What is the functional role of adult neurogenesis in the hippocampus?

Wiskott, Laurenz and Rasch, Malte J. and Kempermann, Gerd (2004) What is the functional role of adult neurogenesis in the hippocampus? [Preprint]

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The dentate gyrus is part of the hippocampal memory system and special in that it generates new neurons throughout life. Here we discuss the question of what the functional role of these new neurons might be. Our hypothesis is that they help the dentate gyrus to avoid the problem of catastrophic interference when adapting to new environments. We assume that old neurons are rather stable and preserve an optimal encoding learned for known environments while new neurons are plastic to adapt to those features that are qualitatively new in a new environment. A simple network simulation demonstrates that adding new plastic neurons is indeed a successful strategy for adaptation without catastrophic interference.

Item Type:Preprint
Keywords:hippocampus, dentate gyrus, adult neurogenesis, network model, catastrophic interference
Subjects:Biology > Animal Cognition
Computer Science > Neural Nets
Biology > Theoretical Biology
ID Code:4012
Deposited By:Wiskott, Laurenz
Deposited On:30 Dec 2004
Last Modified:11 Mar 2011 08:55

References in Article

Select the SEEK icon to attempt to find the referenced article. If it does not appear to be in cogprints you will be forwarded to the paracite service. Poorly formated references will probably not work.

Abraham, W. C. and Williams, J. M. (2003). Properties and mechanisms of LTP maintenance. Neuroscientist, 9(6):463­474.

Altman, J. and Das, G. D. (1965). Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. The Journal of Comparative Neurology, 124:319­335.

Amaral, D. G., Ishizuka, N., and Claiborne, B. J. (1990). Neurons, numbers and the hippocampal network. Progress in Brain Research, 83:1­11.

Amaral, D. G. and Witter, M. P. (1989). The three-dimensional organization of the hippocampal formation: A review of anatomical data. Neuroscience, 31(3):571­591.

Amit, D. J. (1989). Modeling Brain Function: The World of Attractor Neural Networks. Cambridge University Press.

Ans, B. and Rousset, S. (1997). Avoiding catastrophic forgetting by coupling two reverberating neural networks. Comptes Rendus de l'Académie des Sciences - Series III - Sciences de la Vie, 320(12):989­997.

Barnes, C. A., McNaughton, B. L., Mizumori, S. J., Leonard, B. W., and Lin, L. H. (1990). Comparison of spatial and temporal characteristics of neuronal activity in sequential stages of hippocampal processing. Progress in Brain Research, 83:287­300.

Bentz, H. J., Hagstroem, M., and Palm, G. (1989). Information storage and effective data retrieval in sparse matrices. Neural Networks, 2:289­293.

Bishop, C. M. (1995). Neural Networks for Pattern Recognition. Oxford University Press.

Borisyuk, R., Denham, M., Denham, S., and Hoppensteadt, F. (1999). Computational models of predictive and memory-related functions of the hippocampus. Reviews in the Neurosciences, 10(3-4):213­232.

Buzsáki, G. (2002). Theta oscillations in the hippocampus. Neuron, 33:325­340.

Cameron, H. A. and McKay, R. D. (2001). Adult neurogenesis produces a large pool of new granule cells in the dentate gyrus. The Journal of Comparative Neurology, 435(4):406­417.

Carleton, A., Rochefort, C., Morante-Oria, J., Desmaisons, D., Vincent, J.-D., Gheusi, G., and Lledo, P.-M. (2002). Making scents of olfactory neurogenesis. J. Neurophysiology - Paris, 96:115-122.

Carpenter, G. A. and Grossberg, S. (1987). ART 2: Self-organization of stable category recognition codes for analog input patterns. Applied Optics, 26:4919­4930.

Carpenter, G. A., Grossberg, S., and Rosen, D. B. (1991). ART 2-A; an adaptive resonance algorithm for rapid category learning and recognition. Neural Networks, 4(4):493­504.

Cecchi, G. A., Petreanu, L. T., Alvarez-Buylla, A., and Magnasco, M. O. (2001). Unsupervised learning and adaptation in a model of adult neurogenesis. The Journal of Computational Neuroscience, 11(2):175­182.

Chrobak, J. J. and Buzsáki, G. (1998). Operational dynamics in the hippocampal-entorhinal axis. Neuroscience & Biobehavioral Reviews, 22(2):303­310.

Chrobak, J. J., Lörincz, A., and Buzsáki, G. (2000). Physiological patterns in the hippocampo-entorhinal cortex system. Hippocampus, 10(4):457­465.

Deisseroth, K., Singla, S., Toda, H., Monje, M., Palmer, T. D., and Malenka, R. C. (2004). Excitation-neurogenesis coupling in adult neural stem/progenitor cells. Neuron, 42(4):535­552.

D'Hooge, R. and De Deyn, P. P. (2001). Applications of the morris water maze in the study of learning and memory. Brain Research Reviews, 36(1):60­90.

Dudek, S. M. and Bear, M. F. (1992). Homosynaptic long-term depression in area CA1 of hippocampus and effects of N-methyl-D-aspartate receptor blockade. Proceedings of the National Academy of Sciences of the United States of America, 89(10):4363­4367.

Eriksson, P. S., Perfilieva, E., Bjork-Eriksson, T., Alborn, A. M., Nordborg, C., Peterson, D. A., and Gage, F. H. (1998). Neurogenesis in the adult human hippocampus. Nature Medicine, 4(11):1313­1317.

Fahlman, S. E. and Lebiere, C. (1990). The cascade-correlation learning architecture. In Touretzky, D., editor, Advances in Neural Information Processing Systems 2 (NIPS'1989), pages 524­532. Morgan-Kaufmann.

French, R. M. (1997). Pseudo-recurrent connectionist networks: An approach to the "sensitivity-stability" dilemma. Connection Science, 9:353­379.

Freund, T. F. and Buzsáki, G. (1996). Interneurons of the hippocampus. Hippocampus, 6(4):347­470.

Fritzke, B. (1994). Growing cell structures - a self-organizing network for unsupervised and supervised learning. Neural Networks, 7(9):1441­1460.

Geman, S., Bienenstock, E., and Doursat, R. (1992). Neural networks and the bias/variance dilemma. Neural Computation, 4(1):1­58.

Gerstner, W. and Kistler, W. (2002). Spiking Neuron Models. Cambridge University Press.

Gluck, M. A. and Myers, C. E. (2001). Gateway to memory. MIT Press.

Gould, E., Beylin, A., Tanapat, P., Reeves, A., and Shors, T. J. (1999). Learning enhances adult neurogenesis in the hippocampal formation. Nature Neuroscience, 2(3):260­265.

Gould, E. and Gross, C. G. (2002). Neurogenesis in adult mammals: some progress and problems. The Journal of Neuroscience, 22(3):619­623.

Gould, E., McEwen, B. S., Tanapat, P., Galea, L. A., and Fuchs, E. (1997). Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. The Journal of Neuroscience, 17(7):2492­2498.

Gould, E., Tanapat, P., McEwen, B. S., Flugge, G., and Fuchs, E. (1998). Proliferation of granule cell precursors in the dentate gyrus of adult monkeys is diminished by stress. Proceedings of the National Academy of Sciences of the United States of America, 95(6):3168­3171.

Gould, E., Vail, N., Wagers, M., and Gross, C. G. (2001). Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proceedings of the National Academy of Sciences of the United States of America, 98(19):10910­10917.

Hammond, C. (2001). Cellular and molecular neurobiology. Academic Press, San Diego.

Harding, A. J., Halliday, G. M., and Kril, J. J. (1998). Variation in hippocampal neuron number with age and brain volume. Cerebral Cortex, 8(8):710­718.

Henze, D. A., Urban, N. N., and Barrionuevo, G. (2000). The multifarious hippocamal mossy fiber pathway: a review. Neuroscience, 98(3):407­427.

Hertz, J., Krogh, A., and Palmer, R. G. (1991). Introduction to the Theory of Neural Computation. Addison-Wesley, Redwood City, CA.

Hölscher, C. (1999). Synaptic plasticity and learning and memory: LTP and beyond. Journal of Neuroscience Research, 58(1):62­75.

Howard, R. E., Schwartz, D., Denker, J. S., Epworth, R. W., Graf, H. P., Hubbard, W. E., Jackel, L. D., Straughn, B. L., and Tennant, D. M. (1987). An associative memory based on an electronic neural network architecture. IEEE Trans. ED, 34:1553.

Jessberger, S. and Kempermann, G. (2003). Adult-born hippocampal neurons mature into activity-dependent responsiveness. European Journal of Neuroscience, 18(10):2707­2712.

Jones, S. and Yakel, J. L. (1999). Inhibitory interneurons in hippocampus. Cell Biochem. Biophys., 31(2):207­218.

Jung, M. W. and McNaughton, B. L. (1993). Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus, 3(2):165­182.

Kandel, E. R. (2000). Cellular mechanisms of learning and the biological basis of individuality. In Kandel, E. R., Schwartz, J. H., and Jessel, T. M., editors, Principles of Neural Science, chapter 63. McGraw-Hill.

Kempermann, G. and Gage, F. H. (2002). Genetic determinants of adult hippocampal neurogenesis correlate with acquisition, but not probe trial performance, in the water maze task. European Journal of Neuroscience, 16(1):129­136.

Kempermann, G., Gast, D., Kronenberg, G., Yamaguchi, M., and Gage, F. H. (2003). Early determination and long-term persistence of adult-generated new neurons in the hippocampus of mice. Development, 130(2):391­399.

Kempermann, G. and Kronenberg, G. (2003). Depressed new neurons? - Adult hippocampal neurogenesis and a cellular plasticity hypothesis of major depression. Biological Psychiatry, 54(5):499­503.

Kempermann, G., Kuhn, H. G., and Gage, F. H. (1997). Genetic influence on neurogenesis in the dentate gyrus of adult mice. Proceedings of the National Academy of Sciences of the United States of America, 94(19):10409­10414.

Kempermann, G., Kuhn, H. G., and Gage, F. H. (1998). Experience-induced neurogenesis in the senescent dentate gyrus. The Journal of Neuroscience, 18(9):3206­3212.

Kempermann, G. and Wiskott, L. (2004). What is the functional role of new neurons in the adult dentate gyrus? In Gage, F. H., Björklund, A., Prochiantz, A., and Christen, Y., editors, Proc. Stem Cells in the Nervous System: Functional and Clinical Implications, Paris, January 20, 2003, Research and Perspectives in Neurosciences (Fondation Ipsen), pages 57­65, Berlin. Springer.

Kempermann, G., Wiskott, L., and Gage, F. H. (2004). Functional significance of adult neurogenesis. Curr. Opin. Neurobiol., 14:186­191.

Kronenberg, G., Reuter, K., Steiner, B., Brandt, M. D., Jessberger, S., Yamaguchi, M., and Kempermann, G. (2003). Subpopulations of proliferating cells of the adult hippocampus respond differently to physiologic neurogenic stimuli. The Journal of Comparative Neurology, 467(4):455­463.

Lavenex, P. and Amaral, D. G. (2000). Hippocampal-neocortical interaction: a hierarchy of associativity. Hippocampus, 10(4):420­430.

Lee, J. H., Duan, W., Long, J. M., Ingram, D. K., and Mattson, M. P. (2000). Dietary restriction increases the number of newly generated neural cells, and induces BDNF expression, in the dentate gyrus of rats. Journal of Molecular Neuroscience, 15(2):99­108.

Martin, S. J. and Morris, R. G. (2002). New life in an old idea: the synaptic plasticity and memory hypothesis revisited. Hippocampus, 12(5):609­636.

McClelland, J. L., McNaughton, B. L., and O'Reilly, R. C. (1995). Why there are complementary learning systems in the hippocampus and neocortex: Insights from the successes and failures of connectionist models of learning and memory. Psychological Review, 102(3):419­457.

McCloskey, M. and Cohen, N. J. (1989). Catastrophic interference in connectionist networks: The sequential learning problem. In Bower, G. H., editor, The psychology of learning and motivation, volume 24, pages 109­165. Academic Press, New York.

Morris, R. G., Garrud, P., Rawlins, J. N., and O'Keefe, J. (1982). Place navigation impaired in rats with hippocampal lesions. Nature, 297(5868):681­683.

Moser, E. I. and Paulsen, O. (2001). New excitement in cognitive space: between place cells and spatial memory. Current Opinion in Neurobiology, 11(6):745­751.

Nadel, L. and Moscovitch, M. (1997). Memory consolidation, retrograde amnesia and the hippocampal complex. Current Opinion in Neurobiology, 7(2):217­227.

Nilsson, M., Perfilieva, E., Johansson, U., Orwar, O., and Eriksson, P. S. (1999). Enriched environment increases neurogenesis in the adult rat dentate gyrus and improves spatial memory. Journal of Neurobiology, 39(4):569­578.

O'Keefe, J. (1979). A review of the hippocampal place cells. Progress in Neurobiology, 13(4):419­439.

O'Reilly, R. C. and McClelland, J. L. (1994). Hippocampal conjunctive encoding, storage, and recall: avoiding a trade-off. Hippocampus, 4(6):661­682.

Patton, P. E. and McNaughton, B. L. (1995). Connection matrix of the hippocampal formation: I. The dentate gyrus. Hippocampus, 5(4):245­286.

Rasch, M. (2003). Modellierung adulter Neurogenese im Hippocampus [Modeling adult neurogenesis in the hippocampus]. Diploma thesis, Institute for Biology, Humboldt University Berlin, D-10115 Berlin, Germany.

Rolls, E. T. (1999). Spatial view cells and the representation of place in the primate hippocampus. Hippocampus, 9(4):467­480.

Santarelli, L., Saxe, M., Gross, C. G., Surget, A., Battaglia, F. P., Dulawa, S., Weisstaub, N., Lee, J. H., Duman, R., Arancio, O., Belzung, C., and Hen, R. (2003). Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science, 301(5634):805­809.

Schmidt-Hieber, C., Jonas, P., and Bischofberger, J. (2004). Enhanced synaptic plasticity in newly generated granule cells of the adult hippocampus. Nature, 429(6988):184­187.

Seki, T. and Arai, Y. (1995). Age-related production of new granule cells in the adult dentate gyrus. NeuroReport, 6(18):2479­2482.

Shors, T. J., Miesegaes, G., Beylin, A., Zhao, M., Rydel, T. A., and Gould, E. (2001). Neurogenesis in the adult is involved in the formation of trace memories. Nature, 410:372­376.

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(5):578­584.

Snyder, J. S., Kee, N., and Wojtowicz, J. M. (2001). Effects of adult neurogenesis on synaptic plasticity in the rat dentate gyrus. Journal of Neurophysiology, 85(6):2423­2431.

Sutherland, G. R. and McNaughton, B. L. (2000). Memory trace reactivation in hippocampal and neocortical neuronal ensembles. Current Opinion in Neurobiology, 10(2):180­186.

Tanapat, P., Hastings, N. B., Rydel, T. A., Galea, L. A., and Gould, E. (2001). Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. The Journal of Comparative Neurology, 437(4):496­504.

Treves, A. and Rolls, E. T. (1992). Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network. Hippocampus, 2(2):189­199.

Treves, A. and Rolls, E. T. (1994). Computational analysis of the role of the hippocampus in memory. Hippocampus, 4(3):374­391.

Urban, N. N., Henze, D. A., and Barrionuevo, G. (2001). Revisiting the role of the hippocampal mossy fiber synapse. Hippocampus, 11(4):408­417.

van Praag, H., Christie, B. R., Sejnowski, T. J., and Gage, F. H. (1999a). Running enhances neurogenesis, learning, and long-term potentiation in mice. Proceedings of the National Academy of Sciences of the United States of America, 96(23):13427­13431.

van Praag, H., Kempermann, G., and Gage, F. H. (1999b). Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nature Neuroscience, 2(3):266­270.

van Praag, H., Schinder, A. F., Christie, B. R., Toni, N., Palmer, T. D., and Gage, F. H. (2002). Functional neurogenesis in the adult hippocampus. Nature, 415(6875):1030­1034.

Wang, S.-S., Scott, B. W., and Wojtowicz, J. M. (2000). Heterogenous properties of dentate granule neurons in the adult rat. Journal of Neurobiology, 42(2):248­257.

West, M. J. and Slomianka, L. (1998). Total number of neurons in the layers of the human entorhinal cortex. (and corrigendum). Hippocampus, 8:69­82 (and 426).

Witter, M. P. (1993). Organization of the entorhinal-hippocampal system: a review of current anatomical data. Hippocampus, 3(Spec. No.):33­44.

Witter, M. P., Naber, P. A., van Haeften, T., Machielsen, W. C., Rombouts, S. A., Barkhof, F., Scheltens, P., and Lopes da Silva, F. H. (2000). Cortico- hippocampal communication by way of parallel parahippocampal-subicular pathways. Hippocampus, 10(4):398­410.


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