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Neuronal morphology in the African elephant (Loxodonta africana) neocortex


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.

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  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 19:2131–2144

  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 186:209–214

  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 148:522–534

  4. Barasa A (1960) Forma, grandezza e densità dei neuroni della corteccia cerebrale in mammiferi di grandezza corporea differente. Z Zellforsch 53:69–89

  5. Barasa A, Shochatovitz A (1961) Grandezza e densità della cellule nervose della corteccia cerebrale de Elephas indicus. Rendiconti Accad Naz Lincei 30:246–249

  6. Barbas H (1995) Anatomic basis of cognitive-emotional interactions in the primate prefrontal cortex. Neurosci Biobehav Rev 19:499–510

  7. Bartesaghi R, Severo S, Guidi S (2003) Effects of early environment on pyramidal neuron morphology in field CA1 of the guinea-pig. Neuroscience 116:715–732

  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 17:1938–1942

  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 4:34–36

  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 15:204–225

  11. Bates LA, Poole JH, Byrne RW (2008b) Elephant cognition. Curr Biol 18:R544–R546

  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 16:990–1001

  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)

  14. Bok ST (1959) Histonomy of the cerebral cortex. Elsevier, Amsterdam

  15. Bota M, Swanson LW (2007) The neuron classification problem. Brain Res Rev 56:79–88

  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 172:103–119

  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 25:93–139

  18. Brown KM, Gillette TA, Ascoli GA (2008) Quantifying neuronal size: summing up trees and splitting the branch difference. Semin Cell Dev Biol 19:485–493

  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 3:415–430

  20. Butti C, Hof PR (2010) The insular cortex: a comparative perspective. Brain Struct Func 214:477–493

  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 515:243–259

  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 5:175–180

  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 54:219–227

  24. de Crinis M (1934) Über die Spezialzellen in der menschlichen Grosshirnrinde. J Psych Neurol. 45:439–449

  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 296:159–172

  26. de Ruiter JP (1983) The influence of post-mortem fixation delay on the reliability of the Golgi silver impregnation. Brain Res 266:143–147

  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 14:1–19

  28. DeFelipe J, Alonso-Nanclares L, Arellano JI (2002) Microstructure of the neocortex: comparative aspects. J Neurocytol 31:299–316

  29. Druga R (2009) Neocortical inhibitory system. Folia Biol (Prague) 55:201–217

  30. Elston GN (2003) Cortex, cognition and the cell: new insights into the pyramidal neuron and prefrontal function. Cereb Cortex 13:1124–1138

  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 191–242

  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 7:432–452

  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 9:127–131

  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 8:278–294

  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 6:807–813

  36. Ferrer I (1986) Golgi study of the isocortex in an insectivore: the common European mole (Talpa europaea). Brain Behav Evol 29:105–114

  37. Ferrer I (1987) The basic structure of the neocortex in insectivorous bats (Miniopterus sthreibersi and Pipistrellus pipistrellus). J Hirnforsch 28:237–243

  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) 178:161–173

  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 145:217–234

  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 146:87–104

  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 152:71–82

  42. Fitzpatrick DC, Henson OW (1994) Cell types in the mustached bat auditory cortex. Brain Behav Evol 43:79–91

  43. Fleischhauer K (1974) On different patterns of dendritic bundling in the cerebral cortex of the cat. Z Anat Entwickl-Gesch 143:115–126

  44. Fleischhauer K, Petsche H, Wittkowski W (1972) Vertical bundles of dendrites in the neocortex. Anat Embryol 136:213–223

  45. Foxe JJ, Simpson GV (2002) Flow of activation from V1 to frontal cortex in humans. Exp Brain Res 142:139–150

  46. Garey LJ, Winkelmann E, Brauer K (1985) Golgi and Nissl studies of the visual cortex of the bottlenose dolphin. J Comp Neurol 240:305–321

  47. Garstang M (2004) Long-distance, low-frequency elephant communication. J Comp Physiol A 190:791–805

  48. Geisler HC, Ijkema-Paassen J, Westerga J, Gramsbergen A (2000) Vestibular deprivation and the development of dendritic bundles in the rat. Neural Plast 7:193–203

  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 30:683–691

  50. Gheerbrant E, Tassy P (2009) L’origine et l’évolution des elephants. C R Palevol 8:281–294

  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 24:401–427

  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. 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 106:20824–20829

  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 88–92

  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 38:57–74

  56. Group Petilla Interneuron Nomenclature (2008) Petilla terminology: nomenclature of features of GABAergic interneurons of the cerebral cortex. Nat Rev Neurosci 9:557–568

  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:1117–1127

  58. Hakeem AY, Sherwood CC, Bonar CJ, Butti C, Hof PR, Allman JM (2009) Von Economo neurons in the elephant brain. Anat Rec 292:242–248

  59. Harrison KH, Hof PR, Wang SS-H (2002) Scaling laws in the mammalian neocortex: does form provide blues to function? J Neurocytol 31:289–298

  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 491–497

  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)

  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 62:839–847

  63. Hart BL, Hart LA, Pinter-Wollman N (2008) Large brains and cognition: where do elephants fit in? Neurosci Biobehav Rev 32:86–98

  64. Hassiotis M, Ashwell KWS (2003) Neuronal classes in the isocortex of a monotreme, the Australian echidna (Tachyglossus aculeatus). Brain Behav Evol 61:6–27

  65. Hassiotis M, Paxinos G, Ashwell KWS (2003) The anatomy of the cerebral cortex of the echidna (Tachyglossus aculeatus). Comp Biochem Physiol Part A 136:827–850

  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 482:94–122

  67. Haug H (1970) Die makrospkoschie Aufbau des Großhirns: qualitative und quantitative Untersuchungen an den Gehirnen des Menschen der Delphinoideae und des Elefanten. Springer, Berlin

  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 180:126–142

  69. Hof PR, Sherwood CC (2005) Morphomolecular neuronal phenotypes in the neocortex reflect phylogenetic relationships among certain mammalian orders. Anat Rec 287A:1153–1163

  70. Hof PR, Van der Gucht E (2007) Structure of the cerebral cortex of the humpback whale, Megaptera novaeangliae (Cetacea, Mysticeti, Balaeopteridae). Anat Rec 290:1–31

  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 146:91–95

  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 11:81–98

  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 16:77–116

  74. Hof PR, Chanis R, Marino L (2005) Cortical complexity in cetacean brains. Anat Rec 287A:1142–1152

  75. Hoffmann JN, Montag AG, Dominy NJ (2004) Meissner corpuscles and somatosensory acuity: the prehensile appendages of primates and elephants. Anat Rec 281A:1138–1147

  76. Hofman MA (1982) Encephalization in mammals in relation to the size of the cerebral cortex. Brain Behav Evol 20:84–96

  77. Horner CH, Arbuthnott E (1991) Methods of estimation of spine density—are spines evenly distributed throughout the dendritic field? J Anat 177:179–184

  78. Hou ZC, Romero R, Wildman DE (2009) Phylogeny of the Ferungulata (Mammalia: Laurasiatheria) as determined from phylogenomic data. Mol Phylogenet Evol 52:660–664

  79. Innocenti GM, Vercelli A (2010) Dendritic bundles, minicolumns, columns, and cortical output units. Front Neuroanat 4:1–7

  80. Jacobs B, Scheibel AB (1993) A quantitative dendritic analysis of Wernicke’s area in humans I. Lifespan changes. J Comp Neurol 327:83–96

  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 111–131

  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 327:97–111

  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 386:661–680

  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 11:558–571

  85. Jones EG (1984) Neurogliaform or spiderweb cells. In: Peters A, Jones EG (eds) Cerebral cortex. Plenum Press, New York and London, pp 409–418

  86. Juba A (1934) Über seltenere Ganglienzellformen der Grosshirnrinde. Z Zellforsch 21:441–447

  87. Kaiserman-Abramof IR, Peters A (1972) Some aspects of the morphology of Betz cells in the cerebral cortex of the cat. Brain Res 43:527–546

  88. Kawaguchi Y (1995) Physiological subgroups of nonpyramidal cells with specific morphological characteristics in layer II/III of rat frontal cortex. J Neurosci 15:2638–2665

  89. Kesarev VS (1975) Homologization of the cerebral neocortex in cetaceans. Arkh Anat Gistol Embriol 68:5–13

  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 113:793–812

  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 643–647

  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 20:5300–5311

  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 13:1051–1063

  94. Lund JS, Lewis DA (1993) Local circuit neurons of developing mature macaque prefrontal cortex: Golgi and immunocytochemical characteristics. J Comp Neurol 328:282–312

  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 182:143–156

  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 10:153–166

  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 2:1–7

  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 179:16–21

  99. Manger PR, Hemingway J, Haagensen M, Gilissen E (2010) Cross-sectional area of the elephant corpus callosum: comparison to other eutherian mammals. Neuroscience 167:815–824

  100. Markowitz H, Schmidt M, Nadal L, Squire L (1975) Do elephants ever forget? J Appl Behav Anal 8:333–335

  101. Masland RH (2004) Neuronal cell types. Curr Biol 14:R497–R500

  102. McComb K, Moss C, Sayialel S, Baker L (2000) Unusually extensive networks of vocal recognition in African elephants. Anim Behav 59:103–1109

  103. McComb K, Moss C, Durant SM, Baker L, Sayialel S (2001) Matriarchs as repositories of social knowledge in African elephants. Science 292:491–494

  104. Mendizabal-Zubiaga JL, Reblet C, Bueno-Lopez JL (2007) The underside of the cerebral cortex: layer V/VI spiny inverted neurons. J Anat 211:223–236

  105. Meyer G (1987) Forms and spatial arrangement of neurons in the primary motor cortex of man. J Comp Neurol 262:402–428

  106. Miller MW (1988) Maturation of rat visual cortex: IV. The generation, migration, morphogenesis and connectivity of atypically oriented pyramidal cells. J Comp Neurol 274:387–405

  107. Morest DK, Morest RR (2005) Perfusion-fixation of the brain with chrome-osmium solutions for the rapid Golgi method. Am J Anat 118:811–831

  108. Mountcastle VB (1997) The columnar organization of the neocortex. Brain 120:701–722

  109. Ngowyang G (1932) Beschreibung einer Art von Specialzellen in der Inselrinde. J Psychol Neurol 44:671–674

  110. Ngowyang G (1936) Neuere Befunde über die Gabelzellen. Z Zellforsch 25:236–239

  111. Nimchinsky EA, Vogt BA, Morrison JH, Hof PR (1995) Spindle neurons of the human anterior cingulate cortex. J Comp Neurol 355:27–37

  112. Ong WY, Garey LJ (1990) Neuronal architecture of the human temporal cortex. Anat Embryol 181:351–364

  113. Parnavelas JG, Lieberman AR, Webster KE (1977) Organization of neurons in the visual cortex, area 17, of the rat. J Anat 124:305–322

  114. Peters A, Regidor J (1981) A reassessment of the forms of nonpyramidal neurons in area 17 of cat visual cortex. J Comp Neurol 203:685–716

  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 39:175–188

  116. Plotnik JM, de Waal FBM, Reiss D (2006) Self-recognition in an Asian elephant. Proc Natl Acad Sci USA 103:17053–17057

  117. Poole JH (1999) Signals and assessment in African elephants: evidence from playback experiments. Anim Behav 58:185–193

  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 69–98

  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 434:455–456

  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 97:1030–1039

  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 16:49–56

  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 23–54

  123. Ramón y Cajal S (1922) Studien über die Sehrinde der Katze. J Psychol Neurol 29:161–181

  124. Roney KJ, Scheibel AB, Shaw GL (1979) Dendritic bundles: survey of anatomical experiments and physiological theories. Brain Res Rev 1:225–271

  125. Roth G, Dicke U (2005) Evolution of the brain and intelligence. Trends Cogn Sci 9:250–257

  126. Sanides F, Sanides D (1972) The “extraverted neurons” of the mammalian cerebral cortex. Z Anat Entwickl-Gesch 136:272–293

  127. Scheibel ME, Scheibel AB (1975) Dendrite bundles, central programs and the olfactory bulb. Brain Res 95:407–421

  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 43–57

  129. Scheibel ME, Scheibel AB (1978b) The methods of Golgi. In: Robertson RT (ed) Neuroanatomical research techniques. Academic Press, New York, pp 89–114

  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 187:515–522

  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 196:195–213

  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 61:28–44

  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 213:301–328

  134. Sholl DA (1953) Dendritic organization of the neurons of the visual and motor cortices of the cat. J Anat 87:387–406

  135. Shoshani J, Tassy P (2005) Advances in proboscidean taxonomy and classification, anatomy and physiology, and ecology and behavior. Quat Int 126–128:5–20

  136. Shoshani J, Kupsky WJ, Marchant GH (2006) Elephant brain part I: gross morphology, functions, comparative anatomy, and evolution. Brain Res Bull 70:124–157

  137. Soltis J (2009) Vocal communication in African elephants (Loxodonta africana). Zoo Biol 28:1–18

  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 10:261–294

  139. Sukumar R (2003) The living elephants: evolutionary ecology behavior, and conservation. Oxford University Press, New York

  140. Syring A (1956) Die Verbreitung von Spezialzellen in der Grosshirnrinde verschiedener Säugertiergruppen. Z Zellforsch 45:399–434

  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 101:19–51

  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 400:449–468

  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 18:127–151

  144. Valverde F, Facal-Valverde MV (1986) Neocortical layers I and II of the hedgehog (Erinaceus europaeus). I. Intrinsic organization. Anat Embryol 173:413–430

  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 101:851–861

  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 117:228–250

  147. von Economo CF, Koskinas GN (1925) Die cytoarchitektonik der Hirnrinde des erwachsenen Menschen. Springer, Berlin

  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 28:4047–4056

  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 104:14395–14400

  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 43–67

  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 295:33–42

  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 265:380–390

  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 19:1597–1615

  154. Zhang K, Sejnowski TJ (2000) A universal scaling law between gray matter and white matter of cerebral cortex. Proc Natl Acad Sci USA 97:5621–5626

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Partial support for this work was provided by the Thomas M. McKee Professorship in the Natural Sciences (B.J.), The Colorado College’s divisional research funds (B.J.), the James S. McDonnell Foundation (grant 22002078, to C.C.S., P.R.H.), and the South African National Research Foundation (P.R.M.; FA2005033100004). We would also like to thank Dr. Hilary Madzikanda of the Zimbabwe Parks and Wildlife Management Authority, and Dr. Bruce Fivaz and the team at the Malilangwe Trust, Zimbabwe.

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Correspondence to Bob Jacobs.

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Jacobs, B., Lubs, J., Hannan, M. et al. Neuronal morphology in the African elephant (Loxodonta africana) neocortex. Brain Struct Funct 215, 273–298 (2011). https://doi.org/10.1007/s00429-010-0288-3

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  • Dendrite
  • Morphometry
  • Dendritic spine
  • Golgi method
  • Brain evolution