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Brain Structure and Function

, Volume 219, Issue 5, pp 1587–1601 | Cite as

Organization and chemical neuroanatomy of the African elephant (Loxodonta africana) hippocampus

  • Nina Patzke
  • Olatunbosun Olaleye
  • Mark Haagensen
  • Patrick R. Hof
  • Amadi O. Ihunwo
  • Paul R. Manger
Original Article

Abstract

Elephants are thought to possess excellent long-term spatial–temporal and social memory, both memory types being at least in part hippocampus dependent. Although the hippocampus has been extensively studied in common laboratory mammalian species and humans, much less is known about comparative hippocampal neuroanatomy, and specifically that of the elephant. Moreover, the data available regarding hippocampal size of the elephant are inconsistent. The aim of the current study was to re-examine hippocampal size and provide a detailed neuroanatomical description of the hippocampus in the African elephant. In order to examine the hippocampal size the perfusion-fixed brains of three wild-caught adult male African elephants, aged 20–30 years, underwent MRI scanning. For the neuroanatomical description brain sections containing the hippocampus were stained for Nissl, myelin, calbindin, calretinin, parvalbumin and doublecortin. This study demonstrates that the elephant hippocampus is not unduly enlarged, nor specifically unusual in its internal morphology. The elephant hippocampus has a volume of 10.84 ± 0.33 cm³ and is slightly larger than the human hippocampus (10.23 cm3). Histological analysis revealed the typical trilaminated architecture of the dentate gyrus (DG) and the cornu ammonis (CA), although the molecular layer of the dentate gyrus appears to have supernumerary sublaminae compared to other mammals. The three main architectonic fields of the cornu ammonis (CA1, CA2, and CA3) could be clearly distinguished. Doublecortin immunostaining revealed the presence of adult neurogenesis in the elephant hippocampus. Thus, the elephant exhibits, for the most part, what might be considered a typically mammalian hippocampus in terms of both size and architecture.

Keywords

Adult hippocampal neurogenesis Calcium-binding proteins Hippocampus Doublecortin Memory Proboscidean 

Notes

Acknowledgments

This study was supported by a grant from the South African National Research Foundation to PRM (Grant number: FA2005033100004), the Swiss-South African Joint Research Programme to AOI and PRM, a fellowship within the Postdoc-Programme of the German Academic Exchange Service, DAAD (NP), and the James S. McDonnell Foundation (Grant 22002078 to PRH). We would 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.

Conflict of interest

The authors have no conflict of interest.

References

  1. Baimbridge KG, Celio MR, Rogers JH (1992) Calcium-binding proteins in the nervous system. Trends Neurosci 15:303–308PubMedCrossRefGoogle Scholar
  2. Barinka F, Druga R (2010) Calretinin expression in the mammalian neocortex: a review. Physiol Rev 59:665–677Google Scholar
  3. Bartkowska K, Turlejski K, Grabiec M, Ghazaryan A, Yavruoyan E, Djavadian RL (2010) Adult neurogenesis in the hedgehog (Erinaceus concolor) and mole (Talpa europaea). Brain Behav Evol 76:128–143PubMedCrossRefGoogle Scholar
  4. Bates LA, Sayialel KN, Njiraini N, Poole JH, Moss C, Byrne RW (2008) African elephants have expectations about the locations of out-of-sight family members. Biol Lett 4:34–36PubMedCentralPubMedCrossRefGoogle Scholar
  5. Blasco-Ibáñez JM, Freund TF (1997) Distribution, ultrastructure, and connectivity of calretinin-immunoreactive mossy cells of the mouse dentate gyrus. Hippocampus 7:307–320PubMedCrossRefGoogle Scholar
  6. Bonfanti L, Rossi F, Zupanc GK (2011) Towards a comparative understanding of adult neurogenesis. Eur J Neurosci 34:845–846PubMedCrossRefGoogle Scholar
  7. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG (2003) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1–10PubMedCrossRefGoogle Scholar
  8. Byrne RW, Bates LA, Moss CJ (2009) Elephant cognition in primate perspective. Comp Cog Behav Rev 4:1–15Google Scholar
  9. Caillard O, Moreno H, Schwaller B, Llano I, Celio MR, Marty A (2000) Role of the calcium-binding protein parvalbumin in short-term synaptic plasticity. Proc Natl Acad Sci USA 97:13372–13377PubMedCentralPubMedCrossRefGoogle Scholar
  10. Deller T, Adelmann G, Nitsch R, Frotscher M (1996) The alvear pathway of the rat hippocampus. Cell Tissue Res 286:293–303PubMedCrossRefGoogle Scholar
  11. Faas GC, Schwaller B, Vergara JL, Mody I (2007) Resolving the fast kinetics of cooperative binding: Ca2+ buffering by calretinin. PLoS Biol 5:e311PubMedCentralPubMedCrossRefGoogle Scholar
  12. Foley CAH, Pettorelli N, Foley L (2008) Severe drought and calf survival in elephants. Biol Lett 4:541–544PubMedCentralPubMedCrossRefGoogle Scholar
  13. Fujise N, Liu Y, Hori N, Kosaka T (1998) Distribution of calretinin immunoreactivity in the mouse dentate gyrus: II. Mossy cells, with special reference to their dorsoventral difference in calretinin immunoreactivity. Neuroscience 82:181–200PubMedCrossRefGoogle Scholar
  14. Gallyas F (1979) Silver staining of myelin by means of physical development. Neurol Res 1:203–209PubMedGoogle Scholar
  15. Gould E (2007) How widespread is adult neurogenesis in mammals? Nat Rev Neurosci 8:481–488PubMedCrossRefGoogle Scholar
  16. 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
  17. Gulyás AI, Miettinen R, Jacobowitz DM, Freund TF (1992) Calretinin is present in non-pyramidal cells of the rat hippocampus-I. A new type of neuron specifically associated with the mossy fiber system. Neuroscience 48:1–27PubMedCrossRefGoogle Scholar
  18. Hakeem AY, Hof PR, Sherwood CC, Switzer RC, Rasmussen LE, Allman JM (2005) Brain of the African elephant (Loxodonta africana): neuroanatomy from magnetic resonance images. Anat Rec 287:1117–1127CrossRefGoogle Scholar
  19. Hart BL, Hart LA, Pinter-Wollman N (2008) Large brains and cognition: where do elephants fit in? Neurosci Biobehav Rev 32:86–98PubMedCrossRefGoogle Scholar
  20. Haug H (1970) Der makroskopische Aufbau des Grosshirns; Qualitative und quantitative Untersuchungen an den Gehirnen des Menschen, der Delphinoideae und des Elefanten. Ergebn Anat Entwicklungesch 43:3–70Google Scholar
  21. Healy SD, de Kort SR, Clayton NS (2005) The hippocampus spatial memory and food hoarding: a puzzle revisited. Trends Ecol Evol 20:17–22PubMedCrossRefGoogle Scholar
  22. Hof PR, Rosenthal RE, Fiskum G (1996) Distribution of neurofilament protein and calcium-binding proteins parvalbumin, calbindin, and calretinin in the canine hippocampus. J Chem Neuroanat 11:1–12PubMedCrossRefGoogle Scholar
  23. Hof PR, Glezer II, Conde 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
  24. Katsumaru H, Kosaka T, Heizmann CW, Hama K (1988) Immunocytochemical study of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat hippocampus. Exp Brain Res 72:347–362PubMedGoogle Scholar
  25. Kempermann G (2012) New neurons for ‘survival of the fittest’. Nat Rev Neurosci 13:727–736PubMedGoogle Scholar
  26. Krzywkowski P, Jacobowitz DM, Lamour Y (1995) Calretinin-containing pathways in the rat forebrain. Brain Res 705:273–294PubMedCrossRefGoogle Scholar
  27. 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 1st International Congress of “La Terra degli Elefanti”, The World of Elephants. Consiglio Nazionale delle Ricerche, Roma, pp 643–647Google Scholar
  28. Lindsey BW, Tropepe V (2006) A comparative framework for understanding the biological principles of adult neurogenesis. Prog Neurobiol 80:281–307PubMedCrossRefGoogle Scholar
  29. Liu Y, Fujise N, Kosaka T (1996) Distribution of calretinin immunoreactivity in the mouse dentate gyrus. I. General description. Exp Brain Res 108:389–403PubMedCrossRefGoogle Scholar
  30. Lucas JR, Brodin A, de Kort SR, Clayton NS (2004) Does hippocampal size correlate with degree of caching specialization? Proc Biol Sci 271:2423–2429PubMedCentralPubMedCrossRefGoogle Scholar
  31. Manger PR, Pillay P, Maseko BC, Bhagwandin A, Gravett N, Moon D, Jillani NE, Hemingway J (2009) Acquisition of the brain of the African elephant (Loxodonta africana): perfusion-fixation and dissection. J Neurosci Methods 179:16–21PubMedCrossRefGoogle Scholar
  32. Maseko BC, Spocter MA, Haagensen M, Manger PR (2011) Volumetric analysis of the African elephant ventricular system. Anat Rec 298:1412–1417CrossRefGoogle Scholar
  33. Maseko BC, Jacobs B, Spocter MA, Sherwood CC, Hof PR, Manger PR (2013) Qualitative and quantitative aspects of the microanatomy of the African elephant cerebellar cortex. Brain Behav Evol 81:40–55PubMedCrossRefGoogle Scholar
  34. Maskey D, Pradhan J, Oh CK, Kim MJ (2012) Changes in the distribution of calbindin D28-k, parvalbumin, and calretinin in the hippocampus of the circling mouse. Brain Res 1437:58–68PubMedCrossRefGoogle Scholar
  35. McComb K, Moss C, Sayailel S, Baker L (2000) Unusually extensive networks of vocal recognition in African elephants. Anim Behav 59:1103–1109PubMedCrossRefGoogle Scholar
  36. McComb K, Reby D, Baker L, Moss C, Sayailel S (2003) Longdistance communication of acoustic cues to social identity in African elephants. Anim Behav 65:317–329CrossRefGoogle Scholar
  37. Ming GL, Song H (2011) Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron 70:687–702PubMedCentralPubMedCrossRefGoogle Scholar
  38. Morris R (2007) Theories of hippocampal function. In: Anderson P, Morris R, Amaral D, Bliss T, O’Keefe J (eds) The Hippocampus Book. Oxford Press, New York, pp 581–715Google Scholar
  39. Ngwenya A, Patzke N, Ihunwo AO, Manger PR (2011) Organisation and chemical neuroanatomy of the African elephant (Loxodonta africana) olfactory bulb. Brain Struct Funct 216:403–416PubMedCrossRefGoogle Scholar
  40. Nitsch R, Leranth C (1993) Calretinin immunoreactivity in the monkey hippocampal formation-II. Intrinsic GABAergic and hypothalamic non-GABAergic systems: an experimental tracing and co-existence study. Neuroscience 55:797–812PubMedCrossRefGoogle Scholar
  41. Nitsch R, Ohm TG (1995) Calretinin immunoreactive structures in the human hippocampal formation. J Comp Neurol 360:475–487PubMedCrossRefGoogle Scholar
  42. Poole JH, Payne K, Langbauer WR, Moss CJ (1988) The social contexts of some very low frequency calls of African elephants. Behav Ecol Sociobiol 22:385–392CrossRefGoogle Scholar
  43. Quiroga RQ, Reddy L, Kreiman G, Koch C, Fried I (2005) Invariant visual representation by single neurons in the human brain. Nature 435:1102–1107PubMedCrossRefGoogle Scholar
  44. Rao MS, Shetty AK (2004) Efficacy of doublecortin as a marker to analyse the absolute number and dendritic growth of newly generated neurons in the adult dentate gyrus. Eur J Neurosci 19:234–246PubMedCrossRefGoogle Scholar
  45. Reep RL, Finlay BL, Darlington RB (2007) The limbic system in mammalian brain evolution. Brain Behav Evol 70:57–70PubMedCrossRefGoogle Scholar
  46. Rosset A, Spadola L, Ratib O (2004) OsiriX: an open-source software for navigating in multidimensional DICOM images. J Digit Imaging 17:205–216PubMedCentralPubMedCrossRefGoogle Scholar
  47. Salwiczek LH, Watanabe A, Clayton NS (2010) Ten years of research into avian models of episodic-like memory and its implications for developmental and comparative cognition. Behav Brain Res 215:221–234PubMedCrossRefGoogle Scholar
  48. Seress L, Gulyás AI, Freund TF (1991) Parvalbumin- and calbindin D28k-immunoreactive neurons in the hippocampal formation of the macaque monkey. J Comp Neurol 313:162–177PubMedCrossRefGoogle Scholar
  49. Seress L, Abrahám H, Czéh B, Fuchs E, Léránth C (2008) Calretinin expression in hilar mossy cells of the hippocampal dentate gyrus of nonhuman primates and humans. Hippocampus 18:425–434PubMedCrossRefGoogle Scholar
  50. 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
  51. Skinner JD, Chimimba CT (2005) The Mammals of the Southern African Subregion, 3rd edn. Cambridge University Press, Cape TownCrossRefGoogle Scholar
  52. Sloviter RS (1989) Calcium-binding protein (calbindin-D28k) and parvalbumin immunocytochemistry: localization in the rat hippocampus with specific reference to the selective vulnerability of hippocampal neurons to seizure activity. J Comp Neurol 280:183–196PubMedCrossRefGoogle Scholar
  53. Sloviter RS, Sollas AL, Barbaro NM, Laxer KD (1991) Calcium-binding protein (calbindin-D28K) and parvalbumin immunocytochemistry in the normal and epileptic human hippocampus. J Comp Neurol 308:381–396PubMedCrossRefGoogle Scholar
  54. Stephan H, Frahm H, Baron G (1981) New and revised data on volumes of brain structures in insectivores and primates. Folia Primatol 35:1–29PubMedCrossRefGoogle Scholar
  55. Vidya TNC, Sukumar R (2005) Social and reproductive behaviour in elephants. Curr Sci 89:1200–1207Google Scholar
  56. von Heimendahl M, Rao RP, Brecht M (2012) Weak and nondiscriminative responses to conspecifics in the rat hippocampus. J Neurosci 32:2129–2141CrossRefGoogle Scholar
  57. Watson C, Andermann F, Gloor P, Jones-Gotman M, Peters T, Evans A, Olivier A, Melanson D, Leroux G (1992) Anatomic basis of amygdaloid and hippocampal volume measurement by magnetic resonance imaging. Neurology 42:1743–1750PubMedCrossRefGoogle Scholar
  58. Western D, Lindsay WK (1984) Seasonal herd dynamics of a savanna elephant population. Afr J Ecol 22:229–244CrossRefGoogle Scholar
  59. Witter MP (2007) The perforant path: projections from the entorhinal cortex to the dentate gyrus. Prog Brain Res 163:43–61PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Nina Patzke
    • 1
  • Olatunbosun Olaleye
    • 1
  • Mark Haagensen
    • 2
  • Patrick R. Hof
    • 3
  • Amadi O. Ihunwo
    • 1
  • Paul R. Manger
    • 1
  1. 1.School of Anatomical Sciences, Faculty of Health SciencesUniversity of the WitwatersrandJohannesburgSouth Africa
  2. 2.Department of Radiology, Donald Gordon Medical CentreUniversity of the WitwatersrandJohannesburgSouth Africa
  3. 3.Fishberg Department of Neuroscience and Friedman Brain InstituteIcahn School of Medicine at Mount SinaiNew YorkUSA

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