Brain Structure and Function

, Volume 215, Issue 3–4, pp 273–298 | Cite as

Neuronal morphology in the African elephant (Loxodonta africana) neocortex

  • Bob Jacobs
  • Jessica Lubs
  • Markus Hannan
  • Kaeley Anderson
  • Camilla Butti
  • Chet C. Sherwood
  • Patrick R. Hof
  • Paul R. Manger
Original Article

Abstract

Virtually nothing is known about the morphology of cortical neurons in the elephant. To this end, the current study provides the first documentation of neuronal morphology in frontal and occipital regions of the African elephant (Loxodonta africana). Cortical tissue from the perfusion-fixed brains of two free-ranging African elephants was stained with a modified Golgi technique. Neurons of different types (N = 75), with a focus on superficial (i.e., layers II–III) pyramidal neurons, were quantified on a computer-assisted microscopy system using Neurolucida software. Qualitatively, elephant neocortex exhibited large, complex spiny neurons, many of which differed in morphology/orientation from typical primate and rodent pyramidal neurons. Elephant cortex exhibited a V-shaped arrangement of bifurcating apical dendritic bundles. Quantitatively, the dendrites of superficial pyramidal neurons in elephant frontal cortex were more complex than in occipital cortex. In comparison to human supragranular pyramidal neurons, elephant superficial pyramidal neurons exhibited similar overall basilar dendritic length, but the dendritic segments tended to be longer in the elephant with less intricate branching. Finally, elephant aspiny interneurons appeared to be morphologically consistent with other eutherian mammals. The current results thus elaborate on the evolutionary roots of Afrotherian brain organization and highlight unique aspects of neural architecture in elephants.

Keywords

Dendrite Morphometry Dendritic spine Golgi method Brain evolution 

References

  1. Anderson K, Bones B, Robinson B, Hass C, Lee H, Ford K, Roberts T-A, 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. Anderson K, Yamamoto E, Kaplan J, Hannan M, Jacobs B (2010) Neurolucida lucivid versus Neurolucida camera: a quantitative and qualitative comparison of three-dimensional neuronal reconstructions. J Neurosci Methods 186:209–214PubMedCrossRefGoogle Scholar
  3. Badlangana NL, Bhagwandin A, Fuxe K, Manger PR (2007) Observations on the giraffe central nervous system related to the corticospinal tract, motor cortex and spinal cord: what difference does a long neck make? Neuroscience 148:522–534PubMedCrossRefGoogle Scholar
  4. Barasa A (1960) Forma, grandezza e densità dei neuroni della corteccia cerebrale in mammiferi di grandezza corporea differente. Z Zellforsch 53:69–89PubMedCrossRefGoogle Scholar
  5. Barasa A, Shochatovitz A (1961) Grandezza e densità della cellule nervose della corteccia cerebrale de Elephas indicus. Rendiconti Accad Naz Lincei 30:246–249Google Scholar
  6. Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primate prefrontal cortex. Neurosci Biobehav Rev 19:499–510PubMedCrossRefGoogle Scholar
  7. Bartesaghi R, Severo S, Guidi S (2003) Effects of early environment on pyramidal neuron morphology in field CA1 of the guinea-pig. Neuroscience 116:715–732PubMedCrossRefGoogle Scholar
  8. Bates LA, Sayialel KN, Njiraini NW, Moss CJ, Poole JH, Byrne RW (2007a) Elephants classify human ethnic groups by odor and garment color. Curr Biol 17:1938–1942PubMedCrossRefGoogle Scholar
  9. Bates LA, Sayialel KN, Njiraini NW, Poole JH, Moss CJ, Byrne RW (2007b) African elephants have expectations about the locations of out-of-site family members. Biol Lett 4:34–36CrossRefGoogle Scholar
  10. Bates LA, Lee PC, Njiraini NW, Poole JH, Sayialel KN, Sayialel S, Sayialel S, Moss CJ, Byrne RW (2008a) Do elephants show empathy? J Consc Stud 15:204–225Google Scholar
  11. Bates LA, Poole JH, Byrne RW (2008b) Elephant cognition. Curr Biol 18:R544–R546PubMedCrossRefGoogle Scholar
  12. Benavides-Piccione R, Hamzei-Sichani F, Ballesteros-Yáñez I, DeFelipe J, Yuste R (2006) Dendritic size of pyramidal neurons differs among mouse cortical regions. Cereb Cortex 16:990–1001PubMedCrossRefGoogle Scholar
  13. Bianchi S, Bauernfeind AL, Stimpson CD, Bonar CJ, Manger PR, Hof PR, Jacobs B, Sherwood CC Neuronal diversity in Afrotheria: a Golgi study of the rock hyrax (Procavia capensis) neocortex and comparison with the African elephant (Loxodonta africana). NY Acad Sci (in review)Google Scholar
  14. Bok ST (1959) Histonomy of the cerebral cortex. Elsevier, AmsterdamGoogle Scholar
  15. Bota M, Swanson LW (2007) The neuron classification problem. Brain Res Rev 56:79–88PubMedCrossRefGoogle Scholar
  16. 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
  17. Braak H, Braak E (1985) Golgi preparations as a tool in neuropathology with particular reference to investigations of the human telencephalic cortex. Prog Neurobiol 25:93–139PubMedCrossRefGoogle Scholar
  18. Brown KM, Gillette TA, Ascoli GA (2008) Quantifying neuronal size: summing up trees and splitting the branch difference. Semin Cell Dev Biol 19:485–493PubMedCrossRefGoogle Scholar
  19. Bueno-López JL, Reblet C, López-Medina A, Gómez-Urquijo Grandes P, Gondra J, Hennequet L (1991) Targets and laminar distribution of projection neurons with “inverted” morphology in rabbit cortex. Eur J Neurosci 3:415–430PubMedCrossRefGoogle Scholar
  20. Butti C, Hof PR (2010) The insular cortex: a comparative perspective. Brain Struct Func 214:477–493CrossRefGoogle Scholar
  21. 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
  22. Constantinidis C, Williams GV, Goldman-Rakic PS (2002) A role for inhibition in shaping the temporal flow of information in prefrontal cortex. Nat Neurosci 5:175–180PubMedCrossRefGoogle Scholar
  23. Cozzi B, Spagnoli S, Bruno L (2001) An overview of the central nervous system of the elephant through a critical appraisal of the literature published in the XIX and XX centuries. Brain Res Bull 54:219–227PubMedCrossRefGoogle Scholar
  24. de Crinis M (1934) Über die Spezialzellen in der menschlichen Grosshirnrinde. J Psych Neurol. 45:439–449Google Scholar
  25. 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
  26. 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
  27. 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
  28. DeFelipe J, Alonso-Nanclares L, Arellano JI (2002) Microstructure of the neocortex: comparative aspects. J Neurocytol 31:299–316PubMedCrossRefGoogle Scholar
  29. Druga R (2009) Neocortical inhibitory system. Folia Biol (Prague) 55:201–217Google Scholar
  30. Elston GN (2003) Cortex, cognition and the cell: new insights into the pyramidal neuron and prefrontal function. Cereb Cortex 13:1124–1138PubMedCrossRefGoogle Scholar
  31. Elston GN (2007) Specialization of the neocortical pyramidal cell during primate evolution. In: Kass JH, Preuss TM (eds) Evolution of nervous systems: a comprehensive reference, vol 4. Elsevier, New York, pp 191–242CrossRefGoogle Scholar
  32. Elston GN, Rosa MGP (1997) The occipitoparietal pathway of the macaque monkey: comparison of pyramidal cell morphology in layer III of functionally related cortical visual areas. Cereb Cortex 7:432–452PubMedCrossRefGoogle Scholar
  33. Elston GN, Rosa MGP (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
  34. Elston GN, Rosa MGP (1998b) Morphological variation of layer III pyramidal neurones in the occipitotemporal pathway of the macaque monkey visual cortex. Cereb Cortex 8:278–294PubMedCrossRefGoogle Scholar
  35. Elston GN, Rosa MGP, Calford MB (1996) Comparison of dendritic fields of layer III pyramidal neurons in striate and extrastriate visual areas of the marmoset: a Lucifer Yellow intracellular injection study. Cereb Cortex 6:807–813PubMedCrossRefGoogle Scholar
  36. Ferrer I (1986) Golgi study of the isocortex in an insectivore: the common European mole (Talpa europaea). Brain Behav Evol 29:105–114PubMedCrossRefGoogle Scholar
  37. Ferrer I (1987) The basic structure of the neocortex in insectivorous bats (Miniopterus sthreibersi and Pipistrellus pipistrellus). J Hirnforsch 28:237–243PubMedGoogle Scholar
  38. 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 (Berl) 178:161–173CrossRefGoogle Scholar
  39. Ferrer I, Fabregues 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 145:217–234PubMedGoogle Scholar
  40. Ferrer I, Fabregues 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 146:87–104PubMedGoogle Scholar
  41. Ferrer I, Fábregues I, Condom E (1987) A Golgi study of the sixth layer of the cerebral cortex III. Neuronal changes during normal and abnormal cortical folding. J Anat 152:71–82PubMedGoogle Scholar
  42. Fitzpatrick DC, Henson OW (1994) Cell types in the mustached bat auditory cortex. Brain Behav Evol 43:79–91PubMedCrossRefGoogle Scholar
  43. Fleischhauer K (1974) On different patterns of dendritic bundling in the cerebral cortex of the cat. Z Anat Entwickl-Gesch 143:115–126CrossRefGoogle Scholar
  44. Fleischhauer K, Petsche H, Wittkowski W (1972) Vertical bundles of dendrites in the neocortex. Anat Embryol 136:213–223CrossRefGoogle Scholar
  45. Foxe JJ, Simpson GV (2002) Flow of activation from V1 to frontal cortex in humans. Exp Brain Res 142:139–150PubMedCrossRefGoogle Scholar
  46. 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
  47. Garstang M (2004) Long-distance, low-frequency elephant communication. J Comp Physiol A 190:791–805CrossRefGoogle Scholar
  48. Geisler HC, Ijkema-Paassen J, Westerga J, Gramsbergen A (2000) Vestibular deprivation and the development of dendritic bundles in the rat. Neural Plast 7:193–203PubMedCrossRefGoogle Scholar
  49. 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
  50. Gheerbrant E, Tassy P (2009) L’origine et l’évolution des elephants. C R Palevol 8:281–294CrossRefGoogle 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 hale. 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. Goodman M, Sterner KN, Islam M, Uddin M, Sherwood CC, Hof PR, Hou Z-C, Lipovich L, Jia H, Grossman LI, Wildman DE (2009) Phylogenomic analyses reveal convergent patterns of adaptive evolution in elephant and human ancestries. Proc Natl Acad Sci USA 106:20824–20829PubMedCrossRefGoogle Scholar
  54. Grande F (1980) Energy expenditure of organs and tissues. In: Kinney JM (ed) Assessment of energy metabolism in health and disease: report of the first Ross conference on medical research. Ross Laboratories, Columbus, pp 88–92Google Scholar
  55. Gravett N, Bhagwandin A, Fuxe K, Manger PR (2009) Nuclear organization and morphology of cholinergic, putative catecholaminergic and serotonergic neurons in the brain of the rock hyrax, Procavia capensis. J Chem Neuroanat 38:57–74PubMedCrossRefGoogle Scholar
  56. Group Petilla Interneuron Nomenclature (2008) Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 9:557–568Google Scholar
  57. Hakeem AY, Hof PR, Sherwood CC, Switzer RC, Rasmussen LRL, Allman JM (2005) Brain of the African elephant (Loxodonta africana): neuroanatomy from magnetic resonance images. Anat Rec 287A:1117–1127CrossRefGoogle Scholar
  58. Hakeem AY, Sherwood CC, Bonar CJ, Butti C, Hof PR, Allman JM (2009) Von Economo neurons in the elephant brain. Anat Rec 292:242–248CrossRefGoogle Scholar
  59. Harrison KH, Hof PR, Wang SS-H (2002) Scaling laws in the mammalian neocortex: does form provide blues to function? J Neurocytol 31:289–298PubMedCrossRefGoogle Scholar
  60. Hart BL, Hart LA (2007) Evolution of the elephant brain: a paradox between brain size and cognitive behavior. In: Kaas JH, Krubitzer LA (eds) Evolution of nervous systems: a comprehensive reference. Vol 3: Mammals. Elsevier, Amsterdam (NL), pp 491–497Google Scholar
  61. Hart BL, Hart LA (2010) Unique attributes of the elephant mind offer perspectives on the human mind. In: Smith J, Mitchell RW (eds) Experiencing animals: encounters between animals and human minds. Columbia University Press, New York (in press)Google Scholar
  62. Hart BL, Hart LA, McCoy M, Sarath CR (2001) Cognitive behaviour in Asian elephants: use and modification of branches for fly switching. Anim Behav 62:839–847CrossRefGoogle Scholar
  63. Hart BL, Hart LA, Pinter-Wollman N (2008) Large brains and cognition: where do elephants fit in? Neurosci Biobehav Rev 32:86–98PubMedCrossRefGoogle Scholar
  64. Hassiotis M, Ashwell KWS (2003) Neuronal classes in the isocortex of a monotreme, the Australian echidna (Tachyglossus aculeatus). Brain Behav Evol 61:6–27PubMedCrossRefGoogle Scholar
  65. Hassiotis M, Paxinos G, Ashwell KWS (2003) The anatomy of the cerebral cortex of the echidna (Tachyglossus aculeatus). Comp Biochem Physiol Part A 136:827–850CrossRefGoogle Scholar
  66. Hassiotis M, Paxinos G, Ashwell KWS (2005) Cyto- and chemoarchitecture of the cerebral cortex of an echidna (Tachyglossus aculeatus) II. Laminar organization and synaptic density. J Comp Neurol 482:94–122PubMedCrossRefGoogle Scholar
  67. Haug H (1970) Die makrospkoschie Aufbau des Großhirns: qualitative und quantitative Untersuchungen an den Gehirnen des Menschen der Delphinoideae und des Elefanten. Springer, BerlinGoogle Scholar
  68. Haug H (1987) Brain sizes, surfaces, and neuronal sizes of the cortex cerebri: a stereological investigation of man and his variability and a comparison with some mammals (primates, whales, marsupials, insectivores, and one elephant). Am J Anat 180:126–142PubMedCrossRefGoogle Scholar
  69. Hof PR, Sherwood CC (2005) Morphomolecular neuronal phenotypes in the neocortex reflect phylogenetic relationships among certain mammalian orders. Anat Rec 287A:1153–1163CrossRefGoogle Scholar
  70. Hof PR, Van der Gucht E (2007) Structure of the cerebral cortex of the humpback whale, Megaptera novaeangliae (Cetacea, Mysticeti, Balaeopteridae). Anat Rec 290:1–31CrossRefGoogle Scholar
  71. 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
  72. Hof PR, Bogaert YE, Rosenthal RE, Fiskum G (1996) Distribution of neuronal populations containing neurofilament protein and calcium-binding proteins in the canine neocortex: regional analysis and cell typology. J Chem Neuroanat 11:81–98PubMedCrossRefGoogle Scholar
  73. 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
  74. Hof PR, Chanis R, Marino L (2005) Cortical complexity in cetacean brains. Anat Rec 287A:1142–1152CrossRefGoogle Scholar
  75. Hoffmann JN, Montag AG, Dominy NJ (2004) Meissner corpuscles and somatosensory acuity: the prehensile appendages of primates and elephants. Anat Rec 281A:1138–1147CrossRefGoogle Scholar
  76. Hofman MA (1982) Encephalization in mammals in relation to the size of the cerebral cortex. Brain Behav Evol 20:84–96PubMedCrossRefGoogle Scholar
  77. Horner CH, Arbuthnott E (1991) Methods of estimation of spine density—are spines evenly distributed throughout the dendritic field? J Anat 177:179–184PubMedGoogle Scholar
  78. Hou ZC, Romero R, Wildman DE (2009) Phylogeny of the Ferungulata (Mammalia: Laurasiatheria) as determined from phylogenomic data. Mol Phylogenet Evol 52:660–664PubMedCrossRefGoogle Scholar
  79. Innocenti GM, Vercelli A (2010) Dendritic bundles, minicolumns, columns, and cortical output units. Front Neuroanat 4:1–7CrossRefGoogle Scholar
  80. 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
  81. Jacobs B, Scheibel AB (2002) Regional dendritic variation in primate cortical pyramidal cells. In: Schüz A, Miller R (eds) Cortical areas: unity and diversity (Conceptual advances in brain research series). Taylor & Francis, London, pp 111–131Google Scholar
  82. Jacobs B, Schall M, Scheibel AB (1993) A quantitative dendritic analysis of Wernicke’s area in humans II. Gender, hemispheric, and environmental factors. J Comp Neurol 327:97–111PubMedCrossRefGoogle Scholar
  83. Jacobs B, Driscoll L, Schall M (1997) Life-span dendritic and spine changes in areas 10 and 18 of human cortex: a quantitative Golgi study. J Comp Neurol 386:661–680PubMedCrossRefGoogle Scholar
  84. Jacobs B, Schall M, Prather M, Kapler E, Driscoll L, Baca S (2001) Regional dendritic and spine variation in human cerebral cortex: a quantitative Golgi study. Cereb Cortex 11:558–571PubMedCrossRefGoogle Scholar
  85. Jones EG (1984) Neurogliaform or spiderweb cells. In: Peters A, Jones EG (eds) Cerebral cortex. Plenum Press, New York and London, pp 409–418Google Scholar
  86. Juba A (1934) Über seltenere Ganglienzellformen der Grosshirnrinde. Z Zellforsch 21:441–447CrossRefGoogle Scholar
  87. Kaiserman-Abramof IR, Peters A (1972) Some aspects of the morphology of Betz cells in the cerebral cortex of the cat. Brain Res 43:527–546PubMedCrossRefGoogle Scholar
  88. Kawaguchi Y (1995) Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J Neurosci 15:2638–2665PubMedGoogle Scholar
  89. Kesarev VS (1975) Homologization of the cerebral neocortex in cetaceans. Arkh Anat Gistol Embriol 68:5–13PubMedGoogle Scholar
  90. Kisvárday ZF, Gulyas A, Beroukas D, North JB, Chub IW, Somogyi P (1990) Synapses, axonal and dendritic patterns of GABA-immunoreactive neurons in human cerebral cortex. Brain 113:793–812PubMedCrossRefGoogle Scholar
  91. Kupsky WJ, Marchant GH, Cook K, Shoshani J (2001) Morphologic analysis of the hippocampal formation in Elephas maximus and Loxodonta africana with comparison to that of human. In: Cavarretta G, Gioia P, Mussi M, Palombo MR (eds) Proceedings of the first international congress of La Terra degli Elefanti, the world of elephants. Consiglio Nazionale delle Ricerche, Rome (IT), pp 643–647Google Scholar
  92. Lübke J, Egger V, Sakmann B, Feldmeyer D (2000) Columnar organization of dendrites and axons of single and synaptically coupled excitatory spiny neurons in layer 4 of the rat barrel cortex. J Neurosci 20:5300–5311PubMedGoogle Scholar
  93. Lübke J, Roth A, Feldmeyer D, Sakmann B (2003) Morphometric analysis of the columnar innervation domain of neurons connecting layer 4 and layer 2/3 of juvenile rat barrel cortex. Cereb Cortex 13:1051–1063PubMedCrossRefGoogle Scholar
  94. Lund JS, Lewis DA (1993) Local circuit neurons of developing mature macaque prefrontal cortex: Golgi and immunocytochemical characteristics. J Comp Neurol 328:282–312PubMedCrossRefGoogle Scholar
  95. Lyck L, Dalmau Santamaria I, Pakkenberg B, Chemnitz J, Daa Schrøder H, Finsen B, Gundersen HJG (2009) An empirical analysis of the precision of estimating the numbers of neurons and glia in human neocortex using a fractionator-design with sub-sampling. J Neurosci Methods 182:143–156PubMedCrossRefGoogle Scholar
  96. Manger PR, Sum M, Szymanski M, Ridgway S, Krubitzer L (1998) Modular subdivisions of dolphin insular cortex: does evolutionary history repeat itself? J Cogn Neurosci 10:153–166PubMedCrossRefGoogle Scholar
  97. Manger PR, Cort J, Ebrahim N, Goodman A, Henning J, Karolia M, Rodrigues S-L, Strkalj G (2008) Is 21st century neuroscience too focused on the rat/mouse model of the brain function and dysfunction? Front Neuroanat 2:1–7CrossRefGoogle Scholar
  98. Manger PR, Pillay P, Madeko BC, Bhagwandin A, Gravett N, Moon D-J, Jillani N, Hemingway J (2009) Acquisition of brains from the African elephant (Loxodonta africana): Perfusion-fixation and dissection. J Neurosci Methods 179:16–21PubMedCrossRefGoogle Scholar
  99. Manger PR, Hemingway J, Haagensen M, Gilissen E (2010) Cross-sectional area of the elephant corpus callosum: comparison to other eutherian mammals. Neuroscience 167:815–824PubMedCrossRefGoogle Scholar
  100. Markowitz H, Schmidt M, Nadal L, Squire L (1975) Do elephants ever forget? J Appl Behav Anal 8:333–335PubMedCrossRefGoogle Scholar
  101. Masland RH (2004) Neuronal cell types. Curr Biol 14:R497–R500PubMedCrossRefGoogle Scholar
  102. McComb K, Moss C, Sayialel S, Baker L (2000) Unusually extensive networks of vocal recognition in African elephants. Anim Behav 59:103–1109CrossRefGoogle Scholar
  103. McComb K, Moss C, Durant SM, Baker L, Sayialel S (2001) Matriarchs as repositories of social knowledge in African elephants. Science 292:491–494PubMedCrossRefGoogle Scholar
  104. Mendizabal-Zubiaga JL, Reblet C, Bueno-Lopez JL (2007) The underside of the cerebral cortex: layer V/VI spiny inverted neurons. J Anat 211:223–236PubMedCrossRefGoogle Scholar
  105. Meyer G (1987) Forms and spatial arrangement of neurons in the primary motor cortex of man. J Comp Neurol 262:402–428PubMedCrossRefGoogle Scholar
  106. Miller MW (1988) Maturation of rat visual cortex: IV. The generation, migration, morphogenesis and connectivity of atypically oriented pyramidal cells. J Comp Neurol 274:387–405PubMedCrossRefGoogle Scholar
  107. Morest DK, Morest RR (2005) Perfusion-fixation of the brain with chrome-osmium solutions for the rapid Golgi method. Am J Anat 118:811–831CrossRefGoogle Scholar
  108. Mountcastle VB (1997) The columnar organization of the neocortex. Brain 120:701–722PubMedCrossRefGoogle Scholar
  109. Ngowyang G (1932) Beschreibung einer Art von Specialzellen in der Inselrinde. J Psychol Neurol 44:671–674Google Scholar
  110. Ngowyang G (1936) Neuere Befunde über die Gabelzellen. Z Zellforsch 25:236–239CrossRefGoogle Scholar
  111. Nimchinsky EA, Vogt BA, Morrison JH, Hof PR (1995) Spindle neurons of the human anterior cingulate cortex. J Comp Neurol 355:27–37PubMedCrossRefGoogle Scholar
  112. Ong WY, Garey LJ (1990) Neuronal architecture of the human temporal cortex. Anat Embryol 181:351–364PubMedCrossRefGoogle Scholar
  113. Parnavelas JG, Lieberman AR, Webster KE (1977) Organization of neurons in the visual cortex, area 17, of the rat. J Anat 124:305–322PubMedGoogle Scholar
  114. 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
  115. Pieters R, Gravett N, Fuxe K, Manger PR (2010) Nuclear organization of cholinergic, putative catecholaminergic and serotonergic nuclei in the brain of the eastern rock elephant shrew, Elephantulus myurus. J Chem Neuroanat 39:175–188PubMedCrossRefGoogle Scholar
  116. Plotnik JM, de Waal FBM, Reiss D (2006) Self-recognition in an Asian elephant. Proc Natl Acad Sci USA 103:17053–17057PubMedCrossRefGoogle Scholar
  117. Poole JH (1999) Signals and assessment in African elephants: evidence from playback experiments. Anim Behav 58:185–193PubMedCrossRefGoogle Scholar
  118. Poole J, Moss CJ (2008) Elephant sociality and complexity: the scientific evidence. In: Wemmer CC (ed) Elephants and ethics: towards a morality of coexistence. John Hopkins University Press, Baltimore, pp 69–98Google Scholar
  119. Poole JH, Tyack PL, Stoeger-Horwath AS, Watwood S (2005) Elephants are capable of vocal learning: two animals coin unexpected sounds as a surprising form of social communication. Nature 434:455–456PubMedCrossRefGoogle Scholar
  120. Povysheva NV, Zaitsev AV, Kröner S, Krimer OA, Rotaru DC, González-Burgos G, Lewis DA, Krimer LS (2007) Electrophysiological differences between neurogliaform cells from monkey and rat prefrontal cortex. J Neurophysiol 97:1030–1039PubMedCrossRefGoogle Scholar
  121. Qi H-X, 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
  122. Ramón y, Cajal S (1891) On the structure of the cerebral cortex of certain mammals. (La Cellule 7:125–176). In: DeFelipe J, Jones EG (trans. and eds) Cajal on the cerebral cortex: an annotated translation on the complete writings (History of neuroscience; No 1) (1988) Oxford University Press, New York, pp 23–54Google Scholar
  123. Ramón y Cajal S (1922) Studien über die Sehrinde der Katze. J Psychol Neurol 29:161–181Google Scholar
  124. Roney KJ, Scheibel AB, Shaw GL (1979) Dendritic bundles: survey of anatomical experiments and physiological theories. Brain Res Rev 1:225–271CrossRefGoogle Scholar
  125. Roth G, Dicke U (2005) Evolution of the brain and intelligence. Trends Cogn Sci 9:250–257PubMedCrossRefGoogle Scholar
  126. Sanides F, Sanides D (1972) The “extraverted neurons” of the mammalian cerebral cortex. Z Anat Entwickl-Gesch 136:272–293CrossRefGoogle Scholar
  127. Scheibel ME, Scheibel AB (1975) Dendrite bundles, central programs and the olfactory bulb. Brain Res 95:407–421PubMedCrossRefGoogle Scholar
  128. Scheibel ME, Scheibel AB (1978a) The dendritic structure of the human Betz cell. In: Brazier MAB, Petsche H (eds) Architectonics of the cerebral cortex (IBRO) monographic series, vol 3. Raven Press, New York, pp 43–57Google Scholar
  129. Scheibel ME, Scheibel AB (1978b) The methods of Golgi. In: Robertson RT (ed) Neuroanatomical research techniques. Academic Press, New York, pp 89–114Google Scholar
  130. Schlaug G, Armstrong E, Schleicher A, Zilles K (1993) Layer V pyramidal cells in the adult human cingulate cortex: a quantitative Golgi-study. Anat Embryol 187:515–522PubMedCrossRefGoogle Scholar
  131. Schmolke C, Künzle H (1997) On the presence of dendrite bundles in the cerebral cortex of the Madagascan lesser hedgehog tenrec and the red-eared pond turtle. Anat Embryol 196:195–213PubMedCrossRefGoogle Scholar
  132. Sherwood CC, Lee PWH, Rivara C-B, Holloway RL, Gilissen EPE, Simmons RMT, 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
  133. 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
  134. Sholl DA (1953) Dendritic organization of the neurons of the visual and motor cortices of the cat. J Anat 87:387–406PubMedGoogle Scholar
  135. Shoshani J, Tassy P (2005) Advances in proboscidean taxonomy and classification, anatomy and physiology, and ecology and behavior. Quat Int 126–128:5–20CrossRefGoogle Scholar
  136. Shoshani J, Kupsky WJ, Marchant GH (2006) Elephant brain part I: gross morphology, functions, comparative anatomy, and evolution. Brain Res Bull 70:124–157PubMedCrossRefGoogle Scholar
  137. Soltis J (2009) Vocal communication in African elephants (Loxodonta africana). Zoo Biol 28:1–18CrossRefGoogle Scholar
  138. Somogyi P, Kisvárday ZF, Martin KAC, Whitteridge D (1983) Synaptic connections of morphologically characterized large basket cells in the striate cortex of cat. Neurosci 10:261–294CrossRefGoogle Scholar
  139. Sukumar R (2003) The living elephants: evolutionary ecology behavior, and conservation. Oxford University Press, New YorkGoogle Scholar
  140. Syring A (1956) Die Verbreitung von Spezialzellen in der Grosshirnrinde verschiedener Säugertiergruppen. Z Zellforsch 45:399–434CrossRefGoogle Scholar
  141. Tower DB (1954) Structural and functional organization of mammalian cerebral cortex; the correlation of neurone density with brain size; cortical neurone density in the fin whale (Balaenoptera physalus L.) with a note on the cortical neurone density in the Indian elephant. J Comp Neurol 101:19–51PubMedCrossRefGoogle Scholar
  142. Tyler CJ, Dunlop SA, Lund RD, Harman AM, Dann JF, Beazley LD (1998) Anatomical comparison of the macaque and marsupial visual cortex: common features that may reflect retention of essential cortical elements. J Comp Neurol 400:449–468PubMedCrossRefGoogle Scholar
  143. Uylings HBM, 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
  144. Valverde F, Facal-Valverde MV (1986) Neocortical layers I and II of the hedgehog (Erinaceus europaeus). I. Intrinsic organization. Anat Embryol 173:413–430PubMedCrossRefGoogle Scholar
  145. Van Brederode JFM, Foehring RC, Spain WJ (2000) Morphological and electrophysiological properties of atypically oriented layer 2 pyramidal cells of the juvenile rat neocortex. Neuroscience 101:851–861PubMedCrossRefGoogle Scholar
  146. Van der Loos H (1965) The “improperly” oriented pyramidal cell in the cerebral cortex and its possible bearing on problems of neuronal growth and cell orientation. Bull Johns Hopkins Hosp 117:228–250Google Scholar
  147. von Economo CF, Koskinas GN (1925) Die cytoarchitektonik der Hirnrinde des erwachsenen Menschen. Springer, BerlinGoogle Scholar
  148. Wang SS-H, Shultz JR, Burish MJ, Harrison KH, Hof PR, Towns LC, Wagers MW, Wyat KD (2008) Functional trade-offs in white matter axonal scaling. J Neurosci 28:4047–4056PubMedCrossRefGoogle Scholar
  149. Wildman DE, Uddin M, Opazo JC, Liu G, Lefort V, Guindon S, Gascuel O, Grossman LI, Romero R, Goodman M (2007) Genomics, biogeography, and the diversification of placental mammals. Proc Natl Acad Sci USA 104:14395–14400PubMedCrossRefGoogle Scholar
  150. Wittenberg GM, Wang SS-H (2007) Evolution and scaling of dendrites. In: Stuart G, Spruston N, Hausser M (eds) Dendrites. Oxford University Press, New York, pp 43–67Google Scholar
  151. Wyss JM, Van Groen T, Sripanidkulchai K (1990) Dendritic bundling in layer I of granular retrosplenial cortex: intracellular labeling and selectivity of innervation. J Comp Neurol 295:33–42PubMedCrossRefGoogle Scholar
  152. Yamamoto T, Samejima A, Oka H (1987) Morphological features of layer V pyramidal neurons in the cat parietal cortex: an intracellular HRP study. J Comp Neurol 265:380–390PubMedCrossRefGoogle Scholar
  153. Zeitsev 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 19:1597–1615CrossRefGoogle Scholar
  154. Zhang K, Sejnowski TJ (2000) A universal scaling law between gray matter and white matter of cerebral cortex. Proc Natl Acad Sci USA 97:5621–5626PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Bob Jacobs
    • 1
  • Jessica Lubs
    • 1
  • Markus Hannan
    • 1
  • Kaeley Anderson
    • 1
  • Camilla Butti
    • 2
  • Chet C. Sherwood
    • 3
  • Patrick R. Hof
    • 2
  • Paul R. Manger
    • 4
  1. 1.Laboratory of Quantitative Neuromorphology, PsychologyThe Colorado CollegeColorado SpringsUSA
  2. 2.Department of Neuroscience and Friedman Brain InstituteMount Sinai School of MedicineNew YorkUSA
  3. 3.Department of AnthropologyThe George Washington UniversityWashingtonUSA
  4. 4.Faculty of Health Sciences, School of Anatomical SciencesUniversity of the WitwatersrandJohannesburgSouth Africa

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