Olfactory bulbectomy, but not odor conditioned aversion, induces the differentiation of immature neurons in the adult rat piriform cortex

Neuroscience

Volumn 181, Issue , 2011, Pages 18-27

  Gómez Climent, Á ^a   Hernandez Gonzalez S ^a   Shionoya, K ^b   Belles, M ^a   Alonso Llosa, G ^a   Datiche, F ^b   Nacher, J ^a  

^a UNIVERSITY OF VALENCIA   (Spain)

^b UNIVERSITÉ DE BOURGOGNE   (France)

Author keywords

Adult neurogenesis; Doublecortin; GAD67; Neuronal differentiation; Olfactory learning; PSA NCAM

Indexed keywords

DOUBLECORTIN; GLUTAMATE DECARBOXYLASE 67; NERVE CELL ADHESION MOLECULE; NEURON SPECIFIC NUCLEAR PROTEIN; POLYSIALIC ACID;

ANIMAL TISSUE; ARTICLE; AVERSION; BRAIN NERVE CELL; CELL DEATH; CELL DIFFERENTIATION; CELL FUNCTION; CONTROLLED STUDY; INTERNEURON; MALE; NONHUMAN; ODOR AVERSION; OLFACTORY BULBECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRIFORM CORTEX; RAT;

ANIMALS; CELL DIFFERENTIATION; MALE; NEURAL STEM CELLS; NEUROGENESIS; OLFACTORY BULB; OLFACTORY PATHWAYS; RATS; RATS, WISTAR;

EID: 79953703974     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.03.004     Document Type: Article

References (54)

1. Abrous D.N., Montaron M.F., Petry K.G., Rougon G., Darnaudery M., Le Moal M., Mayo W. Decrease in highly polysialylated neuronal cell adhesion molecules and in spatial learning during ageing are not correlated. Brain Res 1997, 744:285-292.
2. Acarin L., Villapol S., Faiz M., Rohn T.T., Castellano B., Gonzalez B. Caspase-3 activation in astrocytes following postnatal excitotoxic damage correlates with cytoskeletal remodeling but not with cell death or proliferation. Glia 2007, 55:954-965.
3. Barker J.M., Galea L.A. Repeated estradiol administration alters different aspects of neurogenesis and cell death in the hippocampus of female, but not male, rats. Neuroscience 2008, 152:888-902.
4. Bonfanti L. PSA-NCAM in mammalian structural plasticity and neurogenesis. Prog Neurobiol 2006, 80:129-164.
5. Bonfanti L., Olive S., Poulain D.A., Theodosis D.T. Mapping of the distribution of polysialylated neural cell adhesion molecule throughout the central nervous system of the adult rat: an immunohistochemical study. Neuroscience 1992, 49:419-436.
6. Brennan P.A., Keverne E.B. Neural mechanisms of mammalian olfactory learning. Prog Neurobiol 1997, 51:457-481.
7. Cai Y., Xiong K., Chu Y., Luo D.W., Luo X.G., Yuan X.Y., Struble R.G., Clough R.W., Spencer D.D., Williamson A., Kordower J.H., Patrylo P.R., Yan X.X. Doublecortin expression in adult cat and primate cerebral cortex relates to immature neurons that develop into GABAergic subgroups. Exp Neurol 2009, 216:342-356.
8. Chapuis J., Garcia S., Messaoudi B., Thevenet M., Ferreira G., Gervais R., Ravel N. The way an odor is experienced during aversive conditioning determines the extent of the network recruited during retrieval: a multisite electrophysiological study in rats. J Neurosci 2009, 29:10287-10298.
9. Dardou D., Datiche F., Cattarelli M. Fos and Egr1 expression in the rat brain in response to olfactory cue after taste-potentiated odor aversion retrieval. Learn Mem 2006, 13:150-160.
10. Ferry B., Sandner G., Di Scala G. Neuroanatomical and functional specificity of the basolateral amygdaloid nucleus in taste-potentiated odor aversion. Neurobiol Learn Mem 1995, 64:169-180.
11. Fontana X., Nacher J., Soriano E., Del Rio J.A. Cell proliferation in the adult hippocampal formation of rodents and its modulation by entorhinal and fimbria-fornix afferents. Cereb Cortex 2006, 16:301-312.
12. Fox G.B., Fichera G., Barry T., O'Connell A.W., Gallagher H.C., Murphy K.J., Regan C.M. Consolidation of passive avoidance learning is associated with transient increases of polysialylated neurons in layer II of the rat medial temporal cortex. J Neurobiol 2000, 45:135-141.
13. Friedman B., Price J.L. Age-dependent cell death in the olfactory cortex: lack of transneuronal degeneration in neonates. J Comp Neurol 1986, 246:20-31.
14. Gomez-Climent M.A., Castillo-Gomez E., Varea E., Guirado R., Blasco-Ibanez J.M., Crespo C., Martinez-Guijarro F.J., Nacher J. A population of prenatally generated cells in the rat paleocortex maintains an immature neuronal phenotype into adulthood. Cereb Cortex 2008, 18:2229-2240.
15. Gomez-Climent M.A., Guirado R., Varea E., Nacher J. "Arrested development". Immature, but not recently generated, neurons in the adult brain. Arch Ital Biol 2010, 148:159-172.
16. Gould E., Wooley C.S., McEwen B.S. Naturally occurring cell death in the developing dentate gyrus of the rat. J Comp Neurol 1991, 304:408-418.
17. Gramsbergen A., Ijkema-Paassen J. Do early lesions affect cell death in the central nervous system?. A study on the effects of early cerebellar hemispherectomy in rats. J Comp Neurol 1987, 255:617-624.
18. Gundersen H.J., Jensen E.B. The efficiency of systematic sampling in stereology and its prediction. J Microsc 1987, 147(Pt 3):229-263.
19. Guo F., Maeda Y., Ma J., Xu J., Horiuchi M., Miers L., Vaccarino F., Pleasure D. Pyramidal neurons are generated from oligodendroglial progenitor cells in adult piriform cortex. J Neurosci 2010, 30:12036-12049.
20. Haberly L.B. Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem Senses 2001, 26:551-576.
21. Kempermann G., Jessberger S., Steiner B., Kronenberg G. Milestones of neuronal development in the adult hippocampus. Trends Neurosci 2004, 27:447-452.
22. Knafo S., Barkai E., Herrero A.I., Libersat F., Sandi C., Venero C. Olfactory learning-related NCAM expression is state, time, and location specific and is correlated with individual learning capabilities. Hippocampus 2005, 15:316-325.
23. Kornack D.R., Kelly E.A., Shannon D.E. Persistent doublecortin expression identifies a novel neuronal population in adult primate neocortex 2005, Program No143102005 Abstract Viewer/Itinerary Planner, Society for Neuroscience, Washington, DC, 2005 Online.
24. Leung C.H., Wilson D.A. Trans-neuronal regulation of cortical apoptosis in the adult rat olfactory system. Brain Res 2003, 984:182-188.
25. Litaudon P., Mouly A.M., Sullivan R., Gervais R., Cattarelli M. Learning-induced changes in rat piriform cortex activity mapped using multisite recording with voltage sensitive dye. Eur J Neurosci 1997, 9:1593-1602.
26. Luzzati F., Bonfanti L., Fasolo A., Peretto P. DCX and PSA-NCAM expression identifies a population of neurons preferentially distributed in associative areas of different pallial derivatives and vertebrate species. Cereb Cortex 2009, 19:1028-1041.
27. Luzzati F., Peretto P., Aimar P., Ponti G., Fasolo A., Bonfanti L. Glia-independent chains of neuroblasts through the subcortical parenchyma of the adult rabbit brain. Proc Natl Acad Sci U S A 2003, 100:13036-13041.
28. Mullen R.J., Buck C.R., Smith A.M. NeuN, a neuronal specific nuclear protein in vertebrates. Development 1992, 116:201-211.
29. Murphy K.J., Fox G.B., Foley A.G., Gallagher H.C., O'Connell A., Griffin A.M., Nau H., Regan C.M. Pentyl-4-yn-valproic acid enhances both spatial and avoidance learning, and attenuates age-related NCAM-mediated neuroplastic decline within the rat medial temporal lobe. J Neurochem 2001, 78:704-714.
30. Nacher J., Alonso-Llosa G., Rosell D.R., McEwen B.S. PSA-NCAM expression in the piriform cortex of the adult rat. Modulation by NMDA receptor antagonist administration. Brain Res 2002, 927:111-121.
31. Nacher J., Crespo C., McEwen B.S. Doublecortin expression in the adult rat telencephalon. Eur J Neurosci 2001, 14:629-644.
32. Nacher J., Guirado R., Varea E., Alonso-Llosa G., Rockle I., Hildebrandt H. Divergent impact of the polysialyltransferases ST8SiaII and ST8SiaIV on polysialic acid expression in immature neurons and interneurons of the adult cerebral cortex. Neuroscience 2010, 167:825-837.
33. O'Connell A.W., Fox G.B., Barry T., Murphy K.J., Fichera G., Foley A.G., Kelly J., Regan C.M. Spatial learning activates neural cell adhesion molecule polysialylation in a corticohippocampal pathway within the medial temporal lobe. J Neurochem 1997, 68:2538-2546.
34. Palmerino C.C., Rusiniak K.W., Garcia J. Flavor-illness aversions: the peculiar roles of odor and taste in memory for poison. Science 1980, 208:753-755.
35. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1986, Academic Press, London.
36. Pekcec A., Loscher W., Potschka H. Neurogenesis in the adult rat piriform cortex. Neuroreport 2006, 17:571-574.
37. Phillips W., Jennifer M.A., Barker R.A. Limbic neurogenesis/plasticity in the R6/2 mouse model of Huntington's disease. Neuroreport 2006, 17:1623-1627.
38. Reeves R.H., Yao J., Crowley M.R., Buck S., Zhang X., Yarowsky P., Gearhart J.D., Hilt D.C. Astrocytosis and axonal proliferation in the hippocampus of S100b transgenic mice. Proc Natl Acad Sci U S A 1994, 91:5359-5363.
39. Rivers L.E., Young K.M., Rizzi M., Jamen F., Psachoulia K., Wade A., Kessaris N., Richardson W.D. PDGFRA/NG2 glia generate myelinating oligodendrocytes and piriform projection neurons in adult mice. Nat Neurosci 2008, 11:1392-1401.
40. Sarma AA, Richard MB, Greer CA (in press) Developmental dynamics of piriform cortex. Cereb Cortex, in press.
41. Seki T., Arai Y. Expression of highly polysialylated NCAM in the neocortex and piriform cortex of the developing and the adult rat. Anat Embryol (Berl) 1991, 184:395-401.
42. Shapiro L.A., Ng K., Zhou Q.Y., Ribak C.E. Subventricular zone-derived, newly generated neurons populate several olfactory and limbic forebrain regions. Epilepsy Behav 2009, 14(Suppl 1):74-80.
43. Shapiro L.A., Ng K.L., Kinyamu R., Whitaker-Azmitia P., Geisert E.E., Blurton-Jones M., Zhou Q.Y., Ribak C.E. Origin, migration and fate of newly generated neurons in the adult rodent piriform cortex. Brain Struct Funct 2007, 212:133-148.
44. Shapiro L.A., Ng K.L., Zhou Q.Y., Ribak C.E. Olfactory enrichment enhances the survival of newly born cortical neurons in adult mice. Neuroreport 2007, 18:981-985.
45. Shionoya K., Datiche F. Inactivation of the basolateral amygdala impairs the retrieval of recent and remote taste-potentiated odor aversion memory. Neurobiol Learn Mem 2009, 92:590-596.
46. Shipley M.T., Adamek G.D. The connections of the mouse olfactory bulb: a study using orthograde and retrograde transport of wheat germ agglutinin conjugated to horseradish peroxidase. Brain Res Bull 1984, 12:669-688.
47. Varea E., Castillo-Gomez E., Gomez-Climent M.A., Guirado R., Blasco-Ibañez J.M., Crespo C., Martinez-Guijarro F.J., Nacher J. Differential evolution of PSA-NCAM expression during aging of the rat telencephalon. Neurobiol Aging 2009, 30:808-818.
48. West M.J. New stereological methods for counting neurons. Neurobiol Aging 1993, 14:275-285.
49. Wilson D.A. Receptive fields in the rat piriform cortex. Chem Senses 2001, 26:577-584.
50. Wilson D.A., Fletcher M.L., Sullivan R.M. Acetylcholine and olfactory perceptual learning. Learn Mem 2004, 11:28-34.
51. Wilson D.A., Stevenson R.J. The fundamental role of memory in olfactory perception. Trends Neurosci 2003, 26:243-247.
52. Xiong K., Luo D.W., Patrylo P.R., Luo X.G., Struble R.G., Clough R.W., Yan X.X. Doublecortin-expressing cells are present in layer II across the adult guinea pig cerebral cortex: partial colocalization with mature interneuron markers. Exp Neurol 2008, 211:271-282.
53. Zhang R., Xue Y.Y., Lu S.D., Wang Y., Zhang L.M., Huang Y.L., Signore A.P., Chen J., Sun F.Y. Bcl-2 enhances neurogenesis and inhibits apoptosis of newborn neurons in adult rat brain following a transient middle cerebral artery occlusion. Neurobiol Dis 2006, 24:345-356.
54. Zhang X.M., Cai Y., Chu Y., Chen E.Y., Feng J.C., Luo X.G., Xiong K., Struble R.G., Clough R.W., Patrylo P.R., Kordower J.H., Yan X.X. Doublecortin-expressing cells persist in the associative cerebral cortex and amygdala in aged nonhuman primates. Front Neuroanat 2009, 3:17.