Influence of ontogenetic age on the role of dentate granule neurons

Brain Structure and Function - Tập 220 - Trang 645-661 - 2014
Sophie Tronel1,2, Valérie Lemaire1,2, Vanessa Charrier1,2, Marie-Françoise Montaron1,2, Djoher Nora Abrous1,2
1Inserm U862, Bordeaux, France
2Université de Bordeaux, Bordeaux, France

Tóm tắt

New neurons are continuously produced in the adult dentate gyrus of the hippocampus, a key structure in learning and memory. It has been shown that adult neurogenesis is crucial for normal memory processing. However, it is not known whether neurons born during the developmental period and during adulthood support the same functions. Here, we demonstrate that neurons born in neonates (first postnatal week) are activated in different memory processes when they are mature compared to neurons born in adults. By imaging the activation of these two different neuron generations in the same rat and using the IEG Zif268 and Fos, we show that these neurons are involved in discriminating dissimilar contexts and spatial problem solving, respectively. These findings demonstrate that the ontogenetic stage during which neurons are generated is crucial for their function within the memory network.

Tài liệu tham khảo

Abrous DN, Koehl M, Le Moal M (2005) Adult neurogenesis: from precursors to network and physiology. Physiol Rev 85(2):523–569 Akers KG, Arruda-Carvalho M, Josselyn SA, Frankland PW (2012) Ontogeny of contextual fear memory formation, specificity, and persistence in mice. Learn Mem 19(12):598–604. doi:10.1101/lm.027581.112 Albert JR (1987) Early learning and ontogenetic adaptation. In: Krasnegor NA, Blass EM, Hofer MA, Smotherman WP (eds) Perinatal development: a psychological perspective, vol 1. Academic Press, INC, pp 11–38 Campbell BA, Spear NE (1972) Ontogeny of memory. Psychol Rev 79(3):215–236 Campbell NR, Fernandes CC, John D, Lozada AF, Berg DK (2011) Nicotinic control of adult-born neuron fate. Biochem Pharmacol 82(8):820–827. doi:10.1016/j.bcp.2011.06.021 Clark RE, Broadbent NJ, Squire LR (2005) Hippocampus and remote spatial memory in rats. Hippocampus 15(2):260–272. doi:10.1002/hipo.20056 Clelland CD, Choi M, Romberg C, Clemenson GD Jr, Fragniere A, Tyers P, Jessberger S, Saksida LM, Barker RA, Gage FH, Bussey TJ (2009) A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325(5937):210–213 Davis S, Bozon B, Laroche S (2003) How necessary is the activation of the immediate early gene zif268 in synaptic plasticity and learning? BehavBrain Res 142(1–2):17–30 Denenberg VH (1972) Readings in the development of behavior. Sinauer Associates Inc, Stamford Deng W, Mayford M, Gage FH (2013) Selection of distinct populations of dentate granule cells in response to inputs as a mechanism for pattern separation in mice. eLife 2:00312. doi:10.7554/eLife.00312 Dumas TC (2005) Late postnatal maturation of excitatory synaptic transmission permits adult-like expression of hippocampal-dependent behaviors. Hippocampus 15(5):562–578. doi:10.1002/hipo.20077 Dupret D, Fabre A, Dobrossy MD, Panatier A, Rodriguez JJ, Lamarque S, Lemaire V, Oliet SH, Piazza PV, Abrous DN (2007) Spatial learning depends on both the addition and removal of new hippocampal neurons. PLoSBiol 5(8):e214 Dupret D, Revest JM, Koehl M, Ichas JF, De Giorgi F, Costet P, Abrous DN, Piazza PV (2008) Spatial relational memory requires hippocampal adult neurogenesis. PLoS ONE 3(4):e1959 Garthe A, Behr J, Kempermann G (2009) Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLoS ONE 4(5):5464 Ge S, Yang CH, Hsu KS, Ming GL, Song H (2007) A critical period for enhanced synaptic plasticity in newly generated neurons of the adult brain. Neuron 54(4):559–566 Gu Y, Arruda-Carvalho M, Wang J, Janoschka SR, Josselyn SA, Frankland PW, Ge S (2012) Optical controlling reveals time-dependent roles for adult-born dentate granule cells. Nat Neurosci 15(12):1700–1706. doi:10.1038/nn.3260 Guzowski JF, Timlin JA, Roysam B, McNaughton BL, Worley PF, Barnes CA (2005) Mapping behaviorally relevant neural circuits with immediate-early gene expression. Curr Opin Neurobiol 15(5):599–606. doi:10.1016/j.conb.2005.08.018 Harlow HF, Harlow MK, Rueping RR, Mason WA (1960) Performance of infant rhesus monkeys on discrimination learning, delayed response, and discrimination learning set. J Comp Physiol Psychol 53:113–121 Hofacer RD, Deng M, Ward CG, Joseph B, Hughes EA, Jiang C, Danzer SC, Loepke AW (2013) Cell age-specific vulnerability of neurons to anesthetic toxicity. Ann Neurol 73(6):695–704. doi:10.1002/ana.23892 Jackson JH (1958) Evolution and dissolution of the nervous system. In: Taylor J (ed) Selected writings of John Hughlings Jackson, vol 2. New York Basic Books, New York, pp 44–63 Kee N, Teixeira CM, Wang AH, Frankland PW (2007) Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat Neurosci 10(3):355–362. doi:10.1038/nn1847 Kempermann G, Jessberger S, Steiner B, Kronenberg G (2004) Milestones of neuronal development in the adult hippocampus. Trends Neurosci 27(8):447–452 Koya E, Golden SA, Harvey BK, Guez-Barber DH, Berkow A, Simmons DE, Bossert JM, Nair SG, Uejima JL, Marin MT, Mitchell TB, Farquhar D, Ghosh SC, Mattson BJ, Hope BT (2009) Targeted disruption of cocaine-activated nucleus accumbens neurons prevents context-specific sensitization. Nat Neurosci 12(8):1069–1073. doi:10.1038/nn.2364 Kron MM, Zhang H, Parent JM (2010) The developmental stage of dentate granule cells dictates their contribution to seizure-induced plasticity. J Neurosci Off J Soc Neurosci 30(6):2051–2059. doi:10.1523/JNEUROSCI.5655-09.2010 Kruger HS, Brockmann MD, Salamon J, Ittrich H, Hanganu-Opatz IL (2012) Neonatal hippocampal lesion alters the functional maturation of the prefrontal cortex and the early cognitive development in pre-juvenile rats. Neurobiol Learn Mem 97(4):470–481. doi:10.1016/j.nlm.2012.04.001 Langston RF, Ainge JA, Couey JJ, Canto CB, Bjerknes TL, Witter MP, Moser EI, Moser MB (2010) Development of the spatial representation system in the rat. Science 328(5985):1576–1580. doi:10.1126/science.1188210 Laplagne DA, Esposito MS, Piatti VC, Morgenstern NA, Zhao C, van PH, Gage FH, Schinder AF (2006) Functional convergence of neurons generated in the developing and adult hippocampus. PLoSBiol 4(12):409 Laplagne DA, Kamienkowski JE, Esposito MS, Piatti VC, Zhao C, Gage FH, Schinder AF (2007) Similar GABAergic inputs in dentate granule cells born during embryonic and adult neurogenesis. Eur J Neurosci 25(10):2973–2981. doi:10.1111/j.1460-9568.2007.05549.x Lavenex P, Banta Lavenex P (2013) Building hippocampal circuits to learn and remember: insights into the development of human memory. Behav Brain Res. doi:10.1016/j.bbr.2013.02.007 Lemaire V, Koehl M, Le Moal M, Abrous DN (2000) Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci USA 97(20):11032–11037 Lemaire V, Tronel S, Montaron MF, Fabre A, Dugast E, Abrous DN (2012) Long-lasting plasticity of hippocampal adult-born neurons. J Neurosci Off J Soc Neurosci 32(9):3101–3108. doi:10.1523/JNEUROSCI.4731-11.2012 Leuner B, Glasper ER, Gould E (2009) Thymidine analog methods for studies of adult neurogenesis are not equally sensitive. J Comp Neurol 517(2):123–133. doi:10.1002/cne.22107 Loy R, Koziell DA, Lindsey JD, Moore RY (1980) Noradrenergic innervation of the adult rat hippocampal formation. J Comp Neurol 189(4):699–710. doi:10.1002/cne.901890406 Lucassen PJ, Naninck EF, van Goudoever JB, Fitzsimons C, Joels M, Korosi A (2013) Perinatal programming of adult hippocampal structure and function; emerging roles of stress, nutrition and epigenetics. Trends Neurosci 36(11):621–631. doi:10.1016/j.tins.2013.08.002 Marin-Burgin A, Mongiat LA, Pardi MB, Schinder AF (2012) Unique processing during a period of high excitation/inhibition balance in adult-born neurons. Science 335(6073):1238–1242. doi:10.1126/science.1214956 Mathews EA, Morgenstern NA, Piatti VC, Zhao C, Jessberger S, Schinder AF, Gage FH (2010) A distinctive layering pattern of mouse dentate granule cells is generated by developmental and adult neurogenesis. J Comp Neurol 518(22):4479–4490. doi:10.1002/cne.22489 Moye TB, Rudy JW (1987) Ontogenesis of trace conditioning in young rats: dissociation of associative and memory processes. Dev Psychobiol 20(4):405–414. doi:10.1002/dev.420200405 Nakashiba T, Cushman JD, Pelkey KA, Renaudineau S, Buhl DL, McHugh TJ, Rodriguez Barrera V, Chittajallu R, Iwamoto KS, McBain CJ, Fanselow MS, Tonegawa S (2012) Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 149(1):188–201. doi:10.1016/j.cell.2012.01.046 Nokia MS, Sisti HM, Choksi MR, Shors TJ (2012) Learning to learn: theta oscillations predict new learning, which enhances related learning and neurogenesis. PLoS ONE 7(2):31375. doi:10.1371/journal.pone.0031375 Oppenheim RW (1980) Metamorphosis and adaptation in the behavior of developing organisms. Dev Psychobiol 13(4):353–356. doi:10.1002/dev.420130402 Piaget J, Inhelder B (1969) The psychology of the child. New York Basic Books Inc, New York Ribordy F, Jabes A, Banta Lavenex P, Lavenex P (2013) Development of allocentric spatial memory abilities in children from 18 months to 5 years of age. Cogn Psychol 66(1):1–29. doi:10.1016/j.cogpsych.2012.08.001 Rice D, Barone S Jr (2000) Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect 108(Suppl 3):511–533 Rudy JW, Cheatle MD (1977) Odor-aversion learning in neonatal rats. Science 198(4319):845–846 Rudy JW, Hyson RL (1984) Ontogenesis of learning: III. Variation in the rat’s differential reflexive and learned responses to sound frequencies. Dev Psychobiol 17(3):285–300. doi:10.1002/dev.420170308 Rudy JW, Stadler-Morris S, Albert P (1987) Ontogeny of spatial navigation behaviors in the rat: dissociation of “proximal”- and “distal”-cue-based behaviors. Behav Neurosci 101(1):62–73 Sagar SM, Sharp FR, Curran T (1988) Expression of c-fos protein in brain: metabolic mapping at the cellular level. Science 240(4857):1328–1331 Sara SJ (2009) The locus coeruleus and noradrenergic modulation of cognition. Nat Rev Neurosci 10(3):211–223. doi:10.1038/nrn2573 Schenk F (1985) Development of place navigation in rats from weaning to puberty. Behav Neural Biol 43(1):69–85 Schlessinger AR, Cowan WM, Gottlieb DI (1975) An autoradiographic study of the time of origin and the pattern of granule cell migration in the dentate gyrus of the rat. J Comp Neurol 159(2):149–175. doi:10.1002/cne.901590202 Scott RC, Richard GR, Holmes GL, Lenck-Santini PP (2011) Maturational dynamics of hippocampal place cells in immature rats. Hippocampus 21(4):347–353. doi:10.1002/hipo.20789 Snyder JS, Clifford MA, Jeurling SI, Cameron HA (2012) Complementary activation of hippocampal-cortical subregions and immature neurons following chronic training in single and multiple context versions of the water maze. Behav Brain Res 227(2):330–339. doi:10.1016/j.bbr.2011.06.025 Stone SS, Teixeira CM, Zaslavsky K, Wheeler AL, Martinez-Canabal A, Wang AH, Sakaguchi M, Lozano AM, Frankland PW (2011) Functional convergence of developmentally and adult-generated granule cells in dentate gyrus circuits supporting hippocampus-dependent memory. Hippocampus 21(12):1348–1362. doi:10.1002/hipo.20845 Tronel S, Belnoue L, Grosjean N, Revest JM, Piazza PV, Koehl M, Abrous DN (2010a) Adult-born neurons are necessary for extended contextual discrimination. Hippocampus Tronel S, Fabre A, Charrier V, Oliet SH, Gage FH, Abrous DN (2010b) Spatial learning sculpts the dendritic arbor of adult-born hippocampal neurons. Proc Natl Acad Sci USA 107(17):7963–7968. doi:10.1073/pnas.0914613107 Trouche S, Bontempi B, Roullet P, Rampon C (2009) Recruitment of adult-generated neurons into functional hippocampal networks contributes to updating and strengthening of spatial memory. Proc Natl Acad Sci USA 106(14):5919–5924 Vega CJ, Peterson DA (2005) Stem cell proliferative history in tissue revealed by temporal halogenated thymidine analog discrimination. Nat Methods 2(3):167–169. doi:10.1038/nmeth741 Wei L, Meaney MJ, Duman RS, Kaffman A (2011) Affiliative behavior requires juvenile, but not adult neurogenesis. J Neurosci Off J Soc Neurosci 31(40):14335–14345. doi:10.1523/JNEUROSCI.1333-11.2011 Wills TJ, Cacucci F, Burgess N, O’Keefe J (2010) Development of the hippocampal cognitive map in preweanling rats. Science 328(5985):1573–1576. doi:10.1126/science.1188224 Wills TJ, Barry C, Cacucci F (2012) The abrupt development of adult-like grid cell firing in the medial entorhinal cortex. Front Neural Circuits 6:21. doi:10.3389/fncir.2012.00021