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Neural Plasticity
Volume 2012 (2012), Article ID 581291, 8 pages
doi:10.1155/2012/581291
Review Article
Molecular Determinants of the Spacing Effect
1Department of Physiology, Montreal Neurological Institute, McGill University, Montreal, QC, H3A 2B4, Canada
2Department of Neurology and Neurosurgery, Montreal Neurological Institute, McGill University, Montreal, QC, H3A 2B4, Canada
Received 25 October 2011; Revised 16 December 2011; Accepted 16 January 2012
Academic Editor: Andrew Weeks
Copyright © 2012 Faisal Naqib 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
- S. Commins, L. Cunningham, D. Harvey, and D. Walsh, “Massed but not spaced training impairs spatial memory,” Behavioural Brain Research, vol. 139, no. 1-2, pp. 215–223, 2003. View at Publisher · View at Google Scholar · View at Scopus
- G. Isabel, A. Pascual, and T. Preat, “Exclusive consolidated memory phases in Drosophila,” Science, vol. 304, no. 5673, pp. 1024–1027, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- S. A. Josselyn, C. Shi, W. A. Carlezon, R. L. Neve, E. J. Nestler, and M. Davis, “Long-term memory is facilitated by cAMP response element-binding protein overexpression in the amygdala,” Journal of Neuroscience, vol. 21, no. 7, pp. 2404–2412, 2001. View at Scopus
- C. Margulies, T. Tully, and J. Dubnau, “Deconstructing memory in Drosophila,” Current Biology, vol. 15, no. 17, pp. R700–R713, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- M. A. Sutton, J. Ide, S. E. Masters, and T. J. Carew, “Interaction between amount and pattern of training in the induction of intermediate- and long-term memory for sensitization in Aplysia,” Learning and Memory, vol. 9, no. 1, pp. 29–40, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- T. Tully, T. Preat, S. C. Boynton, and M. Del Vecchio, “Genetic dissection of consolidated memory in Drosophila,” Cell, vol. 79, no. 1, pp. 35–47, 1994. View at Publisher · View at Google Scholar · View at Scopus
- H. Ebbinghaus, Űber das Gedächtnis: Untersuchen zur experimentallen Psychologie, Duncker & Humblot, Leipzig, Germany, 1885, Translated in H. A. Ruger and C. E. Bussenius, Teachers College, Columbia University, Dover Press, New York, NY, USA, 1964.
- Y. Goverover, J. C. Arango-Lasprilla, F. G. Hillary, N. Chiaravalloti, and J. Deluca, “Application of the spacing effect to improve learning and memory for functional tasks in traumatic brain injury: a pilot study,” American Journal of Occupational Therapy, vol. 63, no. 5, pp. 543–548, 2009. View at Scopus
- Y. Goverover, F. G. Hillary, N. Chiaravalloti, J. C. Arango-Lasprilla, and J. Deluca, “A functional application of the spacing effect to improve learning and memory in persons with multiple sclerosis,” Journal of Clinical and Experimental Neuropsychology, vol. 31, no. 5, pp. 513–522, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- P. A. Kelley, Making Minds: What's Wrong with Education- and What Should We Do About It?Routledge, London, UK, 2007.
- N. J. Cepeda, H. Pashler, E. Vul, J. T. Wixted, and D. Rohrer, “Distributed practice in verbal recall tasks: a review and quantitative synthesis,” Psychological Bulletin, vol. 132, no. 3, pp. 354–380, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- H. A. Vlach, C. M. Sandhofer, and N. Kornell, “The spacing effect in children's memory and category induction,” Cognition, vol. 109, no. 1, pp. 163–167, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- N. Caporale and Y. Dan, “Spike timing-dependent plasticity: a Hebbian learning rule,” Annual Review of Neuroscience, vol. 31, pp. 25–46, 2008. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- H. W. Kessels and R. Malinow, “Synaptic AMPA receptor plasticity and behavior,” Neuron, vol. 61, no. 3, pp. 340–350, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- R. C. Malenka, “Synaptic plasticity and AMPA receptor trafficking,” Annals of the New York Academy of Sciences, vol. 1003, pp. 1–11, 2003. View at Publisher · View at Google Scholar · View at Scopus
- Y. Yovell and T. W. Abrams, “Temporal asymmetry in activation of Aplysia adenylyl cyclase by calcium and transmitter may explain temporal requirements of conditioning,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 14, pp. 6526–6530, 1992. View at Publisher · View at Google Scholar · View at Scopus
- C. M. Alberini, “Genes to remember,” Journal of Experimental Biology, vol. 202, no. 21, pp. 2887–2891, 1999. View at Scopus
- D. A. Frank and M. E. Greenberg, “CREB: a mediator of long-term memory from mollusks to mammals,” Cell, vol. 79, no. 1, pp. 5–8, 1994. View at Publisher · View at Google Scholar · View at Scopus
- F. Naqib, C. A. Farah, C. C. Pack, and W. S. Sossin, “The rates of protein synthesis and degradation account for the differential response of neurons to spaced and massed training protocols,” PLoS Computational Biology, vol. 7, no. 12, 2011. View at Publisher · View at Google Scholar · View at PubMed
- U. Frey, Y. Y. Huang, and E. R. Kandel, “Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons,” Science, vol. 260, no. 5114, pp. 1661–1664, 1993. View at Scopus
- G. Grecksch and H. Matthies, “Two sensitive periods for the amnesic effect of anisomycin,” Pharmacology Biochemistry and Behavior, vol. 12, no. 5, pp. 663–665, 1980. View at Publisher · View at Google Scholar
- Y. Y. Huang, X. C. Li, and E. R. Kandel, “cAMP Contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase,” Cell, vol. 79, no. 1, pp. 69–79, 1994. View at Publisher · View at Google Scholar · View at Scopus
- E. R. Kandel, “The molecular biology of memory storage: a dialogue between genes and synapses,” Science, vol. 294, no. 5544, pp. 1030–1038, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- P. G. Montarolo, P. Goelet, and V. F. Castellucci, “A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia,” Science, vol. 234, no. 4781, pp. 1249–1254, 1986.
- P. V. Nguyen, T. Abel, and E. R. Kandel, “Requirement of a critical period of transcription for induction of a late phase of LTP,” Science, vol. 265, no. 5175, pp. 1104–1107, 1994. View at Scopus
- T. J. Carew, H. M. Pinsker, and E. R. Kandel, “Long-term habilitation of a defensive withdrawal reflex in Aplysia,” Science, vol. 175, no. 4020, pp. 451–454, 1972. View at Scopus
- T. D. Gover and T. W. Abrams, “Insights into a molecular switch that gates sensory neuron synapses during habituation in Aplysia,” Neurobiology of Learning and Memory, vol. 92, no. 2, pp. 155–165, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- D. L. Glanzman, S. L. Mackey, R. D. Hawkins, A. M. Dyke, P. E. Lloyd, and E. R. Kandel, “Depletion of serotonin in the nervous system of Aplysia reduces the behavioral enhancement of gill withdrawal as well as the heterosynaptic facilitation produced by tail shock,” Journal of Neuroscience, vol. 9, no. 12, pp. 4200–4213, 1989. View at Scopus
- S. Marinesco, K. E. Kolkman, and T. J. Carew, “Serotonergic modulation in Aplysia. I. Distributed serotonergic network persistently activated by sensitizing stimuli,” Journal of Neurophysiology, vol. 92, no. 4, pp. 2468–2486, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- J. Mauelshagen, C. M. Sherff, and T. J. Carew, “Differential induction of long-term synaptic facilitation by spaced and massed applications of serotonin at sensory neuron synapses of Aplysia californica,” Learning and Memory, vol. 5, no. 3, pp. 246–256, 1998. View at Scopus
- C. M. Alberini, M. Ghirardi, R. Metz, and E. R. Kandel, “C/EBP is an immediate-early gene required for the consolidation of long-term facilitation in Aplysia,” Cell, vol. 76, no. 6, pp. 1099–1114, 1994. View at Scopus
- D. Bartsch, M. Ghirardi, P. A. Skehel et al., “Aplysia CREB2 represses long-term facilitation: relief of repression converts transient facilitation into long-term functional and structural change,” Cell, vol. 83, no. 6, pp. 979–992, 1995. View at Publisher · View at Google Scholar · View at Scopus
- P. K. Dash, B. Hochner, and E. R. Kandel, “Injection of the cAMP-responsive element into the nucleus of Aplysia sensory neurons blocks long-term facilitation,” Nature, vol. 345, no. 6277, pp. 718–721, 1990. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- B. K. Kaang, E. R. Kandel, and S. G. N. Grant, “Activation of cAMP-responsive genes by stimuli that produce long-term facilitation in Aplysia sensory neurons,” Neuron, vol. 10, no. 3, pp. 427–435, 1993. View at Publisher · View at Google Scholar · View at Scopus
- W. S. Sossin, “Mechanisms for the generation of synapse specificity in long-term memory: the implications of a requirement for transcription,” Trends in Neurosciences, vol. 19, no. 6, pp. 215–218, 1996. View at Publisher · View at Google Scholar · View at Scopus
- C. D. O. Beck, B. Schroeder, and R. L. Davis, “Learning performance of normal and mutant drosophila after repeated conditioning trials with discrete stimuli,” Journal of Neuroscience, vol. 20, no. 8, pp. 2944–2953, 2000. View at Scopus
- I. S. Ho, F. Hannan, H. F. Guo, I. Hakker, and Y. Zhong, “Distinct functional domains of neurofibromatosis type 1 regulate immediate versus long-term memory formation,” Journal of Neuroscience, vol. 27, no. 25, pp. 6852–6857, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- J. C. P. Yin, J. S. Wallach, M. Del Vecchio et al., “Induction of a dominant negative CREB transgene specifically blocks long- term memory in Drosophila,” Cell, vol. 79, no. 1, pp. 49–58, 1994. View at Publisher · View at Google Scholar · View at Scopus
- D. B. G. Akalal, D. Yu, and R. L. Davis, “A late-phase, long-term memory trace forms in the γ neurons of Drosophila mushroom bodies after olfactory classical conditioning,” Journal of Neuroscience, vol. 30, no. 49, pp. 16699–16708, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- D. Yu, D. B. G. Akalal, and R. L. Davis, “Drosophilaα/β mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning,” Neuron, vol. 52, no. 5, pp. 845–855, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- M. T. Scharf, N. H. Woo, K. Matthew Lattal, J. Z. Young, P. V. Nguyen, and T. Abel, “Protein synthesis is required for the enhancement of long-term potentiation and long-term memory by spaced training,” Journal of Neurophysiology, vol. 87, no. 6, pp. 2770–2777, 2002. View at Scopus
- D. Genoux, U. Haditsch, M. Knobloch, A. Michalon, D. Storm, and I. M. Mansuy, “Protein phosphatase 1 is a molecular constraint on learning and memory,” Nature, vol. 418, no. 6901, pp. 970–975, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- E. Hummler, T. J. Cole, J. A. Blendy et al., “Targeted mutation of the CREB gene: compensation within the CREB/ATF family of transcription factors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 91, no. 12, pp. 5647–5651, 1994. View at Publisher · View at Google Scholar · View at Scopus
- R. Bourtchuladze, B. Frenguelli, J. Blendy, D. Cioffi, G. Schutz, and A. J. Silva, “Deficient long-term memory in mice with a targeted mutation of the cAMP- responsive element-binding protein,” Cell, vol. 79, no. 1, pp. 59–68, 1994. View at Publisher · View at Google Scholar · View at Scopus
- J. H. Kogan, P. W. Frankland, J. A. Blendy et al., “Spaced training induces normal long-term memory in CREB mutant mice,” Current Biology, vol. 7, no. 1, pp. 1–11, 1997. View at Scopus
- J. A. Blendy, W. Schmid, M. Kiessling, G. Schutz, and P. Gass, “Effects of kainic acid induced seizures on immediate early gene expression in mice with a targeted mutation of the CREB gene,” Brain Research, vol. 681, no. 1-2, pp. 8–14, 1995. View at Publisher · View at Google Scholar · View at Scopus
- R. Maldonado, J. A. Blendy, E. Tzavara et al., “Reduction of morphine abstinence in mice with a mutation in the gene encoding CREB,” Science, vol. 273, no. 5275, pp. 657–659, 1996. View at Scopus
- D. Balschun, D. P. Wolfer, P. Gass et al., “Does cAMP response element-binding protein have a pivotal role in hippocampal synaptic plasticity and hippocampus-dependent memory?” Journal of Neuroscience, vol. 23, no. 15, pp. 6304–6314, 2003. View at Scopus
- Y. Ilin and G. Richter-Levin, “ERK2 and CREB activation in the amygdala when an event is remembered as “fearful” and not when it is remembered as "instructive",” Journal of Neuroscience Research, vol. 87, no. 8, pp. 1823–1831, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- S. A. Josselyn, S. Kida, and A. J. Silva, “Inducible repression of CREB function disrupts amygdala-dependent memory,” Neurobiology of Learning and Memory, vol. 82, no. 2, pp. 159–163, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- Y. Zhou, J. Won, M. G. Karlsson et al., “CREB regulates excitability and the allocation of memory to subsets of neurons in the amygdala,” Nature Neuroscience, vol. 12, no. 11, pp. 1438–1443, 2009. View at Scopus
- T. Abel, P. V. Nguyen, M. Barad, T. A. S. Deuel, E. R. Kandel, and R. Bourtchouladze, “Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory,” Cell, vol. 88, no. 5, pp. 615–626, 1997. View at Publisher · View at Google Scholar · View at Scopus
- T. V. P. Bliss and G. L. Collingridge, “A synaptic model of memory: long-term potentiation in the hippocampus,” Nature, vol. 361, no. 6407, pp. 31–39, 1993. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- S. J. Martin, P. D. Grimwood, and R. G. M. Morris, “Synaptic plasticity and memory: an evaluation of the hypothesis,” Annual Review of Neuroscience, vol. 23, pp. 649–711, 2000. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- H. Matthies and K. G. Reymann, “Protein kinase A inhibitors prevent the maintenance of hippocampal long-term potentiation,” NeuroReport, vol. 4, no. 6, pp. 712–714, 1993. View at Scopus
- T. C. Sacktor, “How does PKM zeta maintain long-term memory?” Nature Reviews Neuroscience, vol. 12, no. 1, pp. 9–15, 2011. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- 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 · View at Scopus
- A. Chen, I. A. Muzzio, G. Malleret et al., “Inducible enhancement of memory storage and synaptic plasticity in transgenic mice expressing an inhibitor of ATF4 (CREB-2) and C/EBP proteins,” Neuron, vol. 39, no. 4, pp. 655–669, 2003. View at Publisher · View at Google Scholar · View at Scopus
- M. Costa-Mattioli, D. Gobert, E. Stern et al., “eIF2α phosphorylation bidirectionally regulates the switch from short- to long-term synaptic plasticity and memory,” Cell, vol. 129, no. 1, pp. 195–206, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- M. Hagiwara, A. Alberts, P. Brindle et al., “Transcriptional attenuation following cAMP induction requires PP-1- mediated dephosphorylation of CREB,” Cell, vol. 70, no. 1, pp. 105–113, 1992. View at Publisher · View at Google Scholar · View at Scopus
- S. Ait-Si-Ali, D. Carlisi, S. Ramirez et al., “Phosphorylation by p44 MAP Kinase/ERK1 stimulates CBP histone acetyl transferase activity in vitro,” Biochemical and Biophysical Research Communications, vol. 262, no. 1, pp. 157–162, 1999. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- D. Michael, K. C. Martin, R. Seger, M. M. Ning, R. Baston, and E. R. Kandel, “Repeated pulses of serotonin required for long-term facilitation activate mitogen-activated protein kinase in sensory neurons of Aplysia,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 4, pp. 1864–1869, 1998. View at Publisher · View at Google Scholar · View at Scopus
- G. T. Philips, E. I. Tzvetkova, and T. J. Carew, “Transient mitogen-activated protein kinase activation is confined to a narrow temporal window required for the induction of two-trial long-term memory in Aplysia,” Journal of Neuroscience, vol. 27, no. 50, pp. 13701–13705, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- G. Y. Wu, K. Deisseroth, and R. W. Tsien, “Spaced stimuli stabilize MAPK pathway activation and its effects on dendritic morphology,” Nature Neuroscience, vol. 4, no. 2, pp. 151–158, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- K. C. Martin, D. Michael, J. C. Rose et al., “MAP kinase translocates into the nucleus of the presynaptic cell and is required for long-term facilitation in Aplysia,” Neuron, vol. 18, no. 6, pp. 899–912, 1997. View at Publisher · View at Google Scholar · View at Scopus
- Y. Zhang, R.-Y. Liu, G. A. Heberton et al., “Computational design of enhanced learning protocols,” Nature Neuroscience, vol. 15, pp. 294–297, 2011. View at Publisher · View at Google Scholar · View at PubMed
- M. R. Pagani, K. Oishi, B. D. Gelb, and Y. Zhong, “The phosphatase SHP2 regulates the spacing effect for long-term memory induction,” Cell, vol. 139, no. 1, pp. 186–198, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- A. Pascual and T. Préat, “Localization of long-term memory within the Drosophila mushroom body,” Science, vol. 294, no. 5544, pp. 1115–1117, 2001. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- D. Cai, K. Pearce, S. Chen, and D. L. Glanzman, “Protein kinase m maintains long-term sensitization and long-term facilitation in Aplysia,” Journal of Neuroscience, vol. 31, no. 17, pp. 6421–6431, 2011. View at Publisher · View at Google Scholar · View at PubMed
- E. A. Drier, M. K. Tello, M. Cowan et al., “Memory enhancement and formation by atypical PKM activity in Drosophila melanogaster,” Nature Neuroscience, vol. 5, no. 4, pp. 316–324, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- D. S. F. Ling, L. S. Benardo, P. A. Serrano et al., “Protein kinase Mζ is necessary and sufficient for LTP maintenance,” Nature Neuroscience, vol. 5, no. 4, pp. 295–296, 2002. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- N. Madroñal, A. Gruart, T. C. Sacktor, and J. M. Delgado-García, “PKMζ inhibition reverses learning-induced increases in hippocampal synaptic strength and memory during trace eyeblink conditioning,” PLoS ONE, vol. 5, no. 4, 2010. View at Publisher · View at Google Scholar · View at PubMed
- E. Pastalkova, P. Serrano, D. Pinkhasova, E. Wallace, A. A. Fenton, and T. C. Sacktor, “Storage of spatial information by the maintenance mechanism of LTP,” Science, vol. 313, no. 5790, pp. 1141–1444, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- S. Sajikumar, S. Navakkode, T. C. Sacktor, and J. U. Frey, “Synaptic tagging and cross-tagging: the role of protein kinase Mζ in maintaining long-term potentiation but not long-term depression,” Journal of Neuroscience, vol. 25, no. 24, pp. 5750–5756, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- P. Serrano, Y. Yao, and T. C. Sacktor, “Persistent phosphorylation by protein kinase Mζ maintains late-phase long-term potentiation,” Journal of Neuroscience, vol. 25, no. 8, pp. 1979–1984, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- O. Hardt, P. V. Migues, M. Hastings, J. Wong, and K. Nader, “PKMζ maintains 1-day- and 6-day-old long-term object location but not object identity memory in dorsal hippocampus,” Hippocampus, vol. 20, no. 6, pp. 691–695, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- J. L. Kwapis, T. J. Jarome, M. E. Lonergan, and F. J. Helmstetter, “Protein kinase mzeta maintains fear memory in the amygdala but not in the hippocampus,” Behavioral Neuroscience, vol. 123, no. 4, pp. 844–850, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- R. Shema, T. C. Sacktor, and Y. Dudai, “Rapid erasure of long-term memory associations in the cortex by an inhibitor of PKMζ,” Science, vol. 317, no. 5840, pp. 951–953, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- L. M. von Kraus, T. C. Sacktor, and J. T. Francis, “Erasing sensorimotor memories via PKMζ inhibition,” PLoS ONE, vol. 5, no. 6, Article ID e11125, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- A. I. Hernandez, N. Blace, J. F. Crary et al., “Protein kinase Mζ synthesis from a brain mRNA encoding an independent protein kinase Cζ catalytic domain. Implications for the molecular mechanism of memory,” Journal of Biological Chemistry, vol. 278, no. 41, pp. 40305–40316, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- P. Osten, L. Valsamis, A. Harris, and T. C. Sacktor, “Protein synthesis-dependent formation of protein kinase Mζ in long-term potentiation,” Journal of Neuroscience, vol. 16, no. 8, pp. 2444–2451, 1996. View at Scopus
- B. Dumitriu, J. E. Cohen, Q. Wan, A. M. Negroiu, and T. W. Abrams, “Serotonin receptor antagonists discriminate between PKA- and PKC-mediated plasticity in Aplysia sensory neurons,” Journal of Neurophysiology, vol. 95, no. 4, pp. 2713–2720, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- J. A. Lee, D. J. Jang, and B. K. Kaang, “Two major gate-keepers in the self-renewal of neural stem cells: Erk1/2 and PLC1 in FGFR signaling,” Molecular Brain, vol. 2, no. 1, article 15, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- I. Nagakura, T. W. Dunn, C. A. Farah, A. Heppner, F. F. Li, and W. S. Sossin, “Regulation of protein kinase C Apl II by serotonin receptors in Aplysia,” Journal of Neurochemistry, vol. 115, no. 4, pp. 994–1006, 2010. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- U. Müller and T. J. Carew, “Serotonin induces temporally and mechanistically distinct phases of persistent PKA activity in Aplysia sensory neurons,” Neuron, vol. 21, no. 6, pp. 1423–1434, 1998. View at Publisher · View at Google Scholar · View at Scopus
- M. A. Sutton and T. J. Carew, “Parallel molecular pathways mediate expression of distinct forms of intermediate-term facilitation at tail sensory-motor synapses in Aplysia,” Neuron, vol. 26, no. 1, pp. 219–231, 2000. View at Scopus
- C. A. Farah, D. Weatherill, T. W. Dunn, and W. S. Sossin, “PKC differentially translocates during spaced and massed training in Aplysia,” Journal of Neuroscience, vol. 29, no. 33, pp. 10281–10286, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
- W. S. Sossin, “An autonomous kinase generated during long-term facilitation in Aplysia is related to the Ca2+-lndependent protein kinase C Apl II,” Learning and Memory, vol. 3, no. 5, pp. 389–401, 1997. View at Scopus
- S. Sugita, D. A. Baxter, and J. H. Byrne, “Modulation of a cAMP/protein kinase A cascade by protein kinase C in sensory neurons of Aplysia,” Journal of Neuroscience, vol. 17, no. 19, pp. 7237–7244, 1997. View at Scopus
- N. Nadif Kasri, A. Nakano-Kobayashi, and L. Van Aelst, “Rapid synthesis of the X-linked mental retardation protein OPHN1 mediates mglur-dependent LTD through interaction with the endocytic machinery,” Neuron, vol. 72, no. 2, pp. 300–315, 2011. View at Publisher · View at Google Scholar · View at PubMed
- G. Villareal, Q. Li, D. Cai, and D. Glanzman, “The role of rapid, local, postsynaptic protein synthesis in learning-related synaptic facilitation in Aplysia,” Current Biology, vol. 17, no. 23, pp. 2073–2080, 2007. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus