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Neural Plasticity
Volume 2008, Article ID 269097, 12 pages
http://dx.doi.org/10.1155/2008/269097
Research Article

Object-Place Recognition Learning Triggers Rapid Induction of Plasticity-Related Immediate Early Genes and Synaptic Proteins in the Rat Dentate Gyrus

1Department of Biomedicine and Bergen Mental Health Research Center, University of Bergen, Jonas Lies vei 91, 5009 Bergen, Norway
2CNRS, Université Paris-Sud, UMR 8620, Laboratoire de Neurobiologie de l’Apprentissage, de la Mémoire et de la Communication, 91405 Orsay Cedex, France

Received 2 September 2008; Accepted 22 October 2008

Academic Editor: Michael Stewart

Copyright © 2008 Jonathan Soulé et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. N. Bourne and K. M. Harris, “Balancing structure and function at hippocampal dendritic spines,” Annual Review of Neuroscience, vol. 31, no. 1, pp. 47–67, 2008. View at Publisher · View at Google Scholar
  2. M. Segal, “Dendritic spines and long-term plasticity,” Nature Reviews Neuroscience, vol. 6, no. 4, pp. 277–284, 2005. View at Publisher · View at Google Scholar
  3. C. R. Bramham, “Local protein synthesis, actin dynamics, and LTP consolidation,” Current Opinion in Neurobiology, vol. 18, no. 5, pp. 524–531, 2008. View at Publisher · View at Google Scholar
  4. T. Tada and M. Sheng, “Molecular mechanisms of dendritic spine morphogenesis,” Current Opinion in Neurobiology, vol. 16, no. 1, pp. 95–101, 2006. View at Publisher · View at Google Scholar
  5. M. Matsuzaki, “Factors critical for the plasticity of dendritic spines and memory storage,” Neuroscience Research, vol. 57, no. 1, pp. 1–9, 2007. View at Publisher · View at Google Scholar
  6. J. F. Guzowski, G. L. Lyford, G. D. Stevenson et al., “Inhibition of activity-dependent arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory,” The Journal of Neuroscience, vol. 20, no. 11, pp. 3993–4001, 2000. View at Google Scholar
  7. N. Plath, O. Ohana, B. Dammermann et al., “Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories,” Neuron, vol. 52, no. 3, pp. 437–444, 2006. View at Publisher · View at Google Scholar
  8. B. Bozon, S. Davis, and S. Laroche, “A requirement for the immediate early gene zif268 in reconsolidation of recognition memory after retrieval,” Neuron, vol. 40, no. 4, pp. 695–701, 2003. View at Publisher · View at Google Scholar
  9. M. W. Jones, M. L. Errington, P. J. French et al., “A requirement for the immediate early gene Zif268 in the expression of late LTP and long-term memories,” Nature Neuroscience, vol. 4, no. 3, pp. 289–296, 2001. View at Publisher · View at Google Scholar
  10. O. Steward, C. S. Wallace, G. L. Lyford, and P. F. Worley, “Synaptic activation causes the mRNA for the IEG Arc to localize selectively near activated postsynaptic sites on dendrites,” Neuron, vol. 21, no. 4, pp. 741–751, 1998. View at Publisher · View at Google Scholar
  11. W. Link, U. Konietzko, G. Kauselmann et al., “Somatodendritic expression of an immediate early gene is regulated by synaptic activity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 92, no. 12, pp. 5734–5738, 1995. View at Publisher · View at Google Scholar
  12. G. L. Lyford, K. Yamagata, W. E. Kaufmann et al., “Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites,” Neuron, vol. 14, no. 2, pp. 433–445, 1995. View at Publisher · View at Google Scholar
  13. E. Messaoudi, T. Kanhema, J. Soulé et al., “Sustained Arc/Arg3.1 synthesis controls long-term potentiation consolidation through regulation of local actin polymerization in the dentate gyrus in vivo,” The Journal of Neuroscience, vol. 27, no. 39, pp. 10445–10455, 2007. View at Publisher · View at Google Scholar
  14. S. Chowdhury, J. D. Shepherd, H. Okuno et al., “Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking,” Neuron, vol. 52, no. 3, pp. 445–459, 2006. View at Publisher · View at Google Scholar
  15. J. D. Shepherd, G. Rumbaugh, J. Wu et al., “Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors,” Neuron, vol. 52, no. 3, pp. 475–484, 2006. View at Publisher · View at Google Scholar
  16. C. R. Bramham, P. F. Worley, M. J. Moore, and J. F. Guzowski, “The immediate early gene Arc/Arg3.1: regulation, mechanisms, and function,” The Journal of Neuroscience, vol. 28, no. 46, pp. 11760–11767, 2008. View at Publisher · View at Google Scholar
  17. A. R. Pfenning, R. Schwartz, and A. L. Barth, “A comparative genomics approach to identifying the plasticity transcriptome,” BMC Neuroscience, vol. 8, article 20, pp. 1–18, 2007. View at Publisher · View at Google Scholar
  18. L. Li, J. Carter, X. Gao, J. Whitehead, and W. G. Tourtellotte, “The neuroplasticity-associated Arc gene is a direct transcriptional target of early growth response (Egr) transcription factors,” Molecular and Cellular Biology, vol. 25, no. 23, pp. 10286–10300, 2005. View at Publisher · View at Google Scholar
  19. S. Davis, B. Bozon, and S. Laroche, “How necessary is the activation of the immediate early gene zif 268 in synaptic plasticity and learning?” Behavioural Brain Research, vol. 142, no. 1-2, pp. 17–30, 2003. View at Publisher · View at Google Scholar
  20. E. Knapska and L. Kaczmarek, “A gene for neuronal plasticity in the mammalian brain: Zif268/Egr-1/NGFI-A/ Krox-24/TIS8/ZENK?” Progress in Neurobiology, vol. 74, no. 4, pp. 183–211, 2004. View at Publisher · View at Google Scholar
  21. S. Kubik, T. Miyashita, and J. F. Guzowski, “Using immediate-early genes to map hippocampal subregional functions,” Learning and Memory, vol. 14, no. 11, pp. 758–770, 2007. View at Publisher · View at Google Scholar
  22. S. Linnarsson, A. Björklund, and P. Ernfors, “Learning deficit in BDNF mutant mice,” European Journal of Neuroscience, vol. 9, no. 12, pp. 2581–2587, 1997. View at Publisher · View at Google Scholar
  23. L. Minichiello, M. Korte, D. Wolfer et al., “Essential role for TrkB receptors in hippocampus-mediated learning,” Neuron, vol. 24, no. 2, pp. 401–414, 1999. View at Publisher · View at Google Scholar
  24. C. R. Bramham and E. Messaoudi, “BDNF function in adult synaptic plasticity: the synaptic consolidation hypothesis,” Progress in Neurobiology, vol. 76, no. 2, pp. 99–125, 2005. View at Publisher · View at Google Scholar
  25. W. J. Tyler, M. Alonso, C. R. Bramham, and L. D. Pozzo-Miller, “From acquisition to consolidation: on the role of brain-derived neurotrophic factor signaling in hippocampal-dependent learning,” Learning and Memory, vol. 9, no. 5, pp. 224–237, 2002. View at Publisher · View at Google Scholar
  26. M. Alonso, M. R. M. Vianna, A. M. Depino et al., “BDNF-triggered events in the rat hippocampus are required for both short- and long-term memory formation,” Hippocampus, vol. 12, no. 4, pp. 551–560, 2002. View at Publisher · View at Google Scholar
  27. J. I. Rossato, L. R. M. Bevilaqua, J. C. Myskiw, J. H. Medina, I. Izquierdo, and M. Cammarota, “On the role of hippocampal protein synthesis in the consolidation and reconsolidation of object recognition memory,” Learning and Memory, vol. 14, no. 1, pp. 36–46, 2007. View at Publisher · View at Google Scholar
  28. P. Bekinschtein, M. Cammarota, L. M. Igaz, L. R. M. Bevilaqua, I. Izquierdo, and J. H. Medina, “Persistence of long-term memory storage requires a late protein synthesis- and BDNF- dependent phase in the hippocampus,” Neuron, vol. 53, no. 2, pp. 261–277, 2007. View at Publisher · View at Google Scholar
  29. P. Bekinschtein, M. Cammarota, C. Katche et al., “BDNF is essential to promote persistence of long-term memory storage,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 7, pp. 2711–2716, 2008. View at Publisher · View at Google Scholar
  30. K. Wibrand, E. Messaoudi, B. Håvik et al., “Identification of genes co-upregulated with Arc during BDNF-induced long-term potentiation in adult rat dentate gyrus in vivo,” European Journal of Neuroscience, vol. 23, no. 6, pp. 1501–1511, 2006. View at Publisher · View at Google Scholar
  31. R. J. O'Brien, D. Xu, R. S. Petralia, O. Steward, R. L. Huganir, and P. Worley, “Synaptic clustering of AMPA receptors by the extracellular immediate- early gene product Narp,” Neuron, vol. 23, no. 2, pp. 309–323, 1999. View at Publisher · View at Google Scholar
  32. R. O'Brien, D. Xu, R. Mi, X. Tang, C. Hopf, and P. Worley, “Synaptically targeted Narp plays an essential role in the aggregation of AMPA receptors at excitatory synapses in cultured spinal neurons,” The Journal of Neuroscience, vol. 22, no. 11, pp. 4487–4498, 2002. View at Google Scholar
  33. D. Xu, C. Hopf, R. Reddy et al., “Narp and NP1 form heterocomplexes that function in developmental and activity-dependent synaptic plasticity,” Neuron, vol. 39, no. 3, pp. 513–528, 2003. View at Publisher · View at Google Scholar
  34. S.-W. Ying, M. Futter, K. Rosenblum et al., “Brain-derived neurotrophic factor induces long-term potentiation in intact adult hippocampus: requirement for ERK activation coupled to CREB and upregulation of Arc synthesis,” The Journal of Neuroscience, vol. 22, no. 5, pp. 1532–1540, 2002. View at Google Scholar
  35. A. Ennaceur and J. Delacour, “A new one-trial test for neurobiological studies of memory in rats. 1: behavioral data,” Behavioural Brain Research, vol. 31, no. 1, pp. 47–59, 1988. View at Publisher · View at Google Scholar
  36. E. R. Wood, D. G. Mumby, J. P. J. Pinel, and A. G. Phillips, “Impaired object recognition memory in rats following ischemia-induced damage to the hippocampus,” Behavioral Neuroscience, vol. 107, no. 1, pp. 51–62, 1993. View at Publisher · View at Google Scholar
  37. K. A. Wiig and D. K. Bilkey, “Lesions of rat perirhinal cortex exacerbate the memory deficit observed following damage to the fimbria-fornix,” Behavioral Neuroscience, vol. 109, no. 4, pp. 620–630, 1995. View at Publisher · View at Google Scholar
  38. L. R. Squire, J. T. Wixted, and R. E. Clark, “Recognition memory and the medial temporal lobe: a new perspective,” Nature Reviews Neuroscience, vol. 8, no. 11, pp. 872–883, 2007. View at Publisher · View at Google Scholar
  39. R. E. Clark, A. N. West, S. M. Zola, and L. R. Squire, “Rats with lesions of the hippocampus are impaired on the delayed nonmatching-to-sample task,” Hippocampus, vol. 11, no. 2, pp. 176–186, 2001. View at Publisher · View at Google Scholar
  40. S. Gaskin, A. Tremblay, and D. G. Mumby, “Retrograde and anterograde object recognition in rats with hippocampal lesions,” Hippocampus, vol. 13, no. 8, pp. 962–969, 2003. View at Publisher · View at Google Scholar
  41. A. Kelly, S. Laroche, and S. Davis, “Activation of mitogen-activated protein kinase/extracellular signal-regulated kinase in hippocampal circuitry is required for consolidation and reconsolidation of recognition memory,” The Journal of Neuroscience, vol. 23, no. 12, pp. 5354–5360, 2003. View at Google Scholar
  42. C. Pittenger, Y. Y. Huang, R. F. Paletzki et al., “Reversible inhibition of CREB/ATF transcription factors in region CA1 of the dorsal hippocampus disrupts hippocampus-dependent spatial memory,” Neuron, vol. 34, no. 3, pp. 447–462, 2002. View at Publisher · View at Google Scholar
  43. B. Bozon, Á. Kelly, S. A. Josselyn, A. J. Silva, S. Davis, and S. Laroche, “MAPK, CREB and zif268 are all required for the consolidation of recognition memory,” Philosophical Transactions of the Royal Society B, vol. 358, no. 1432, pp. 805–814, 2003. View at Publisher · View at Google Scholar
  44. B. Bozon, S. Davis, and S. Laroche, “Regulated transciption of the immediate-early gene Zif268: mechanisms and gene dosage-dependent function in synaptic plasticity and memory formation,” Hippocampus, vol. 12, no. 5, pp. 570–577, 2002. View at Publisher · View at Google Scholar
  45. L. Li, S. H. Yun, J. Keblesh et al., “Egr3, a synaptic activity regulated transcription factor that is essential for learning and memory,” Molecular and Cellular Neuroscience, vol. 35, no. 1, pp. 76–88, 2007. View at Publisher · View at Google Scholar
  46. T. A. Jenkins, E. Amin, J. M. Pearce, M. W. Brown, and J. P. Aggleton, “Novel spatial arrangements of familiar visual stimuli promote activity in the rat hippocampal formation but not the parahippocampal cortices: a c-fos expression study,” Neuroscience, vol. 124, no. 1, pp. 43–52, 2004. View at Publisher · View at Google Scholar
  47. H. Husi, M. A. Ward, J. S. Choudhary, W. P. Blackstock, and S. G. N. Grant, “Proteomic analysis of NMDA receptor-adhesion protein signaling complexes,” Nature Neuroscience, vol. 3, no. 7, pp. 661–669, 2000. View at Publisher · View at Google Scholar
  48. D. E. Moga, M. E. Calhoun, A. Chowdhury, P. Worley, J. H. Morrison, and M. L. Shapiro, “Activity-regulated cytoskeletal-associated protein is localized to recently activated excitatory synapses,” Neuroscience, vol. 125, no. 1, pp. 7–11, 2004. View at Publisher · View at Google Scholar
  49. J. J. Rodriguez, H. A. Davies, A. T. Silva et al., “Long-term potentiation in the rat dentate gyrus is associated with enhanced Arc/Arg3.1 protein expression in spines, dendrites and glia,” European Journal of Neuroscience, vol. 21, no. 9, pp. 2384–2396, 2005. View at Publisher · View at Google Scholar
  50. C. Bats, L. Groc, and D. Choquet, “The interaction between stargazin and PSD-95 regulates AMPA receptor surface trafficking,” Neuron, vol. 53, no. 5, pp. 719–734, 2007. View at Publisher · View at Google Scholar
  51. I. Ehrlich and R. Malinow, “Postsynaptic density 95 controls AMPA receptor incorporation during long-term potentiation and experience-driven synaptic plasticity,” The Journal of Neuroscience, vol. 24, no. 4, pp. 916–927, 2004. View at Publisher · View at Google Scholar
  52. E. Kim, K.-O. Cho, A. Rothschild, and M. Sheng, “Heteromultimerization and NMDA receptor-clustering activity of Chapsyn-110, a member of the PSD-95 family of proteins,” Neuron, vol. 17, no. 1, pp. 103–113, 1996. View at Publisher · View at Google Scholar
  53. J. E. Lisman and A. M. Zhabotinsky, “A model of synaptic memory: a CaMKII/PP1 switch that potentiates transmission by organizing an AMPA receptor anchoring assembly,” Neuron, vol. 31, no. 2, pp. 191–201, 2001. View at Publisher · View at Google Scholar
  54. G. Aakalu, W. B. Smith, N. Nguyen, C. Jiang, and E. M. Schuman, “Dynamic visualization of local protein synthesis in hippocampal neurons,” Neuron, vol. 30, no. 2, pp. 489–502, 2001. View at Publisher · View at Google Scholar
  55. Y. Yin, G. M. Edelman, and P. W. Vanderklish, “The brain-derived neurotrophic factor enhances synthesis of Arc in synaptoneurosomes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 4, pp. 2368–2373, 2002. View at Publisher · View at Google Scholar
  56. R. S. Muddashetty, S. Kelić, C. Gross, M. Xu, and G. J. Bassell, “Dysregulated metabotropic glutamate receptor-dependent translation of AMPA receptor and postsynaptic density-95 mRNAs at synapses in a mouse model of fragile X syndrome,” The Journal of Neuroscience, vol. 27, no. 20, pp. 5338–5348, 2007. View at Publisher · View at Google Scholar
  57. M. K. Chawla, J. F. Guzowski, V. Ramirez-Amaya et al., “Sparse, environmentally selective expression of Arc RNA in the upper blade of the rodent fascia dentata by brief spatial experience,” Hippocampus, vol. 15, no. 5, pp. 579–586, 2005. View at Publisher · View at Google Scholar
  58. A. Elkobi, I. Ehrlich, K. Belelovsky, L. Barki-Harrington, and K. Rosenblum, “ERK-dependent PSD-95 induction in the gustatory cortex is necessary for taste learning, but not retrieval,” Nature Neuroscience, vol. 11, no. 10, pp. 1149–1151, 2008. View at Publisher · View at Google Scholar
  59. S. Miller, M. Yasuda, J. K. Coats, Y. Jones, M. E. Martone, and M. Mayford, “Disruption of dendritic translation of CaMKIIα impairs stabilization of synaptic plasticity and memory consolidation,” Neuron, vol. 36, no. 3, pp. 507–519, 2002. View at Publisher · View at Google Scholar
  60. M. Migaud, P. Charlesworth, M. Dempster et al., “Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein,” Nature, vol. 396, no. 6710, pp. 433–439, 1998. View at Publisher · View at Google Scholar
  61. A. J. Silva, R. Paylor, J. M. Wehner, and S. Tonegawa, “Impaired spatial learning in α-calcium-calmodulin kinase II mutant mice,” Science, vol. 257, no. 5067, pp. 206–211, 1992. View at Publisher · View at Google Scholar
  62. R. D. Fevurly and R. L. Spencer, “Fos expression is selectively and differentially regulated by endogenous glucocorticoids in the paraventricular nucleus of the hypothalamus and the dentate gyrus,” Journal of Neuroendocrinology, vol. 16, no. 12, pp. 970–979, 2004. View at Publisher · View at Google Scholar
  63. E. Messaoudi, S.-W. Ying, T. Kanhema, S. D. Croll, and C. R. Bramham, “Brain-derived neurotrophic factor triggers transcription-dependent, late phase long-term potentiation in vivo,” The Journal of Neuroscience, vol. 22, no. 17, pp. 7453–7461, 2002. View at Google Scholar
  64. X. O. Zhu, M. W. Brown, B. J. McCabe, and J. P. Aggleton, “Effects of the novelty or familiarity of visual stimuli on the expression of the immediate early gene c-fos in rat brain,” Neuroscience, vol. 69, no. 3, pp. 821–829, 1995. View at Publisher · View at Google Scholar
  65. H. Wan, J. P. Aggleton, and M. W. Brown, “Different contributions of the hippocampus and perirhinal cortex to recognition memory,” The Journal of Neuroscience, vol. 19, no. 3, pp. 1142–1148, 1999. View at Google Scholar
  66. J.-C. Béïque, D.-T. Lin, M.-G. Kang, H. Aizawa, K. Takamiya, and R. L. Huganir, “Synapse-specific regulation of AMPA receptor function by PSD-95,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 51, pp. 19535–19540, 2006. View at Publisher · View at Google Scholar
  67. G. M. Schratt, E. A. Nigh, W. G. Chen, L. Hu, and M. E. Greenberg, “BDNF regulates the translation of a select group of mRNAs by a mammalian target of rapamycin-phosphatidylinositol 3-kinase-dependent pathway during neuronal development,” The Journal of Neuroscience, vol. 24, no. 33, pp. 7366–7377, 2004. View at Publisher · View at Google Scholar
  68. T. Kanhema, G. Dagestad, D. Panja et al., “Dual regulation of translation initiation and peptide chain elongation during BDNF-induced LTP in vivo: evidence for compartment-specific translation control,” Journal of Neurochemistry, vol. 99, no. 5, pp. 1328–1337, 2006. View at Publisher · View at Google Scholar
  69. B. Bingol and E. M. Schuman, “Synaptic protein degradation by the ubiquitin proteasome system,” Current Opinion in Neurobiology, vol. 15, no. 5, pp. 536–541, 2005. View at Publisher · View at Google Scholar
  70. M. Lopez-Salon, M. Alonso, M. R. M. Vianna et al., “The ubiquitin-proteasome cascade is required for mammalian long-term memory formation,” European Journal of Neuroscience, vol. 14, no. 11, pp. 1820–1826, 2001. View at Publisher · View at Google Scholar
  71. R. Fonseca, R. M. Vabulas, F. U. Hartl, T. Bonhoeffer, and U. V. Nägerl, “A balance of protein synthesis and proteasome-dependent degradation determines the maintenance of LTP,” Neuron, vol. 52, no. 2, pp. 239–245, 2006. View at Publisher · View at Google Scholar
  72. S.-H. Lee, J.-H. Choi, N. Lee et al., “Synaptic protein degradation underlies destabilization of retrieved fear memory,” Science, vol. 319, no. 5867, pp. 1253–1256, 2008. View at Publisher · View at Google Scholar
  73. D. Moncada and H. Viola, “Phosphorylation state of CREB in the rat hippocampus: a molecular switch between spatial novelty and spatial familiarity?” Neurobiology of Learning and Memory, vol. 86, no. 1, pp. 9–18, 2006. View at Publisher · View at Google Scholar
  74. H. Okuno, T. Kawashima, A. Adachi-Morishima, M. Okamura, P. Worley, and H. Bito, “Critical genomic sequences for synaptic activity-dependent expression of the Arc gene,” Program no. 38.12.2008 Neuroscience Meeting Planner. Society for Neuroscience, Washington, DC, USA, 2008.
  75. D. D. Pollak, K. Herkner, H. Hoeger, and G. Lubec, “Behavioral testing upregulates pCaMKII, BDNF, PSD-95 and egr-1 in hippocampus of FVB/N mice,” Behavioural Brain Research, vol. 163, no. 1, pp. 128–135, 2005. View at Publisher · View at Google Scholar