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Organisation and chemical neuroanatomy of the African elephant (Loxodonta africana) olfactory bulb

Brain Structure and Function volume 216, pages 403–416 (2011)Cite this article

Abstract

The olfactory system of mammals can be divided into a main and accessory olfactory system with initial processing for each system occurring in the olfactory bulb. The main and accessory olfactory bulbs have similar structural features, even though they appear to be functionally independent. In mammals the main olfactory bulb (MOB) is also one of two established sites of lifelong generation of new cells. The present study describes the histological and immunohistochemical neuroanatomy of the olfactory bulb of the African elephant (Loxodonta africana). The morphology of MOB of the elephant does not differ significantly from that described in other mammals; however, it lacks the internal plexiform layer. In addition, the glomeruli of the glomerular layer are organised in 2–4 “honey-combed” layers, a feature not commonly observed. The cell types and structures revealed with immunohistochemical stains (parvalbumin, calbindin, calretinin, tyrosine hydroxylase, orexin-A, glial fibrillary acidic protein) were similar to other mammals. Neurogenesis was examined using the neurogenic marker doublecortin. Migration of newly generated cells was observed in most layers of the MOB. No accessory olfactory bulb (AOB) was observed. Based on the general anatomy and the immunohistochemical observations, it is evident that the morphology of the African elephant MOB is, for the most part, similar to that of all mammals, although very large in absolute size.

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References

  • Ashwell KWS (2006) Chemoarchitecture of the monotreme olfactory bulb. Brain Behav Evol 67:69–84

    PubMed  Article  Google Scholar 

  • Bailey MS, Shipley MT (1993) Astrocyte subtypes in the rat olfactory bulb: morphological heterogeneity and differential laminar distribution. J Comp Neurol 328:501–526

    PubMed  Article  CAS  Google Scholar 

  • Baker H (1986) Substance P and tyrosine hydroxylase are localized in different neurons of the hamster main olfactory bulb. Exp Brain Res 65:245–249

    PubMed  Article  CAS  Google Scholar 

  • Bédard A, Parent A (2004) Evidence of newly generated neurons in the human olfactory bulb. Brain Res Dev Brain Res 151:159–168

    PubMed  Article  Google Scholar 

  • Briñón JG, Alonso JR, Arélavo R, Garcìa-Ojeda E, Lara J, Aijón (1992) Calbindin D-28k-positive neurons in the rat olfactory bulb. An immunohistochemical study. Cell Tissue Res 269:289–297

    PubMed  Article  Google Scholar 

  • Briñón JG, Alonso JR, Arélavo R, Garcìa-Ojeda E, Crespo C, Aijón J (1997) Calretinin- and parvalbumin-immunoreactive neurons in the rat main olfactory bulb do not express NADPH-diaphorase activity. J Chem Neuroanat 13:253–264

    PubMed  Article  Google Scholar 

  • Caillol M, Aïoun J, Baly C, Persuy M, Salesse R (2003) Localization of orexins and their receptors in the rat olfactory system: possible modulation of olfactory perception by a neuropeptide synthesized centrally or locally. Brain Res 960:48–61

    PubMed  Article  CAS  Google Scholar 

  • Chao TI, Kasa P, Wolff JR (1997) Distribution of astroglia in the glomeruli of the rat main olfactory bulb: exclusion from the sensory subcompartment of neuropil. J Comp Neurol 388:191–210

    PubMed  Article  CAS  Google Scholar 

  • Cohen-Tannoudjii J, Lavenet C, Locatelli A, Tillet Y, Signoret JP (1989) Non-involvement of the accessory olfactory system in the LH response of anoestrous ewes to male odor. J Reprod Fertil 86:135–144

    Article  Google Scholar 

  • Davis BJ, Macrides F (1983) Tyrosine hyroxylase immunoreactive neurons and fibers in the olfactory system of the hamster. J Comp Neurol 214:427–440

    Article  Google Scholar 

  • Dorries KM, Adkins-Regan E, Halpern BP (1997) Sensitivity and behavioral responses to the pheromone androstenone are not mediated by the vomeronasal organ in the pig. Brain Behav Evol 49:53–62

    PubMed  Article  CAS  Google Scholar 

  • Eisthen HL (1997) Evolution of vertebrate olfactory systems. Brain Behav Evol 50:222–233

    PubMed  Article  CAS  Google Scholar 

  • Gaeth AP, Short RV, Renfree MB (1999) The developing renal, reproductive, and reproductive respiratory systems of the African elephant suggest an aquatic ancestry. Proc Natl Acad Sci USA 96:5555–5558

    PubMed  Article  CAS  Google Scholar 

  • Göbbel L, Fischer MS, Smith TD, Wible JR, Bhatnagar KP (2004) The vomeronasal organ and associated structures in the fetal African elephant, Loxodonta africana (Proboscidea, Elephantidae). Acta Zool 85:41–53

    Article  Google Scholar 

  • Hakeem AY, Hof PR, Sherwood CC, Switzer RC, Rasmussen ME, Allman JM (2005) Brain of the African elephant (Loxodonta africana): neuroanatomy from magnetic resonance images. Anat Rec A 287:1117–1127

    Google Scholar 

  • Hálász N, Shepherd GM (1983) Neurochemistry of the vertebrate olfactory bulb. Neuroscience 10:579–619

    PubMed  Article  Google Scholar 

  • Halpern M (1987) The organization and function of the vomeronasal system. Ann Rev Neurosci 10:325–362

    PubMed  Article  CAS  Google Scholar 

  • Johansson E (2009) Food preference in African elephants (Loxodonta africana) and the impact of bomas in the vicinity of and in Maasai Mara national reserve. Dissertation, Swedish University of Agricultural Sciences

  • Johnson EW, Rasmussen LEL (2002) Morphological characteristics of the vomeronasal organ of the newborn Asian elephant (Elephas maximus). Anat Rec 267:252–259

    PubMed  Article  Google Scholar 

  • Kálmán M, Hajós F (1989) Distribution of glial fibrillary acidic protein (GFAP)-immunoreactive astrocytes in the rat brain. Exp Brain Res 78:147–163

    PubMed  Article  Google Scholar 

  • Kosaka T, Kosaka K (2008) Heterogeneity of parvalbumin-containing neurons in the mouse main olfactory bulb, with special reference to short axon cells and βIV-spectrin positive dendritic segments. Neurosci Res 60:56–72

    PubMed  Article  CAS  Google Scholar 

  • Kosaka T, Kosaka K (2009) Olfactory bulb anatomy. In: Squire LR (ed) Encyclopedia of neuroscience, 7th edn. Oxford University press, Oxford, pp 59–69

    Chapter  Google Scholar 

  • Kosaka T, Kosaka K (2010) Heterogeneity of calbindin-containing neurons in the mouse main olfactory bulb. Neurosci Res 67:275–292

    PubMed  Article  CAS  Google Scholar 

  • Kosaka K, Heizmann CW, Kosaka T (1994) Calcium-binding protein parvalbumin-immunoreactive neurons in the rat olfactory bulb. 1. Distribution and structural features in the adult rat. Exp Brain Res 99:191–204

    PubMed  Article  CAS  Google Scholar 

  • Kratskin IL, Belluzzi O (2003) Anatomy and neurochemistry of the olfactory bulb. In: Doty RL (ed) Handbook of olfaction and gustation, 2nd edn. Marcel Dekker, New York, pp 235–276

    Google Scholar 

  • Lledo P, Alonso M, Grubb S (2006) Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci 7:179–193

    PubMed  Article  CAS  Google Scholar 

  • MacKay-Sim A, Duvall D, Graves BM (1985) The West Indian manatee (Trichechus manatus) lacks a vomeronasal organ. Brain Behav Evol 27:186–194

    PubMed  Article  CAS  Google Scholar 

  • Macrides F, Schneider SP (1982) Laminar organization of mitral and tufted cells in the main olfactory bulb of the hamster. J Comp Neurol 208:419–430

    PubMed  Article  CAS  Google Scholar 

  • Manger PR, Pillay P, Maseko BC, Bhagwandin A, Gravett N, Moon D, Jillani N, Hemingway J (2009) Acquisition of brains from the African elephant (Loxodonta africana): perfusion-fixation and dissection. J Neurosci Methods 179:16–21

    PubMed  Article  Google Scholar 

  • Marschner C (1970) Qualitative und quantitative untersuchungen am bulbus olfactorius des elefanten im vergleich mit dem des menschen und des schweines. Acta Anat 75:578–595

    PubMed  Article  CAS  Google Scholar 

  • Meisami E, Bhatnagar KP (1998) Structure and diversity in the mammalian accessory olfactory bulb. Microsc Res Tech 43:476–499

    PubMed  Article  CAS  Google Scholar 

  • Parrish-Aungst S, Shipley MT, Erdelyi E, Szabo G, Puche AC (2007) Quantitative analysis of the neuronal diversity in the mouse olfactory bulb. J Comp Neurol 501:825–836

    PubMed  Article  CAS  Google Scholar 

  • Peretto P, Merighi A, Fasolo A, Bonfanti L (1997) Glial tubes in the rostral migratory stream of the adult rat. Brain Res Bull 42(1):9–21

    PubMed  Article  CAS  Google Scholar 

  • Rasmussen LEL, Hultgren B (1990) Gross and microscopic anatomy of the vomeronasal organ in the Asian elephant, Elephas maximus. In: McDonald D, Muller-Schwarze D, Natynczuk SE (eds) Chemical signals in vertebrates, 5th edn. Oxford University press, Oxford, pp 154–161

  • Rasmussen LEL, Lazar J, Greenwood DR (2003) Olfactory adventures of elephantine pheromones. Biochem Soc Trans 31:137–141

    PubMed  Article  CAS  Google Scholar 

  • Santiapillai C, Read B (2010) Would masking the smell of ripening paddy-fields help mitigate human–elephant conflict in Sri Lanka. Oryx 44:509–511

    Article  Google Scholar 

  • Schneider SP, Macrides F (1978) Laminar distribution of interneurons in the main olfactory bulb of the adult hamster. Brain Res Bull 3:73–82

    PubMed  Article  CAS  Google Scholar 

  • Shibata M, Mondal MS, Date Y, Nakazato M, Suzuki H, Ueta Y (2008) Distribution of orexins-containing fibers and contents of orexins in the rat olfactory bulb. Neurosci Res 61:99–105

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  Google Scholar 

  • Smith RL, Baker H, Kolstad K, Spencer DD, Greer CA (1991) Localization of tyrosine hydroxylase and olfactory marker protein immunoreactivities in the human and macaque olfactory bulbs. Brain Res 548:140–148

    Google Scholar 

  • Smitka M, Abomaali N, Witt M, Gerber JC, Neuhuber W, Buschhueter D, Puschmann S, Hummel T (2009) Olfactory bulb ventricles as a frequent finding in magnetic resonance imagery studies of the olfactory system. Neuroscience 162:482–485

    PubMed  Article  CAS  Google Scholar 

  • Tabuce R, Asher R, Lehmann T (2008) Afrotherian mammals: a review of current data. Mammalia 22:2–14

    Article  Google Scholar 

  • Tillet Y, Thibault J, Dubois MP (1987) Immunocytochemical demonstration of the presence of catecholamine and serotonin neurons in the sheep olfactory bulb. Neuroscience 20:1011–1022

    PubMed  Article  CAS  Google Scholar 

  • Vidya TNC, Sukumar R (2005) Social and reproductive behavior in elephants. Curr Sci 89:1200–1207

    Google Scholar 

  • Wouterlood FG, Härtig W (1995) Calretinin-immunoreactivity in mitral cells of the rat olfactory bulb. Brain Res 682:93–100

    PubMed  Article  CAS  Google Scholar 

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Acknowledgments

This study was supported by a grant from the South African National Research Foundation to PRM (Grant number: FA2005033100004) and the Swiss-South African Joint Research Programme to A.O.I. 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.

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The authors have no conflict of interest.

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Authors and Affiliations

  1. School of Anatomical Sciences, Faculty of Health Sciences, University of the Witwatersrand, 7 York Road, Parktown, Johannesburg, 2193, South Africa

    Ayanda Ngwenya, Nina Patzke, Amadi O. Ihunwo & Paul R. Manger

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  1. Ayanda Ngwenya
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  2. Nina Patzke
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  3. Amadi O. Ihunwo
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  4. Paul R. Manger
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Correspondence to Paul R. Manger.

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Ngwenya, A., Patzke, N., Ihunwo, A.O. et al. Organisation and chemical neuroanatomy of the African elephant (Loxodonta africana) olfactory bulb. Brain Struct Funct 216, 403–416 (2011). https://doi.org/10.1007/s00429-011-0316-y

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  • DOI: https://doi.org/10.1007/s00429-011-0316-y

Keywords

  • Proboscidean
  • Olfaction
  • Neurogenesis
  • Immunohistochemistry
  • Glomeruli