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Adult neurogenesis in the African giant rat (Cricetomysgambianus, waterhouse)

Abstract

African giant rats (AGR) are large nocturnal rodents with well-developed olfactory abilities uniquely linked to cognition. The post natal proliferation of neurons (adult neurogenesis), is thought to play an important role in spatial memory and learning. Eighteen brains of the African giant rats (Cricetomys gambianus, Waterhouse) belonging to three age groups (neonates n = 6, juveniles n = 6 and adults n = 6) were examined by immunohistochemistry, using antibodies for proliferating cells (Ki-67), and immature neurons (Doublecortin, DCX). Mean brain weights were 0.40 ± 0.00 g; 4.48 ± 0.43 g and 5.48 ± 0.56 g for neonate, juvenile and adult brains respectively. Our results show positive cell proliferation in the subventricular (SVZ) zone of the lateral ventricle and in the dentate gyrus (DG) of the hippocampus but at low levels in adults compared to juveniles. Estimate of the mean total proliferative Ki-67 positive cells in the SVZ and DG in the neonates was 21145 ± 8395, and 11800 ± 1230; brains from juvenile AGRs, 45530 ± 13950 and 12480 ± 7860 and from adult brains, (6880 ± 340 and 1130 ± 150) respectively. Juvenile AGR in particular, stained positively in potential sites such as the piriform and somatosensory cortices, striatum and cerebellum. This intensity of the proliferating cells within the dentate gyrus in the juvenile and adult brains could be associated with a role in the cognitive functions of landmine detection and tuberculosis diagnosis after olfactory training of the African giant rat. The juvenile rats are proposed as the most suited for experimental research and olfactory training.

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References

  • Ajao MS, Olaleye O, Ihunwo AO (2010) Melatonin potentiates cell proliferation in the dentate gyrus following ischemic brain injury in adult rats. J Anim Vet Adv 9(11):1633–1638

    CAS  Article  Google Scholar 

  • Ajayi SS (1974) The biology and domestication of African giant rat (CricetomysgambianusWaterhouse), Ph.D. Thesis. University of Ibadan, Nigeria

  • Ajayi S (1977) Field observations on the African giant rat Cricetomysgambianus in southern Nigeria. East Afr Wildl J 15(3):191–198

    Article  Google Scholar 

  • Altman J (1962) Are new neurons formed in the brains of adult mammals? Science 135:1127–1128

    CAS  PubMed  Article  Google Scholar 

  • Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319–335

    CAS  PubMed  Article  Google Scholar 

  • Alvarez-Buylla A, Garcia-Verdugo JM (2002) Neurogenesis in adult subventricular zone. J Neurosci 22:629–634

    CAS  PubMed  Google Scholar 

  • Amrein I, Lipp HP (2009) Adult hippocampal neurogenesis of mammals: evolution and life history. Biol Lett 5:141–144

    PubMed Central  PubMed  Article  Google Scholar 

  • Amrein I, Slomianka L, Poletaeva I, Bologova NV, Lipp HP (2004) Marked species and age-dependent differences in cell proliferation and neurogenesis in the hippocampus of wild-living rodents. Hippocampus 14:1000–1010

    PubMed  Article  Google Scholar 

  • Amrein I, Dechmann DK, Winter Y, Lipp HP (2007) Absent or low rate of adult neurogenesis in the hippocampus of bats (Chiroptera). PLoS ONE 2:e455

    PubMed Central  PubMed  Article  Google Scholar 

  • Barker JM, Wojtowicz JM, Boonstra R (2005) Where’s my dinner? Adult neurogenesis in free-living food-storing rodents. Genes Brain Behav 4:89–98

    CAS  PubMed  Article  Google Scholar 

  • Bartkowska K, Djavadian RL, Taylor JR, Turlejski K (2008) Generation recruitment and death of brain cells throughout the life cycle of Sorex shrews (Lipotyphla). Eur J Neurosci 27:1710–1721

    PubMed  Article  Google Scholar 

  • Bartkowska K, Turlejski K, Grabiec M, Ghazaryan A, Yavruoyan E, Djavadian RL (2010) Adult neurogenesis in the Hedgehog (Erinaceusconcolor) and mole (Talpaeuropaea). Brain Behav Evol 76:128–143

    CAS  PubMed  Article  Google Scholar 

  • Bernier PJ, Bedard A, Vinet J, Levesque M, Parent A (2002) Newly generated neurons in the amygdala and adjoining cortex of adult primates. Proc Natl Acad Sci 99:11464–11469

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Biebl M, Cooper CM, Winklera J, Kuhn HG (2000) Analysis of neurogenesis and programmed cell death reveals a self renewing capacity in the adult rat brain. Neurosci Lett 291:17–20

    CAS  PubMed  Article  Google Scholar 

  • Brown JP, Couillard-Després S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG (2003) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1–10

    CAS  PubMed  Article  Google Scholar 

  • Cai Y, Xiong K, Chu Y, Luo DW, Luo XG, Yuan XY, Struble RG, Clough RW, Spencer DD, Williamson A, Kordower JH, Patrylo PR, Yan XX (2009) Doublecortin expression in adult cat and primate cerebral cortex relates to immature neurons that develop into GABAergic subgroups. Exp Neurol 216:342–356

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Cameron HA, Dayer AG (2008) New interneurons in the adult neocortex: small, sparse, but significant? Biol Psychiatry 63:650–655

    PubMed Central  PubMed  Article  Google Scholar 

  • Chawana R, Patzke N, Kaswera C, Gilissen E, Ihunwo AO, Manger PR (2013) Adult neurogenesis in eight Megachiropteran species. Neuroscience 244:159–172

    CAS  PubMed  Article  Google Scholar 

  • Dayer AG, Cleaver KM, Abouantoun T, Cameron HA (2005) New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors. J Cell Biol 168(3):415–427

    Google Scholar 

  • Epp JR, Barker JM, Galea LA (2009) Running wild: neurogenesis in the hippocampus across the lifespan in wild and laboratorybred Norway rats. Hippocampus 19:1040–1049

    PubMed  Article  Google Scholar 

  • Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313–1317

    CAS  PubMed  Article  Google Scholar 

  • Fox CA, Fischer RR, Desalva SJ (1948) The distribution of the anterior commissure in the monkey, Macacamulatta. J Comp Neurol 89:245–277

    CAS  PubMed  Article  Google Scholar 

  • Francis F, Koulakoff A, Boucher D, Chafey P, Schaar B, Vinet MC, Friocourt G, McDonnell N, Reiner O, Kahn A, McConnell SK, Berwald-Netter Y, Denoulet P, Chelly J (1999) Doublecortin is a developmentally regulated, microtubule-associated protein expressed in migrating and differentiating neurons. Neuron 23:247–256

    CAS  PubMed  Article  Google Scholar 

  • Gage FH (2000) Mammalian neural stem cells. Science 287:1433–1438

    CAS  PubMed  Article  Google Scholar 

  • Gleeson JG, Lin PT, Flanagan LA, Walsh CA (1999) Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23:257–271

    CAS  PubMed  Article  Google Scholar 

  • Gould E (2007) How widespread is adult neurogenesis in mammals? Nat Rev Neurosci 8:481–488

    CAS  PubMed  Article  Google Scholar 

  • Gould E, Reeves AJ, Graziano MS, Gross CG (1999) Neurogenesis in the neocortex of adult primates. Science 286:548–552

    CAS  PubMed  Article  Google Scholar 

  • Grabiec M, Turlejski K, Djavadian RL (2009) The partial 5-HT1A receptor agonist buspirone enhances neurogenesis in the opossum (Monodelphisdomestica). Eur Neuropsychpharmacol 19:431–439

    CAS  Article  Google Scholar 

  • Happold DCD (1987) The Mammals of Nigeria. Clarendon, Oxford

    Google Scholar 

  • Heimer L (1968) Synaptic distribution of centripetal and centrifugal nerve fibres in the olfactory system of the rat. An experimental anatomical study. J Anat 103:413–432

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hwang IK, Yoo KY, Li H, Choi JH, Kwon YG, Ahn Y, Lee IS, Won MH (2007) Differences in doublecortinimmunoreactivity and protein levels in the hippocampal dentate gyrus between adult and aged dogs. Neurochem Res 32:1604–1609

    CAS  PubMed  Article  Google Scholar 

  • Ibe CS, Onyeanusi BI, Hambolu JO, Ayo JO (2010) Sexual dimorphism in the whole brain and brainstem morphometry in the African giant pouched rat (Cricetomysgambianus, Waterhouse 1840). Folia Morphol 69(2):69–74

    CAS  Google Scholar 

  • Ihunwo AO, Pillay S (2007) Neurogenic sites in the Adult Mammalian central nervous system. Res J Biol Sci 2(2):170–177

    Google Scholar 

  • Kempermann G, Kuhn HG, Gage FH (1997) Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proc Natl Acad Sci 94:10409–10414

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Kempermann G, Gast D, Kronenberg G, Yamaguchi M, Gage FH (2003) Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development 130:391–399

    CAS  PubMed  Article  Google Scholar 

  • Klempin F, Kronenberg G, Cheung G, Kettenmann H, Kempermann G (2011) Properties of doublecortin-(DCX)-expressing cells in the piriform cortex compared to the neurogenic dentate gyrus of adult mice. PLoS One 6(10):e25760. doi:10.1371/journal.pone.0025760

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Koketsu D, Mikami A, Miyamoto Y, Hisatsune T (2003) Nonrenewal of neurons in the cerebral neocortex of adult macaque monkeys. J Neurosci 23:937–942

    CAS  PubMed  Google Scholar 

  • Kokoeva MV, Yin H, Flier JS (2007) Evidence for constitutive neural cell proliferation in the adult murine hypothalamus. J Comp Neurol 505:209–220

    PubMed  Article  Google Scholar 

  • Kornack DR, Rakic P (1999) Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc Natl Acad Sci U S A 96:5768–5773

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Kornack DR, Rakic P (2001) Cell proliferation without neurogenesis in adult primate neocortex. Science 294:2127–2130

    CAS  PubMed  Article  Google Scholar 

  • Kuhn HG, Dickinson-Anson H, Gage FH (1996) Neurogenesis in the dentate gyrus of the adult rat: age-related decrease of neuronal progenitor proliferation. J Neurosci 16:2027–2033

    CAS  PubMed  Google Scholar 

  • Lavenex P, Steele MA, Jacobs LF (2000) The seasonal pattern of cell proliferation and neuron number in the dentate gyrus of wild adult eastern grey squirrels. Eur J Neurosci 12(2):643–648

    Google Scholar 

  • Leuner B, Kozorovitskiy Y, Gross CG, Gould E (2007) Diminished adult neurogenesis in the marmoset brain precedes old age. Proc Natl Acad Sci U S A 104:17169–17173

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Liu YW, Curtis MA, Gibbons HM, Mee EW, Bergin PS, Teoh HH, Connor B, Dragunow M, Faull RL (2008) Doublecortin expression in the normal and epileptic adult human brain. Eur J Neurosci 28:2254–2265

    CAS  PubMed  Article  Google Scholar 

  • Luskin MB (1993) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11:173–189

    CAS  PubMed  Article  Google Scholar 

  • Luzzati F, De Marchis S, Fasola A, Panetto P (2007) Adult neurogenesis and local neuronal progenitors in the striatum. Neurodegener Dis 4(4):322–327

    PubMed  Article  Google Scholar 

  • Luzzati F, Bonfanti L, Fasolo A, Peretto P (2009) DCX and PSA-NCAM expression identifies a population of neurons preferentially distributed in associative areas of different pallial derivatives and vertebrate species. Cereb Cortex 19:1028–1041

    PubMed  Article  Google Scholar 

  • Maslov AY, Barone TA, Plunkett RJ, Pruitt SC (2004) Neural stem cell detection, characterization, and age-related changes in the subventricular zone of mice. J Neurosci 24:1726–1733

    CAS  PubMed  Article  Google Scholar 

  • Matsuo N, Kawamoto S, Matsubara K, Okubo K (1998) Cloning and developmental expression of the murine homolog of doublecortin. Biochem Biophys Res Commun 252:571–576

    CAS  PubMed  Article  Google Scholar 

  • Nacher J, Crespo C, McEwen BS (2001) Doublecortin expression in the adult rat te encephalon. Eur J Neurosci 14:629–644

    CAS  PubMed  Article  Google Scholar 

  • Oke BO (2009) Form and function: The inseparable twins in veterinary medicine. University of Ibadan Inaugural lecture delivered at the University of Ibadan, 19th February, 2009

  • Olude MA, Olopade JO, Fatola IO, Onwuka SK (2009) Some aspects of the neurocraniometry of the African giant rat (Cricetomysgambianus, Waterhouse). Folia Morphol 68:224–227

    CAS  Google Scholar 

  • Olude MA, Ogunbunmi TK, Olopade JO, Ihunwo AO (2014) The olfactory bulb structure of African giant rat (Cricetomysgambianus, Waterhouse 1840) I: Cytoarchitecture. Anat Sci Int. doi:10.1007/s12565-014-0227-0

    PubMed  Google Scholar 

  • Parent JM, Valentin VV, Lowenstein DH (2002) Prolonged seizures increase proliferating neuroblasts in the adult rat subventricular zone-olfactory bulb pathway. J Neurosci 22:3174–3188

    CAS  PubMed  Google Scholar 

  • Patzke N, Kaswera C, Gilissen E, Ihunwo AO, Manger PR (2013) Adult neurogenesis in a giant Otter shrew (Potamogalevelox). J Neurosci 238:270–279

    CAS  Google Scholar 

  • Pekcec A, Baumgärtner W, Bankstahl JP, Stein VM, Potschka H (2008) Effect of aging on neurogenesis in the canine brain. Aging Cell 7:368–374

    CAS  PubMed  Article  Google Scholar 

  • Plumpe T, Ehninger D, Steiner B, Klempin F, Jessberger S, Brandt M, Romer B, Rodriguez GR, Kronenberg G, Kempermann G (2006) Variability of doublecortin-associated dendrite maturation in adult hippocampal neurogenesis is independent of the regulation of precursor cell proliferation. BMC Neurosci 7(77):1–14

    Google Scholar 

  • Scott JW, McBride RL, Schneider SP (1980) The organization of projections from the olfactory bulb to the piriform cortex and olfactory tubercle in the rat. J Comp Neurol 194:519–534

    CAS  PubMed  Article  Google Scholar 

  • Seki T, Arai Y (1991) Expression of highly polysialylated NCAM in the neocortex and piriform cortex of the developing and the adult rat. Anat Embryol 184:395–401

    CAS  PubMed  Article  Google Scholar 

  • Shapiro LA, Ng KL, Kinyamu R, Whitaker- Azmitia P, Geisert EE, Blurton-Jones M, Zhou QY, Ribak CE (2007) Origin, migration and fate of newly generated neurons in the adult rodent piriform cortex. Brain Struct Funct 212:33–48

    Article  Google Scholar 

  • Verhagen R, Cox C, Machang’u R, Weetjens B, Billet M (2003) Preliminary results on the use of Cricetomysratsas indicators of buried explosives in field conditions. In: Mine detection dogs: Training operations and odourdetection. Geneva International Centre for Humanitarian Demining, Geneva, pp 175–193

    Google Scholar 

  • Weetjens BJ, Mgode GF, Machang’u RS, Kazwala R, Mfinanga G, Lwilla F, Cox C, Jubitana M, Kanyagha H, Mtandu R, Kahwa A, Mwessongo J, Makingi G, Mfaume S, van Steenberge J, Beyene NW, Billet M, Verhagen R (2009) African pouched rats for the detectionof pulmonary tuberculosis. Int J Tuberc Lung Dis 13:737–743

    PubMed  Google Scholar 

  • Xiong K, Luo DW, Patrylo PR, Luo XG, Struble RG, Clough RW, Yan XX (2008) Doublecortin- expressing cells are present in layer II across the adult guinea pig cerebral cortex: partial colocalization with mature interneuron markers. Exp Neurol 211:271–282

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  • Zhao C, Deng W, Gage FH (2008) Mechanisms and functional implications of adult neurogenesis. Cell 132:645–660

    CAS  PubMed  Article  Google Scholar 

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Acknowledgments

The authors will like to acknowledge Dr. Tope Ogunbunmi for participating in preparing the brain samples, Mrs. Hasiena Ali of the School of Anatomical Sciences, University of The Witwatersrand for laboratory assistance, the International Society for Neurochemistry Committee for Aid and Education in Neurochemistry (ISN/CAEN) for travel grant to South Africa and funding from the Swiss-South African Joint Research Programme (SSAJRP) to AOI.

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Correspondence to Amadi Ogonda Ihunwo.

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Olude, A.M., Olopade, J.O. & Ihunwo, A.O. Adult neurogenesis in the African giant rat (Cricetomysgambianus, waterhouse). Metab Brain Dis 29, 857–866 (2014). https://doi.org/10.1007/s11011-014-9512-9

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  • DOI: https://doi.org/10.1007/s11011-014-9512-9

Keywords

  • African giant rat
  • Adult neurogenesis
  • Ki-67
  • DCX
  • Dentate gyrus
  • Olfactory abilities