evolution in dolphin brain. Brain Behav Evol 26:176–184
128. Morgane PJ, Glezer II, Jacobs MS (1988) Visual cortex of the dolphin: an image analysis study. J Comp Neurol 273:3–25
129. Morgane P, Glezer I, Jacobs M (1990) Comparative and evolutionary anatomy of the visual cortex of the dolphin. In: Jones EG, Peters A (eds) Cerebral cortex. Comparative structure and evolution of cerebral cortex, part II, vol 8B. Plenum Press, New York, pp 215–262
130. Neves K, Ferreira FM, Tovar-Moll F, Gravett N, Bennett NC, Kaswera C, Gilissen E, Manger PR, Herculano-Houzel S (2014) Cellular scaling rules for the brain of afrotherians. Front Neuroanat 8:5
131. 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
132. Nikaido M, Matsuno F, Hamilton H, Brownell RL Jr, Cao Y, Ding W, Zuoyan Z, Shedlock AM, Fordyce RE, Hasegawa M, Okada N (2001) Retroposon analysis of major cetacean lineages: the monophyly of toothed whales and the paraphyly of river dolphins. Proc Natl Acad Sci USA 98:7384–7389
133. Oelschläger HA, Oelschläger JS (2008) Brain. In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals. Academic Press, San Diego, pp 134–149
134. Oelschläger HH, Haas-Rioth M, Fung C, Ridgway SH, Knauth M (2008) Morphology and evolutionary biology of the dolphin (Delphinus sp.) brain—MR imaging and conventional histology. Brain Behav Evol 71:68–86
135. Oelschläger HH, Ridgway SH, Knauth M (2010) Cetacean brain evolution: dwarf sperm whale (Kogia sima) and common dolphin (Delphinus delphis)—an investigation with high-resolution 3D MRI. Brain Behav Evol 75:33–62
136. Parnavelas JG, Lieberman AR, Webster KE (1977a) Organization of neurons in the visual cortex, area 17, of the rat. J Anat 124:305–322
137. Parnavelas JG, Sullivan K, Lieberman AR, Webster KE (1977b) Neurons and their synaptic organization in the visual cortex of the rat. Electron microscopy of Golgi preparations. Cell Tissue Res 183:499–517
138. Patzke N, Spocter MA, Karlsson KA, Bertelsen MF, Haagensen M, Chawana R, Streicher S, Kaswera C, Gilissen E, Alagaili AN, Mohammed OB, Reep RL, Bennett NC, Siegel JM, Ihunwo AO, Manger PR (2013) In contrast to many other mammals, cetaceans have relatively small hippocampi that appear to lack adult neurogenesis. Brain Struct Funct. doi:10.1007/s00429-013-0660-1
139. Peters A, Jones EG (1984) Classification of cortical neurons. In: Peters A, Jones EG (eds) Cerebral cortex: cellular components of the cerebral cortex, vol 1. Plenum Press, New York, pp 107–121
140. Peters A, Regidor J (1981) A reassessment of the forms of nonpyramidal neurons in area 17 of cat visual cortex. J Comp Neurol 203:685–716
141. Qi HX, Jain N, Preuss TM, Kaas JH (1999) Inverted pyramidal neurons in chimpanzee sensorimotor cortex are revealed by immunostaining with monoclonal antibody SMI-32. Somatosens Mot Res 16:49–56
142. Revishchin AV, Garey LJ (1989) Sources of thalamic afferent neurons, projecting into the suprasylvian gyrus of the dolphin cerebral cortex. Neirofiziol 21:529–539
143. Ridgway S, Brownson RH (1984) Relative brain sizes and cortical surface areas in odontocetes. Acta Zool Fenn 172:149–152
144. Sanides F, Sanides D (1972) The “extraverted neurons” of the mammalian cerebral cortex. Z Anat Entwickl-gesch 136:272–293
145. Sarko DK, Catania KC, Leitch DB, Kaas JH, Herculano-Houzel S (2009) Cellular scaling rules of insectivore brains. Front Neuroanat 3:8
146. Sasaki S, Iwata M (2001) Ultrastructural study of Betz cells in the primary motor cortex of the human brain. J Anat 199:699–708
147. Scheibel ME, Scheibel AB (1978) The methods of Golgi. In: Neuroanatomical research techniques. Academic Press, New York, pp 89–114
148. Schwartz SP, Coleman PD (1981) Neurons of origin of the perforant path. Exp Neurol 74:305–312
149. Sherwood CC, Lee PW, Rivara CB, Holloway RL, Gilissen EP, Simmons RM, Hakeem A, Allman JM, Erwin JM, Hof PR (2003) Evolution of specialized pyramidal neurons in primate visual and motor cortex. Brain Behav Evol 61:28–44
150. 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
151. 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
152. Shimamura M, Abe H, Nikaido M, Ohshima K, Okada N (1999) Genealogy of families of SINEs in cetaceans and artiodactyls: the presence of a huge superfamily of tRNA(Glu)-derived families of SINEs. Mol Biol Evol 16:1046–1060
153. Sholl DA (1953) Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 87:387–406
154. Sokolov VE, Ladygina TF, Supin A (1972) Localization of sensory zones in the dolphin cerebral cortex. Proc Acad Sci USSR 202:490–493
155. Somogyi P, Kisvarday ZF, Martin KA, Whitteridge D (1983) Synaptic connections of morphologically identified and physiologically characterized large basket cells in the striate cortex of cat. Neuroscience 10:261–294
156. Thewissen JG, Williams EM, Roe LJ, Hussain ST (2001) Skeletons of terrestrial cetaceans and the relationship of whales to artiodactyls. Nature 413:277–281
157. 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
158. Travis K, Ford K, Jacobs B (2005) Regional dendritic variation in neonatal human cortex: a quantitative Golgi study. Dev Neurosci 27:277–287
159. Uylings HB, Ruiz-Marcos A, van Pelt J (1986) The metric analysis of three-dimensional dendritic tree patterns: a methodological review. J Neurosci Methods 18:127–151
160. Walshe F (1942) The giant cells of Betz, the motor cortex and the pyramidal tract: a critical review. Brain 65:409–461
161. Wen Q, Chklovskii DB (2008) A cost–benefit analysis of neuronal morphology. J Neurophysiol 99:2320–2328
162. Williams RS, Ferrante RJ, Caviness VS Jr (1978) The Golgi rapid method in clinical neuropathology: the morphologic consequences of suboptimal fixation. J Neuropathol Exp Neurol 37:13–33
163. Winfield DA, Powell TP (1983) Laminar cell counts and geniculo-cortical boutons in area 17 of cat and monkey. Brain Res 277:223–229
164. Wittenberg GMWS (2008) Evolution and scaling of dendrites. In: Stuart G, Spruston N, Hausser M (eds) Dendrites. Oxford University Press, New York, pp 43–67
165. Zaitsev AV, Povysheva NV, Gonzalez-Burgos G, Rotaru D, Fish KN, Krimer LS, Lewis DA (2009) Interneuron diversity in layers 2–3 of monkey prefrontal cortex. Cereb Cortex 19:1597–1615