An old test for new neurons: Refining the morris water maze to study the functional relevance of adult hippocampal neurogenesis

Frontiers in Neuroscience

Volumn , Issue 7 MAY, 2013, Pages

  Garthe, Alexander ^a,b   Kempermann, Gerd ^a,b  

^a GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^b CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

Author keywords

Adult neurogenesis; CA3; Dentate gyrus; Flexibility; Hippocampus; Pattern separation; Spatial learning; Water maze

Indexed keywords

BRAIN FUNCTION; CELL PROLIFERATION; DENTATE GYRUS; ENTORHINAL CORTEX; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; INFORMATION PROCESSING; MAZE TEST; MORRIS WATER MAZE; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHYSICAL ACTIVITY; PYRAMIDAL NERVE CELL; REVIEW; SPATIAL LEARNING; TASK PERFORMANCE; WORKING MEMORY;

EID: 84878859619     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2013.00063     Document Type: Review

References (54)

1. Aimone, J. B., Deng, W., and Gage, F. H. (2010). Adult neurogenesis: integrating theories and separating functions. Trends Cogn. Sci. 14, 325-337.
2. Aimone, J. B., Wiles, J., and Gage, F. H. (2006). Potential role for adult neurogenesis in the encoding of time in new memories. Nat. Neurosci. 9, 723-727.
3. Aimone, J. B., Wiles, J., and Gage, F. H. (2009). Computational influence of adult neurogenesis on memory encoding. Neuron 61, 187-202.
4. Amaral, D. G., and Witter, M. P. (1995). "Hippocampal Formation," in The Rat Nervous System, 2nd Edn., ed G. Paxinos (San Diego, CA: Academic Press), 443-493.
5. Anderson, P., Morris, R., Amaral, D., Bliss, T., and O'Keefe, J. (eds.). (2006). The Hippocampus Book. New York, NY: Oxford University Press.
6. Appleby, P. A., Kempermann, G., and Wiskott, L. (2011). The role of additive neurogenesis and synaptic plasticity in a hippocampal memory model with grid-cell like input. PLoS Comput. Biol. 7, e1001063. doi: 10.1371/journal.pcbi.1001063
7. Appleby, P. A., and Wiskott, L. (2009). Additive neurogenesis as a strategy for avoiding interference in a sparsely-coding dentate gyrus. Network 20, 137-161.
8. Clelland, C. D., Choi, M., Romberg, C., Clemenson, G. D., Fragniere, A., Tyers, P., et al. (2009). A functional role for adult hippocampal neurogenesis in spatial pattern separation. Science 325, 210-213.
9. Day, L. B., and Schallert, T. (1996). Anticholinergic effects on acquisition of place learning in the Morris water task: spatial mapping deficit or inability to inhibit nonplace strategies?. Behav. Neurosci. 110, 998-1005.
10. Deng, W., Aimone, J. B., and Gage, F. H. (2010). New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory?. Nat. Rev. Neurosci 11, 339-350.
11. Dräger, U. C., and Hubel, D. H. (1975). Responses to visual stimulation and relationship between visual, auditory, and somatosensory inputs in mouse superior colliculus. J. Neurophysiol. 38, 690-713.
12. Dupret, D., Revest, J.-M., Koehl, M., Ichas, F., De Giorgi, F., Costet, P., et al. (2008). Spatial relational memory requires hippocampal adult neurogenesis. PLoS ONE 3:e1959. doi: 10.1371/journal.pone.0001959
13. Eichenbaum, H., Stewart, C., and Morris, R. G. (1990). Hippocampal representation in place learning. J. Neurosci. 10, 3531-3542.
14. Ellard, C. G., and Goodale, M. A. (1988). A functional analysis of the collicular output pathways: a dissociation of deficits following lesions of the dorsal tegmental decussation and the ipsilateral collicular efferent bundle in the Mongolian gerbil. Exp. Brain Res. 71, 307-319.
15. Garthe, A., Behr, J., and Kempermann, G. (2009). Adult-generated hippocampal neurons allow the flexible use of spatially precise learning strategies. PLoS ONE 4:e5464. doi: 10.1371/journal.pone.0005464
16. Hill, A. J. (1978). First occurrence of hippocampal spatial firing in a new environment. Exp. Neurol. 62, 282-297.
17. Hunsaker, M. R., and Kesner, R. P. (2008). Evaluating the differential roles of the dorsal dentate gyrus, dorsal CA3, and dorsal CA1 during a temporal ordering for spatial locations task. Hippocampus 18, 955-964.
18. Jessberger, S., Clark, R. E., Broadbent, N. J., Clemenson, G. D., Consiglio, A., Lie, D. C., et al. (2009). Dentate gyrus-specific knockdown of adult neurogenesis impairs spatial and object recognition memory in adult rats. Learn. Mem. 16, 147-154.
19. Kee, N., Teixeira, C. M., Wang, A. H., and Frankland, P. W. (2007). Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat. Neurosci. 10, 355-362.
20. Kempermann, G. (2008). The neurogenic reserve hypothesis: what is adult hippocampal neurogenesis good for?. Trends Neurosci. 31, 163-169.
21. Kempermann, G. (2012). New neurons for "survival of the fittest". Nat. Rev. Neurosci. 13, 727-736.
22. Kempermann, G., Jessberger, S., Steiner, B., and Kronenberg, G. (2004). Milestones of neuronal development in the adult hippocampus. Trends Neurosci. 27, 447-452.
23. Kempermann G., Kuhn, H.-G., and Gage, F. H. (1997). More hippocampal neurons in adult mice living in an enriched environment. Nature 386, 493-495.
24. Kronenberg, G., Reuter, K., Steiner, B., Brandt, M. D., Jessberger, S., Yamaguchi, M., et al. (2003). Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. J. Comp. Neurol. 467, 455-463.
25. Leuner, B., Gould, E., and Shors, T. J. (2006). Is there a link between adult neurogenesis and learning. Hippocampus 16, 216-224.
26. Leuner, B., and Gould, E. (2010). Structural plasticity and hippocampal function. Annu. Rev. Psychol. 61, 111-140, C1-C3.
27. Marr, D. (1971). Simple memory: a theory for archicortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 262, 23-81.
28. Martinez-Canabal, A., Akers, K. G., Josselyn, S. A., and Frankland, P. W. (2013). Age-dependent effects of hippocampal neurogenesis suppression on spatial learning. Hippocampus 23, 66-74.
29. McNaughton, B. L., Barnes, C. A., Meltzer, J., and Sutherland, R. J. (1989). Hippocampal granule cells are necessary for normal spatial learning but not for spatially-selective pyramidal cell discharge. Exp. Brain Res. 76, 485-496.
30. Meshi, D., Drew, M. R., Saxe, M., Ansorge, M. S., David, D., Santarelli, L., et al. (2006). Hippocampal neurogenesis is not required for behavioral effects of environmental enrichment. Nat. Neurosci. 9, 729-731.
31. Morris, R. (1984). Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods 11, 47-60.
32. Morris, R. G., Garrud, P., Rawlins, J. N., and O'Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature 297, 681-683.
33. Nadel, L., and O'Keefe, J. (1978). The Hippocampus as a Cognitive Map. Oxford: Oxford University Press.
34. Redish, A. D. (1999). Beyond the Cognitive Map. London: MIT Press.
35. Rola, R., Raber, J., Rizk, A., Otsuka, S., VandenBerg, S. R., Morhardt, D. R., et al. (2004). Radiation-induced impairment of hippocampal neurogenesis is associated with cognitive deficits in young mice. Exp. Neurol. 188, 316-330.
36. Rolls, E. T. (1996). A theory of hippocampal function in memory. Hippocampus 6, 601-620.
37. Rolls, E. T. (2010). A computational theory of episodic memory formation in the hippocampus. Behav. Brain Res. 215, 180-196.
38. Saxe, M. D., Malleret, G., Vronskaya, S., Mendez, I., Garcia, A. D., Sofroniew, M. V., et al. (2007). Paradoxical influence of hippocampal neurogenesis on working memory. Proc. Natl. Acad. Sci. U.S.A. 104, 4642-4646.
39. Shapiro, M. L., Tanila, H., and Eichenbaum, H. (1997). Cues that hippocampal place cells encode: dynamic and hierarchical representation of local and distal stimuli. Hippocampus 7, 624-642.
40. Shors, T. J., Townsend, D. A., Zhao, M., Kozorovitskiy, Y., and Gould, E. (2002). Neurogenesis may relate to some but not all types of hippocampal-dependent learning. Hippocampus 12, 578-584.
41. Snyder, J. S., Hong, N. S., McDonald, R. J., and Wojtowicz, J. M. (2005). A role for adult neurogenesis in spatial long-term memory. Neuroscience 130, 843-852.
42. Steiner, B., Zurborg, S., Hörster, H., Fabel, K., and Kempermann, G. (2008). Differential 24 h responsiveness of Prox1-expressing precursor cells in adult hippocampal neurogenesis to physical activity, environmental enrichment, and kainic acid-induced seizures. Neuroscience 154, 521-529.
43. Sutherland, R. J., and Hoesing, J. (1993). Neurobiology of Cingulate Cortex and Limbic Thalamus. Boston: Birkhäuser.
44. Treves, A., Tashiro, A., Witter, M. E., and Moser, E. I. (2008). What is the mammalian dentate gyrus good for? Neuroscience 154, 1155-1172.
45. Tronel, S., Fabre, A., Charrier, V., Oliet, S. H. R., Gage, F. H., and Abrous, D. N. (2010). Spatial learning sculpts the dendritic arbor of adult-born hippocampal neurons. Proc. Natl. Acad. Sci. U.S.A. 107, 7963-7968.
46. Van Praag, H., Kempermann, G., and Gage, F. H. (1999). Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat. Neurosci. 2, 266-270.
47. Winocur, G., Wojtowicz, J. M., Sekeres, M., Snyder, J. S., and Wang, S. (2006). Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus 16, 296-304.
48. Wiskott, L., Rasch, M. J., and Kempermann, G. (2006). A functional hypothesis for adult hippocampal neurogenesis: avoidance of catastrophic interference in the dentate gyrus. Hippocampus 16, 329-343.
49. Wolbers, T., and Hegarty, M. (2010). What determines our navigational abilities? Trends Cogn. Sci. 14, 138-146.
50. Wolfer, D. P., Madani, R., Valenti, P., and Lipp, H. P. (2001). Extended analysis of path data from mutant mice using the public domain software Wintrack. Physiol. Behav. 73, 745-753.
51. Woolley, D. G., Vermaercke, B., Op de Beeck, H., Wagemans, J., Gantois, I., D'Hooge, R., et al. (2010). Sex differences in human virtual water maze performance: novel measures reveal the relative contribution of directional responding and spatial knowledge. Behav. Brain Res. 208, 408-414.
52. Wu, K., and Leung, L. S. (1998). Monosynaptic activation of CA3 by the medial perforant path. Brain Res. 797, 35-41.
53. Zhang, C.-L., Zou, Y., He, W., Gage, F. H., and Evans, R. M. (2008). A role for adult TLX-positive neural stem cells in learning and behaviour. Nature 451, 1004-1007.
54. Zhao, C., Deng, W., and Gage, F. H. (2008). Mechanisms and functional implications of adult neurogenesis. Cell 132, 645-660.