Effects of spaced learning in the water maze on development of dentate granule cells generated in adult mice

Hippocampus

Volumn 25, Issue 11, 2015, Pages 1314-1326

  Trinchero, Mariela F ^a   Koehl, Muriel ^b,c   Bechakra, Malik ^b,c   Delage, Pauline ^b,c   Charrier, Vanessa ^b,c   Grosjean, Noelle ^b,c   Ladeveze, Elodie ^b,c   Schinder, Alejandro F ^a   Abrous, D Nora ^b,c  

^a Consejo Nacional De Investigaciones Científicas Y Técnicas ^*  (Argentina)

^b INSTITUT FRANÇOIS MAGENDIE   (France)

^c UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Adult neurogenesis; Hippocampus; Mice; Spatial memory; Water maze

Indexed keywords

GREEN FLUORESCENT PROTEIN; THYMIDINE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL COUNT; CELL DEATH; CELL LABELING; CELL MATURATION; CELL PROLIFERATION; CELL STRUCTURE; CELL SURVIVAL; CONTROLLED STUDY; DENDRITIC CELL; DENTATE GYRUS; FEMALE; GRANULE CELL; IMMUNOHISTOCHEMISTRY; LEARNING; MALE; MORRIS WATER MAZE TEST; MOUSE; NERVE CELL; NEWBORN; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REFERENCE MEMORY; RETROVIRIDAE; SPATIAL LEARNING; SPINE; ANIMAL; ANIMAL BEHAVIOR; C57BL MOUSE; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CYTOLOGY; MAZE TEST; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY;

ANIMALS; BEHAVIOR, ANIMAL; CELL PHYSIOLOGICAL PROCESSES; DENTATE GYRUS; FEMALE; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; NEUROGENESIS; NEURONS;

EID: 84946494408     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.22438     Document Type: Article

References (53)

1. Altman J. 1962. Are new neurones formed in the brains of adult mammals? Science 135:1127-1128.
2. Ambrogini P, Orsini L, Mancini C, Ferri P, Ciaroni S, Cuppini R. 2004. Learning may reduce neurogenesis in adult rat dentate gyrus. Neurosci Lett 359:13-16.
3. Bailey CH, Kandel ER. 1993. Structural changes accompanying memory storage. Annu Rev Physiol 55:397-426.
4. Chow C, Epp JR, Lieblich SE, Barha CK, Galea LA. 2013. Sex differences in neurogenesis and activation of new neurons in response to spatial learning and memory. Psychoneuroendocrinology 38:1236-1250.
5. 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 325:210-213.
6. Cryan JF, Mombereau C. 2004. In search of a depressed mouse: Utility of models for studying depression-related behavior in genetically modified mice. Mol Psychiatry 9:326-357.
7. Curlik DM, Shors TJ. 2011. Learning increases the survival of newborn neurons provided that learning is difficult to achieve and successful. J Cogn Neurosci 23:2159-2170.
8. Dalla C, Papachristos EB, Whetstone AS, Shors TJ. 2009. Female rats learn trace memories better than male rats and consequently retain a greater proportion of new neurons in their hippocampi. Proc Natl Acad Sci USA 106:2927-2932.
9. Döbrössy MDE, Aurousseau C, Le Moal M, Piazza PV, Abrous DN. 2003. Differential effects of learning on neurogenesis: Learning increases or decreases the number of newly born cells depending on their birth date. Mol Psychiatry 8:974-982.
10. Drapeau E, Mayo W, Aurousseau C, Le Moal M, Piazza PV, Abrous DN. 2003. Spatial memory performances of aged rats in the water maze predict levels of hipppocampal neurogenesis. Proc Natl Acad Sci USA 100:14385-14390.
11. Drapeau E, Montaron MF, Aguerre S, Abrous DN. 2007. Learning-induced survival of new neurons depends on the cognitive status of aged rats. J Neurosci 27:6037-6044.
12. Dupret D, Fabre A, Dobrössy M, Panetier A, Rodriguez JJ, Lemaire V, Oliet SHR, Piazza PV, Abrous DN. 2007. Spatial learning depends on both the addition and removal of new hippocampal neurons. PLoS Biol 5:1683-1694.
13. Dupret D, Revest JM, Koehl M, Ichas F, De GF, Costet P, Abrous DN, Piazza PV. 2008. Spatial relational memory requires hippocampal adult neurogenesis. PLoS One 3:e1959.
14. Epp JR, Scott NA, Galea LA. 2011. Strain differences in neurogenesis and activation of new neurons in the dentate gyrus in response to spatial learning. Neuroscience 172:342-354.
15. Finlay BL, Sengelaub DR. 1981. Toward a neuroethology of mammalian vision: Ecology and anatomy of rodent visuomotor behavior. Behav Brain Res 3:133-149.
16. Garthe A, Behr J, Kempermann G. 2009. Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLoS One 4:e5464-
17. Ge S, Goh EL, Sailor KA, Kitabatake Y, Ming GL, Song H. 2006. GABA regulates synaptic integration of newly generated neurons in the adult brain. Nature 439:589-593.
18. Gibbs RA, Weinstock GM, Metzker ML, Muzny DM, Sodergren EJ, Scherer S, Scott G, Steffen D, Worley KC, Burch PE, Okwuonu G, Hines S, Lewis L, DeRamo C, Delgado O, Dugan-Rocha S, Miner G, Morgan M, Hawes A, Gill R, Celera Holt RA, Adams MD, Amanatides PG, Baden-Tillson H, Barnstead M, Chin S, Evans CA, Ferriera S, Fosler C, Glodek A, Gu Z, Jennings D, Kraft CL, Nguyen T, Pfannkoch CM, Sitter C, Sutton GG, Venter JC, Woodage T, Smith D, Lee HM, Gustafson E, Cahill P, Kana A, Doucette-Stamm L, Weinstock K, Fechtel K, Weiss RB, Dunn DM, Green ED, Blakesley RW, Bouffard GG, Jong D, Osoegawa PJ, Zhu K, Marra B, Schein M, Bosdet J, Fjell I, Jones C, Krzywinski S, Mathewson M, Siddiqui C, Wye A, McPherson N, Zhao J, Fraser S, Shetty CM, Shatsman J, Geer S, Chen K, Abramzon Y, Nierman S, Havlak WC, Chen PH, Durbin R, Egan KJ, Ren A, Song Y, Li XZ, Liu B, Qin Y, Cawley X, Worley S, Cooney KC, D'Souza AJ, Martin LM, Wu K, Gonzalez-Garay JQ, Jackson ML, Kalafus AR, McLeod KJ, Milosavljevic MP, Virk A, Volkov D, Wheeler A, Zhang DA, Bailey Z, Eichler JA, et al. 2004. Genome sequence of the brown norway rat yields insights into mammalian evolution. Nature 428:493-521.
19. Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ. 1999. Learning enhances adult neurogenesis in the hippocampal formation. Nat Neurosci 2:260-265.
20. Gross CG. 2000. Neurogenesis in the adult brain: Death of a dogma. Nat Rev Neurosci 1:67-73.
21. Haditsch U, Anderson MP, Freewoman J, Cord B, Babu H, Brakebusch C, Palmer TD. 2013. Neuronal rac1 is required for learning-evoked neurogenesis. J Neurosci 33:12229-12241.
22. Hairston IS, Little MT, Scanlon MD, Barakat MT, Palmer TD, Sapolsky RM, Heller HC. 2005. Sleep restriction suppresses neurogenesis induced by hippocampus-dependent learning. J Neurophysiol 94:4224-4233.
23. Harrison FE, Hosseini AH, McDonald MP. 2009. Endogenous anxiety and stress responses in water maze and barnes maze spatial memory tasks. Behav Brain Res 198:247-251.
24. Hendriksen H, Mechiel KS, Olivier B, Oosting RS. 2014. The olfactory bulbectomy model in mice and rat: One story or two tails? Eur J Pharmacol 7-11.
25. 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 10:355-362.
26. Koehl M, Abrous DN. 2011. A new chapter in the field of memory: Adult hippocampal neurogenesis. Eur J Neurosci 33:1101-1114.
27. Laplagne DA, Esposito MS, Piatti VC, Morgenstern NA, Zhao C, van Praag H, Gage FH, Schinder AF. 2006. Functional convergence of neurons generated in the developing and adult hippocampus. PLoS Biol 4:e409.
28. Lazic SE, Fuss J, Gass P. 2014. Quantifying the behavioural relevance of hippocampal neurogenesis. PLoS One 9:e113855.
29. Lemaire V, Tronel S, Montaron MF, Fabre A, Dugast E, Abrous DN. 2012. Long-lasting plasticity of hippocampal adult-born neurons. J Neurosci 32:3101-3108.
30. Lipp HP, Schwegler H, Heimrich B, Cerbone A, Sadile AG. 1987. Strain-specific correlations between hippocampal structural traits and habituation in a spatial novelty situation. Behav Brain Res 24:111-123.
31. Marin-Burgin A, Schinder AF. 2012. Requirement of adult-born neurons for hippocampus-dependent learning. Behav Brain Res 227:391-399.
32. Martin AL, Brown RE. 2010. The lonely mouse: Verification of a separation-induced model of depression in female mice. Behav Brain Res 207:196-207:
33. Mohapel P, Mundt-Petersen K, Brundin P, Frielingsdorf H. 2006. Working memory training decreases hippocampal neurogenesis. Neuroscience 142:609-613.
34. Morgenstern NA, Lombardi G, Schinder AF. 2008. Newborn granule cells in the ageing dentate gyrus. J Physiol 586:3751-3757.
35. Moser MB. 1999. Making more synapses: A way to store information? Cell Mol Life Sci 55:593-600.
36. Overstreet-Wadiche LS, Bromberg DA, Bensen AL, Westbrook GL. 2006. Seizures accelerate functional integration of adult-generated granule cells. J Neurosci 26:4095-4103.
37. Piatti VC, Davies-Sala MG, Esposito MS, Mongiat LA, Trinchero MF, Schinder AF. 2011. The timing for neuronal maturation in the adult hippocampus is modulated by local network activity. J Neurosci 31:7715-7728.
38. Ramirez-Amaya V, Balderas I, Sandoval J, Escobar ML, Bermudez-Rattoni F. 2001. Spatial long-term memory is related to mossy fiber synaptogenesis. J Neurosci 21:7340-7348.
39. Rekart JL, Sandoval CJ, Routtenberg A. 2007. Learning-induced axonal remodeling: evolutionary divergence and conservation of two components of the mossy fiber system within rodentia. Neurobiol Learn Mem 87:225-235.
40. Sahay A, Scobie KN, Hill AS, O'Carroll CM, Kheirbek MA, Burghardt NS, Fenton AA, Dranovsky A, Hen R. 2011. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472:466-470.
41. Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, Weisstaub N, Lee J, Duman R, Arancio O, Belzung C, Hen R. 2003. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301:805-809.
42. Shors TJ, Anderson ML, Curlik DM, Nokia MS. 2012. Use it or lose it: How neurogenesis keeps the brain fit for learning. Behav Brain Res 227:450-458.
43. Sisti HM, Glass AL, Shors TJ. 2007. Neurogenesis and the spacing effect: Learning over time enhances memory and the survival of new neurons. Learn Mem 14:368-375.
44. Snyder JS, Hong NS, McDonald RJ, Wojtowicz JM. 2005. A role for adult neurogenesis in spatial long-term memory. Neuroscience 130:843-852.
45. Snyder JS, Choe JS, Clifford MA, Jeurling SI, Hurley P, Brown A, Kamhi JF, Cameron HA. 2009. Adult-born hippocampal neurons are more numerous, faster maturing, and more involved in behavior in rats than in mice. J Neurosci 29:14484-14495.
46. Steib K, Schaffner I, Jagasia R, Ebert B, Lie DC. 2014. Mitochondria modify exercise-induced development of stem cell-derived neurons in the adult brain. J Neurosci 34:6624-6633.
47. Tronel S, Fabre A, Charrier V, Oliet SH, Gage FH, Abrous DN. 2010. Spatial learning sculpts the dendritic arbor of adult-born hippocampal neurons. Proc Natl Acad Sci USA 107:7963-7968.
48. Tronel S, Belnoue L, Grosgean N, Revest JM, Piazza PV, Koehl M, Abrous DN. 2012. Adult-born neurons are necessary for extended contextual discrimination. Hippocampus 22:292-298.
49. 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 106:5919-5924.
50. van Groen T, Kadish I, Wyss JM. 2002. Species differences in the projections from the entorhinal cortex to the hippocampus. Brain Res Bull 57:553-556.
51. van Praag H, Kempermann G, Gage FH. 1999. Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 2:266-270.
52. Whishaw IQ. 1995. A comparison of rats and mice in a swimming pool place task and matching to place task: Some surprising differences. Physiol Behav 58:687-693.
53. Whishaw IQ, Tomie J. 1996. Of mice and mazes: similarities between mice and rats on dry land but not water mazes. Physiol Behav 60:1191-1197.