Brain Structure and Function

, Volume 220, Issue 6, pp 3339–3368 | Cite as

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)

  • Camilla Butti
  • Caroline M. Janeway
  • Courtney Townshend
  • Bridget A. Wicinski
  • Joy S. Reidenberg
  • Sam H. Ridgway
  • Chet C. Sherwood
  • Patrick R. Hof
  • Bob Jacobs
Original Article

Abstract

The present study documents the morphology of neurons in several regions of the neocortex from the bottlenose dolphin (Tursiops truncatus), the North Atlantic minke whale (Balaenoptera acutorostrata), and the humpback whale (Megaptera novaeangliae). Golgi-stained neurons (n = 210) were analyzed in the frontal and temporal neocortex as well as in the primary visual and primary motor areas. Qualitatively, all three species exhibited a diversity of neuronal morphologies, with spiny neurons including typical pyramidal types, similar to those observed in primates and rodents, as well as other spiny neuron types that had more variable morphology and/or orientation. Five neuron types, with a vertical apical dendrite, approximated the general pyramidal neuron morphology (i.e., typical pyramidal, extraverted, magnopyramidal, multiapical, and bitufted neurons), with a predominance of typical and extraverted pyramidal neurons. In what may represent a cetacean morphological apomorphy, both typical pyramidal and magnopyramidal neurons frequently exhibited a tri-tufted variant. In the humpback whale, there were also large, star-like neurons with no discernable apical dendrite. Aspiny bipolar and multipolar interneurons were morphologically consistent with those reported previously in other mammals. Quantitative analyses showed that neuronal size and dendritic extent increased in association with body size and brain mass (bottlenose dolphin < minke whale < humpback whale). The present data thus suggest that certain spiny neuron morphologies may be apomorphies in the neocortex of cetaceans as compared to other mammals and that neuronal dendritic extent covaries with brain and body size.

Keywords

Cetacean neocortex Neuronal morphology Golgi method Brain evolution 

References

  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 19:2131–2144PubMedCrossRefGoogle Scholar
  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 9:557–568PubMedCrossRefGoogle Scholar
  3. Au WW, Nachtigall PE (1997) Acoustics of echolocating dolphins and small whales. Mar Freshw Behav Physiol 29:127–162CrossRefGoogle Scholar
  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 126:460PubMedCrossRefGoogle Scholar
  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 53:69–89PubMedCrossRefGoogle Scholar
  6. Betz W (1881) Ueber die feinere Structur der Gehirnrinde des Menschen. Zentralbl Med Wiss 19:193–195Google Scholar
  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 1225:37–46PubMedCrossRefGoogle Scholar
  8. Bok S (1959) Histonomy of the cerebral cortex. Histonomy of the cerebral cortex, AmsterdamGoogle Scholar
  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 186:473–489PubMedCrossRefGoogle Scholar
  10. Bota M, Swanson LW (2007) The neuron classification problem. Brain Res Rev 56:79–88PubMedCentralPubMedCrossRefGoogle Scholar
  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 172:103–119PubMedCrossRefGoogle Scholar
  12. Buell S (1982) Golgi–Cox and rapid Golgi methods as applied to autopsied human brain tissue: widely disparate results. J Neuropathol Exp Neurol 41:500–507PubMedCrossRefGoogle Scholar
  13. Butler AB (2008) Evolution of brains, cognition, and consciousness. Brain Res Bull 75:442–449PubMedCrossRefGoogle Scholar
  14. Butti C, Hof PR (2010) The insular cortex: a comparative perspective. Brain Struct Funct 214:477–493PubMedCrossRefGoogle Scholar
  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 515:243–259PubMedCrossRefGoogle Scholar
  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 1225:47–58PubMedCrossRefGoogle Scholar
  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 297:670–700CrossRefGoogle Scholar
  18. Chan-Palay V, Palay SL, Billings-Gagliardi SM (1974) Meynert cells in the primate visual cortex. J Neurocytol 3:631–658PubMedCrossRefGoogle Scholar
  19. Chklovskii DB (2004) Synaptic connectivity and neuronal morphology: two sides of the same coin. Neuron 43:609–617PubMedGoogle Scholar
  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 362:587–602PubMedCentralPubMedCrossRefGoogle Scholar
  21. Cupp CJ, Uemura E (1980) Age-related changes in the prefrontal cortex of Macaca mulatta: quantitative analysis of dendritic branching patterns. Exp Neurol 69:143–163PubMedCrossRefGoogle Scholar
  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 296:159–172PubMedCrossRefGoogle Scholar
  23. de Ruiter JP (1983) The influence of post-mortem fixation delay on the reliability of the Golgi silver impregnation. Brain Res 266:143–147PubMedCrossRefGoogle Scholar
  24. Deacon TW (1990) Rethinking mammalian brain evolution. Am Zool 30:629–705CrossRefGoogle Scholar
  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 14:1–19PubMedCrossRefGoogle Scholar
  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 14:202–216PubMedCentralPubMedCrossRefGoogle Scholar
  27. Druga R (2009) Neocortical inhibitory system. Folia Biol 55:201–217Google Scholar
  28. Elias H, Schwartz D (1969) Surface areas of the cerebral cortex of mammals determined by stereological methods. Science 166:111–113PubMedCrossRefGoogle Scholar
  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 9:127–131PubMedCrossRefGoogle Scholar
  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 8:278–294PubMedCrossRefGoogle Scholar
  31. Elston GN, Oga T, Fujita I (2009) Spinogenesis and pruning scales across functional hierarchies. J Neurosci 29:3271–3275PubMedCrossRefGoogle Scholar
  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 20:1398–1408PubMedCrossRefGoogle Scholar
  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 1316:35–42PubMedCrossRefGoogle Scholar
  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 5:42PubMedCentralPubMedCrossRefGoogle Scholar
  35. Eriksen N, Pakkenberg B (2007) Total neocortical cell number in the mysticete brain. Anat Rec 290:83–95CrossRefGoogle Scholar
  36. Ferrer I (1987) The basic structure of the neocortex in insectivorous bats (Miniopterus sthreibersi and Pipistrellus pipistrellus). A Golgi study. J Hirnforsch 28:237–243PubMedGoogle Scholar
  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 178:161–173PubMedCrossRefGoogle Scholar
  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 145:217–234PubMedCentralPubMedGoogle Scholar
  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 146:87–104PubMedCentralPubMedGoogle Scholar
  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 213:241–248PubMedCentralPubMedCrossRefGoogle Scholar
  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 76:32–44PubMedCentralPubMedCrossRefGoogle Scholar
  42. Garey LJ, Winkelmann E, Brauer K (1985) Golgi and Nissl studies of the visual cortex of the bottlenose dolphin. J Comp Neurol 240:305–321PubMedCrossRefGoogle Scholar
  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 485:278–284PubMedCrossRefGoogle Scholar
  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 133:560–569PubMedCrossRefGoogle Scholar
  45. Gatesy J (1997) More DNA support for a Cetacea/Hippopotamidae clade: the blood-clotting protein gene gamma-fibrinogen. Mol Biol Evol 14:537–543PubMedCrossRefGoogle Scholar
  46. Geisler G, Uhen MD (2003) Morphological support for a close relationship between hippos and whales. J Vert Paleontol 23:991–996CrossRefGoogle Scholar
  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 30:683–691PubMedCrossRefGoogle Scholar
  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 2:1–47Google Scholar
  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 293:2239–2242PubMedCrossRefGoogle Scholar
  50. Glezer I (2002) Neural morphology. In: Hoezel AR (ed) Marine mammal biology: an evolutionary approach. Blackwell Science Ltd, Malden, pp 98–115Google Scholar
  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 24:401–427PubMedCrossRefGoogle Scholar
  52. Glezer II, Jacobs MS, Morgane PJ (1988) Implications of the “initial brain” concept for brain evolution in Cetacea. Behav Brain Sci 11:75–116CrossRefGoogle Scholar
  53. Glezer II, Hof PR, Morgane PJ (1992) Calretinin-immunoreactive neurons in the primary visual cortex of dolphin and human brains. Brain Res 595:181–188PubMedCrossRefGoogle Scholar
  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 3:249–272PubMedCrossRefGoogle Scholar
  55. Glezer I, Hof PR, Morgane PJ (1995) Cytoarchitectonics and immunocytochemistry of the inferior colliculus of midbrain in cetaceans. FASEB J 9:A247Google Scholar
  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 15:203–237PubMedCrossRefGoogle Scholar
  57. Hanson A, Grisham W, Sheh C, Annese J, Ridgway S (2013) Quantitative examination of the bottlenose dolphin cerebellum. Anat Rec 296:1215–1228CrossRefGoogle Scholar
  58. Harrison KH, Hof PR, Wang SS (2002) Scaling laws in the mammalian neocortex: does form provide clues to function? J Neurocytol 31:289–298PubMedCrossRefGoogle Scholar
  59. Hart BL, Hart LA, Pinter-Wollman N (2008) Large brains and cognition: where do elephants fit in? Neurosci Biobehav Rev 32:86–98PubMedCrossRefGoogle Scholar
  60. Hassiotis M, Ashwell KW (2003) Neuronal classes in the isocortex of a monotreme, the Australian echidna (Tachyglossus aculeatus). Brain Behav Evol 61:6–27PubMedCrossRefGoogle Scholar
  61. Herculano-Houzel S (2007) Encephalization, neuronal excess, and neuronal index in rodents. Anat Rec 290:1280–1287CrossRefGoogle Scholar
  62. Herculano-Houzel S, Mota B, Lent R (2006) Cellular scaling rules for rodent brains. Proc Natl Acad Sci USA 103:12138–12143PubMedCentralPubMedCrossRefGoogle Scholar
  63. Herculano-Houzel S, Collins CE, Wong P, Kaas JH (2007) Cellular scaling rules for primate brains. Proc Natl Acad Sci USA 104:3562–3567PubMedCentralPubMedCrossRefGoogle Scholar
  64. Herman LM, Tavolga WN (1980) The communication systems of cetaceans. In: Herman LM (ed) Cetacean behavior: mechanisms and functions. Wiley, New York, pp 149–209Google Scholar
  65. Herman LM, Peacock MF, Yunker MP, Madsen CJ (1975) Bottle-nosed dolphin: double-slit pupil yields equivalent aerial and underwater diurnal acuity. Science 189:650–652PubMedCrossRefGoogle Scholar
  66. Hof PR, Sherwood CC (2005) Morphomolecular neuronal phenotypes in the neocortex reflect phylogenetic relationships among certain mammalian orders. Anat Rec 287:1153–1163CrossRefGoogle Scholar
  67. Hof PR, Van der Gucht E (2007) Structure of the cerebral cortex of the humpback whale, Megaptera novaeangliae (Cetacea, Mysticeti, Balaenopteridae). Anat Rec 290:1–31CrossRefGoogle Scholar
  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 146:91–95PubMedCrossRefGoogle Scholar
  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 36:275–284PubMedCrossRefGoogle Scholar
  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 16:77–116PubMedCrossRefGoogle Scholar
  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 55:300–310PubMedCrossRefGoogle Scholar
  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 420:113–126PubMedCrossRefGoogle Scholar
  73. Hof PR, Chanis R, Marino L (2005) Cortical complexity in cetacean brains. Anat Rec 287:1142–1152CrossRefGoogle Scholar
  74. Huggenberger S (2008) The size and complexity of dolphin brains—A paradox? J Mar Biol Assoc UK 88:1103–1108CrossRefGoogle Scholar
  75. Jacobs B, Scheibel AB (1993) A quantitative dendritic analysis of Wernicke’s area in humans. I. Lifespan changes. J Comp Neurol 327:83–96PubMedCrossRefGoogle Scholar
  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 111–131CrossRefGoogle Scholar
  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 141:205–271PubMedCrossRefGoogle Scholar
  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 1:1–108CrossRefGoogle Scholar
  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 225:396–432PubMedCrossRefGoogle Scholar
  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 386:661–680PubMedCrossRefGoogle Scholar
  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 11:558–571PubMedCrossRefGoogle Scholar
  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 215:273–298PubMedCrossRefGoogle Scholar
  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 8:24PubMedCentralPubMedGoogle Scholar
  85. Kawaguchi Y (1995) Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J Neurosci 15:2638–2655PubMedGoogle Scholar
  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 77:79–90PubMedCrossRefGoogle Scholar
  87. Kesarev VS (1971) The inferior brain of the dolphin. Soviet Sci Rev 2:52–58Google Scholar
  88. Kesarev VS (1975) Homologization of the cerebral neocortex in cetaceans. Arkhiv Anat Gistol Embriol 68:5–13Google Scholar
  89. Kesarev VS, Malofeeva LI (1969) Structural organization of the motor zone of the cerebral cortex in dolphins. Arkh Anat Gistol Embriol 56:48–55PubMedGoogle Scholar
  90. Kesarev VS, Malofeeva LI, Trykova OV (1977) Structural organization of the cetacean neocortex. Arkh Anat Gistol Embriol 73:23–30PubMedGoogle Scholar
  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 113:793–812PubMedCrossRefGoogle Scholar
  92. Kraus C, Pilleri G (1969a) Quantitative Untersuchungen über die Grosshirnrinde der Cetaceen. Investig Cetacea 1:127–150Google Scholar
  93. Kraus C, Pilleri G (1969b) Zur Feinstrucktur der großen Pyramidenzellen in der V Cortexschicht der Cetacean (Delphinus delphis und Balaenoptera borealis. Investig Cetacea 1:89–99Google Scholar
  94. Kraus C, Pilleri G (1969c) Zur Histologie der Grosshirnrinde von Balaenoptera borealis Lesson (Cetacea, Mysticeti). Investig Cetacea 1:151–170Google Scholar
  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 13:712–718PubMedGoogle Scholar
  96. Ladygina TF, Mass AM, Supin A (1978) Multiple sensory projections in the dolphin cerebral cortex. Zh Vyssh Nerv Deiat Pavl 28:1047–1053Google Scholar
  97. Le Gros Clark WE (1942) The cells of Meynert in the visual cortex of the monkey. J Anat 76:369–376PubMedCentralPubMedGoogle Scholar
  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 253:135–152PubMedCrossRefGoogle Scholar
  99. Lund JS, Lewis DA (1993) Local circuit neurons of developing and mature macaque prefrontal cortex: Golgi and immunocytochemical characteristics. J Comp Neurol 328:282–312PubMedCrossRefGoogle Scholar
  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 81:293–338PubMedCrossRefGoogle Scholar
  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 250:664–696PubMedCrossRefGoogle Scholar
  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 10:153–166PubMedCrossRefGoogle Scholar
  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 64:42–60PubMedCrossRefGoogle Scholar
  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 2:5PubMedCentralPubMedCrossRefGoogle Scholar
  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 520:2430–2439PubMedCrossRefGoogle Scholar
  106. Marino L (2002) Convergence of complex cognitive abilities in cetaceans and primates. Brain Behav Evol 59:21–32PubMedCrossRefGoogle Scholar
  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 262:429–439PubMedCrossRefGoogle Scholar
  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 203:393–402PubMedCrossRefGoogle Scholar
  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 264:397–414PubMedCrossRefGoogle Scholar
  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 268:411–429PubMedCrossRefGoogle Scholar
  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 203:57–76PubMedCentralPubMedCrossRefGoogle Scholar
  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 257:308–347PubMedCrossRefGoogle Scholar
  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 281:1256–1263CrossRefGoogle Scholar
  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 279:601–610CrossRefGoogle Scholar
  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:e139PubMedCentralPubMedCrossRefGoogle Scholar
  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 83:417–440PubMedGoogle Scholar
  117. Masland RH (2004) Neuronal cell types. Curr Biol 14:R497–R500PubMedCrossRefGoogle Scholar
  118. Mendizabal-Zubiaga JL, Reblet C, Bueno-Lopez JL (2007) The underside of the cerebral cortex: layer V/VI spiny inverted neurons. J Anat 211:223–236PubMedCentralPubMedCrossRefGoogle Scholar
  119. Meyer G (1987) Forms and spatial arrangement of neurons in the primary motor cortex of man. J Comp Neurol 262:402–428PubMedCrossRefGoogle Scholar
  120. Meynert T (1867) Der Bau der Grosshirnrinde und seine örtlichen Verschiedenheiten nebst einem pathologisch anatomischen Corollarium. Vierteljahrsch Psychiatr 198–217Google Scholar
  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 113–131CrossRefGoogle Scholar
  122. Miller MW (1988) Maturation of rat visual cortex: IV. The generation, migration, morphogenesis, and connectivity of atypically oriented pyramidal neurons. J Comp Neurol 274:387–405PubMedCrossRefGoogle Scholar
  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 290:1459–1479CrossRefGoogle Scholar
  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 291:263–282CrossRefGoogle Scholar
  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 5:1–107CrossRefGoogle Scholar
  126. Morgane PJ, McFarland WL, Jacobs MS (1982) The limbic lobe of the dolphin brain: a quantitative cytoarchitectonic study. J Hirnforsch 23:465–552PubMedGoogle Scholar
  127. Morgane PJ, Jacobs MS, Galaburda A (1985) Conservative features of neocortical evolution in dolphin brain. Brain Behav Evol 26:176–184PubMedCrossRefGoogle Scholar
  128. Morgane PJ, Glezer II, Jacobs MS (1988) Visual cortex of the dolphin: an image analysis study. J Comp Neurol 273:3–25PubMedCrossRefGoogle Scholar
  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 215–262Google Scholar
  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 8:5PubMedCentralPubMedCrossRefGoogle Scholar
  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 96:10261–10266PubMedCentralPubMedCrossRefGoogle Scholar
  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 98:7384–7389PubMedCentralPubMedCrossRefGoogle Scholar
  133. Oelschläger HA, Oelschläger JS (2008) Brain. In: Perrin WF, Würsig B, Thewissen JGM (eds) Encyclopedia of marine mammals. Academic Press, San Diego, pp 134–149Google Scholar
  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 71:68–86PubMedCrossRefGoogle Scholar
  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 75:33–62PubMedCrossRefGoogle Scholar
  136. Parnavelas JG, Lieberman AR, Webster KE (1977a) Organization of neurons in the visual cortex, area 17, of the rat. J Anat 124:305–322PubMedCentralPubMedGoogle Scholar
  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 183:499–517PubMedCrossRefGoogle Scholar
  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 Google Scholar
  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 107–121Google Scholar
  140. Peters A, Regidor J (1981) A reassessment of the forms of nonpyramidal neurons in area 17 of cat visual cortex. J Comp Neurol 203:685–716PubMedCrossRefGoogle Scholar
  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 16:49–56PubMedCrossRefGoogle Scholar
  142. Revishchin AV, Garey LJ (1989) Sources of thalamic afferent neurons, projecting into the suprasylvian gyrus of the dolphin cerebral cortex. Neirofiziol 21:529–539Google Scholar
  143. Ridgway S, Brownson RH (1984) Relative brain sizes and cortical surface areas in odontocetes. Acta Zool Fenn 172:149–152Google Scholar
  144. Sanides F, Sanides D (1972) The “extraverted neurons” of the mammalian cerebral cortex. Z Anat Entwickl-gesch 136:272–293CrossRefGoogle Scholar
  145. Sarko DK, Catania KC, Leitch DB, Kaas JH, Herculano-Houzel S (2009) Cellular scaling rules of insectivore brains. Front Neuroanat 3:8PubMedCentralPubMedCrossRefGoogle Scholar
  146. Sasaki S, Iwata M (2001) Ultrastructural study of Betz cells in the primary motor cortex of the human brain. J Anat 199:699–708PubMedCentralPubMedCrossRefGoogle Scholar
  147. Scheibel ME, Scheibel AB (1978) The methods of Golgi. In: Neuroanatomical research techniques. Academic Press, New York, pp 89–114Google Scholar
  148. Schwartz SP, Coleman PD (1981) Neurons of origin of the perforant path. Exp Neurol 74:305–312PubMedCrossRefGoogle Scholar
  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 61:28–44PubMedCrossRefGoogle Scholar
  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 213:301–328PubMedCrossRefGoogle Scholar
  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 388:666–670PubMedCrossRefGoogle Scholar
  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 16:1046–1060PubMedCrossRefGoogle Scholar
  153. Sholl DA (1953) Dendritic organization in the neurons of the visual and motor cortices of the cat. J Anat 87:387–406PubMedCentralPubMedGoogle Scholar
  154. Sokolov VE, Ladygina TF, Supin A (1972) Localization of sensory zones in the dolphin cerebral cortex. Proc Acad Sci USSR 202:490–493Google Scholar
  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 10:261–294PubMedCrossRefGoogle Scholar
  156. Thewissen JG, Williams EM, Roe LJ, Hussain ST (2001) Skeletons of terrestrial cetaceans and the relationship of whales to artiodactyls. Nature 413:277–281PubMedCrossRefGoogle Scholar
  157. Thewissen JGM, Cooper LN, Clementz MT, Bajpai S, Tiwari BN (2007) Whales originated from aquatic artiodactyls in the Eocene epoch of India. Nature 450:1190–1194PubMedCrossRefGoogle Scholar
  158. Travis K, Ford K, Jacobs B (2005) Regional dendritic variation in neonatal human cortex: a quantitative Golgi study. Dev Neurosci 27:277–287PubMedCrossRefGoogle Scholar
  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 18:127–151PubMedCrossRefGoogle Scholar
  160. Walshe F (1942) The giant cells of Betz, the motor cortex and the pyramidal tract: a critical review. Brain 65:409–461CrossRefGoogle Scholar
  161. Wen Q, Chklovskii DB (2008) A cost–benefit analysis of neuronal morphology. J Neurophysiol 99:2320–2328PubMedCrossRefGoogle Scholar
  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 37:13–33PubMedCrossRefGoogle Scholar
  163. Winfield DA, Powell TP (1983) Laminar cell counts and geniculo-cortical boutons in area 17 of cat and monkey. Brain Res 277:223–229PubMedCrossRefGoogle Scholar
  164. Wittenberg GMWS (2008) Evolution and scaling of dendrites. In: Stuart G, Spruston N, Hausser M (eds) Dendrites. Oxford University Press, New York, pp 43–67Google Scholar
  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 19:1597–1615PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Camilla Butti
    • 1
  • Caroline M. Janeway
    • 2
  • Courtney Townshend
    • 2
  • Bridget A. Wicinski
    • 1
  • Joy S. Reidenberg
    • 3
  • Sam H. Ridgway
    • 4
  • Chet C. Sherwood
    • 5
  • Patrick R. Hof
    • 1
  • Bob Jacobs
    • 2
  1. 1.Fishberg Department of Neuroscience and Friedman Brain InstituteIcahn School of Medicine at Mount SinaiNew YorkUSA
  2. 2.Laboratory of Quantitative Neuromorphology, PsychologyColorado CollegeColorado SpringsUSA
  3. 3.Center for Anatomy and Functional MorphologyIcahn School of Medicine at Mount SinaiNew YorkUSA
  4. 4.National Marine Mammal FoundationSan DiegoUSA
  5. 5.Department of AnthropologyThe George Washington UniversityWashingtonUSA

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