Mechanism based approaches for rescuing and enhancing cognition

Frontiers in Neuroscience

Volumn , Issue 7 AUG, 2013, Pages

  Lynch, Gary ^a   Gall, Christine M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Ampakine; Animal models; Cognitive enhancement; Cytoskeleton; Learning; Long term potentiation; LTP; Spaced trials

Indexed keywords

ESTROGEN; INTEGRIN;

ARTICLE; COGNITION; DOWN SYNDROME; ESTROGEN BLOOD LEVEL; FRAGILE X SYNDROME; HAPPY PUPPET SYNDROME; HUMAN; HUNTINGTON CHOREA; INFLAMMATION; INTELLECTUAL IMPAIRMENT; LEARNING DISORDER; LONG TERM MEMORY; LONG TERM POTENTIATION; MEMORY; NERVE CELL PLASTICITY; NEUROBIOLOGY; NEUROPSYCHIATRY; NONHUMAN; RETT SYNDROME; RODENT MODEL; THETA RHYTHM; TUBEROUS SCLEROSIS;

EID: 84900419565     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2013.00143     Document Type: Article

References (132)

1. Abraham, W. C. (2003). How long will long-term potentiation last. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 735-744. doi: 10.1098/rstb.2002.1222
2. Ackerley, S. J., Stinear, C. M., Barber, P. A., and Byblow, W. D. (2010). Combining theta burst stimulation with training after subcortical stroke. Stroke 41, 1568-1572. doi: 10.1161/STROKEAHA.110.583278
3. Arai, A., Kessler, M., Rogers, G., and Lynch, G. (1996). Effects of a memory enhancing drug on AMPA receptor currents and synaptic transmission in hippocampus. J. Pharmacol. Exp. Ther. 278, 627-638.
4. Arai, A. C., and Kessler, M. (2007). Pharmacology of ampakine modulators: from AMPA receptors to synapses and behavior. Curr. Drug Targets 8, 583-602. doi: 10.2174/138945007780618490
5. Arai, A. C., Xia, Y. F., and Suzuki, E. (2004). Modulation of AMPA receptor kinetics differentially influences synaptic plasticity in the hippocampus. Neuroscience. 123, 1011-1024. doi: 10.1016/j.neuroscience.2003.10.033
6. Axmacher, N., Mormann, F., Fernandez, G., Elger, C. E., and Fell, J. (2006). Memory formation by neuronal synchronization. Brain Res. Rev. 52, 170-182. doi: 10.1016/j.brainresrev.2006.01.007
7. Babayan, A. H., Kramar, E. A., Barrett, R. M., Jafari, M., Haettig, J., Chen, L. Y., et al. (2012). Integrin dynamics produce a delayed stage of long-term potentiation and memory consolidation. J. Neurosci. 32, 12854-12861. doi: 10.1523/JNEUROSCI.2024-12.2012
8. Baudry, M., Kramar, E., Xu, X., Zadran, H., Moreno, S., Lynch, G., et al. (2012). Ampakines promote spine actin polymerization, long-term potentiation, and learning in a mouse model of angelman syndrome. Neurobiol. Dis. 47, 210-215. doi: 10.1016/j.nbd.2012.04.002
9. Belichenko, P. V., Kleschevnikov, A. M., Salehi, A., Epstein, C. J., and Mobley, W. C. (2007). Synaptic and cognitive abnormalities in mouse models of down syndrome: exploring genotype-phenotype relationships. J. Comp. Neurol. 504, 329-345. doi: 10.1002/cne.21433
10. Bliss, T. V., and Collingridge, G. L. (1993). A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361, 31-39. doi: 10.1038/361031a0
11. Bozdagi, O., Nagy, V., Kwei, K. T., and Huntley, G. W. (2007). In vivo roles for matrix metalloproteinase-9 in mature hippocampal synaptic physiology and plasticity. J. Neurophysiol. 98, 334-344. doi: 10.1152/jn.00202.2007
12. Brakebusch, C., and Fassler, R. (2003). The integrin-actin connection, an eternal love affair. Embo. J. 22, 2324-2333. doi: 10.1093/emboj/cdg245
13. Buzsaki, G. (2005). Theta rhythm of navigation: link between path integration and landmark navigation, episodic and semantic memory. Hippocampus 15, 827-840. doi: 10.1002/hipo.20113
14. Cakic, V. (2009). Smart drugs for cognitive enhancement: ethical and pragmatic considerations in the era of cosmetic neurology. J. Med. Ethics. 35, 611-615. doi: 10.1136/jme.2009.030882
15. Callan, D. E., and Schweighofer, N. (2010). Neural correlates of the spacing effect in explicit verbal semantic encoding support the deficient-processing theory. Hum. Brain Mapp. 31, 645-659.
16. Cao, C., Rioult-Pedotti, M. S., Migani, P., Yu, C. J., Tiwari, R., Parang, K., et al. (2013). Impairment of TrkB-PSD-95 signaling in angelman syndrome. PLoS Biol. 11:e1001478. doi: 10.1371/journal.pbio.1001478
17. Castren, E., Berninger, B., Leingartner, A., and Lindholm, D. (1998). Regulation of brain derived neurotrophic factor mRNA levels in hippocampus by neuronal activity. Prog. Brain Res. 117, 57-64. doi: 10.1016/S0079-6123(08)64007-8
18. Castrén, E., Zafra, F., Thoenen, H., and Lindholm, D. (1992). Light regulates expression of brain-derived neurotrophic factor mRNA in rat visual cortex. Proc. Natl. Acad. Sci. U.S.A. 89, 9444-9448. doi: 10.1073/pnas.89.20.9444
19. Cepeda, N. J., Pashler, H., Vul, E., Wixted, J. T., and Rohrer, D. (2006). Distributed practice in verbal recall tasks: a review and quantitative synthesis. Psychol. Bull. 132, 354-380. doi: 10.1037/0033-2909.132.3.354
20. Chan, C. S., Levenson, J. M., Mukhopadhyay, P. S., Zong, L., Bradley, A., Sweatt, J. D., et al. (2007). Alpha3-integrins are required for hippocampal long-term potentiation and working memory. Learn. Mem. 14, 606-615. doi: 10.1101/lm.648607
21. Chan, C.-S., Weeber, E. J., Kurup, S., Sweatt, J. D., and Davis, R. L. (2003). Integrin requirement for hippocampal synaptic plasticity and spatial memory. J. Neurosci. 23, 7107-7116.
22. Chan, C. S., Weeber, E. J., Zong, L., Fuchs, E., Sweatt, J. D., and Davis, R. L. (2006). Beta 1-integrins are required for hippocampal AMPA receptor-dependent synaptic transmission, synaptic plasticity, and working memory. J. Neurosci. 26, 223-232. doi: 10.1523/JNEUROSCI.4110-05.2006
23. Chen, L. Y., Rex, C. S., Babayan, A. H., Kramar, E. A., Lynch, G., Gall, C. M., et al. (2010). Physiological activation of synaptic Rac>PAK (p-21 activated kinase) signaling is defective in a mouse model of fragile x syndrome. J. Neurosci. 30, 10977-10984. doi: 10.1523/JNEUROSCI.1077-10.2010
24. Chen, L. Y., Rex, C. S., Casale, M. S., Gall, C. M., and Lynch, G. (2007). Changes in synaptic morphology accompany actin signaling during LTP. J. Neurosci. 27, 5363-5372. doi: 10.1523/JNEUROSCI.0164-07.2007
25. Chen, Y., Kramar, E. A., Chen, L. Y., Babayan, A. H., Andres, A. L., Gall, C. M., et al. (2013). Impairment of synaptic plasticity by the stress mediator CRH involves selective destruction of thin dendritic spines via RhoA signaling. Mol. Psychiatry 18, 485-496. doi: 10.1038/mp.2012.17
26. Chun, D., Gall, C. M., Bi, X., and Lynch, G. (2001). Evidence that integrins contribute to multiple stages in the consolidation of long term potentiation. Neuroscience 105, 815-829. doi: 10.1016/S0306-4522(01)00173-7
27. Costa, A. C., and Grybko, M. J. (2005). Deficits in hippocampal CA1 LTP induced by TBS but not HFS in the Ts65Dn mouse: A model of down syndrome. Neurosci. Lett. 382, 317-322. doi: 10.1016/j.neulet.2005.03.031
28. Danen, E. H., van Rheenen, J., Franken, W., Huveneers, S., Sonneveld, P., Jalink, K., et al. (2005). Integrins control motile strategy through a Rho-cofilin pathway. J. Cell Biol. 169, 515-526. doi: 10.1083/jcb.200412081
29. Darby, R. (2010). Ethical issues in the use of cognitive enhancement. Pharos. Alpha Omega Alpha Honor. Med. Soc. 73, 16-22.
30. Dash, P. K., Orsi, S. A., Moody, M., and Moore, A. N. (2004). A role for hippocampal Rho-ROCK pathway in long-term spatial memory. Biochem. Biophys. Res. Commun. 322, 893-898. doi: 10.1016/j.bbrc.2004.08.004
31. Davis, M., Hanson, S. A., and Altevogt, B. (2008). Neuroscience Biomarkers and Biosignatures. Converging Technologies, Emerging Partnerships: Workshop Summary. Washington, DC: National Academies Press.
32. del Toro, D., Canals, J. M., Gines, S., Kojima, M., Egea, G., and Alberch, J. (2006). Mutant huntingtin impairs the post-golgi trafficking of brain-derived neurotrophic factor but not its val66met polymorphism. J. Neurosci. 26, 12748-12757. doi: 10.1523/JNEUROSCI.3873-06.2006
33. DeMali, K. A., Wennerberg, K., and Burridge, K. (2003). Integrin signaling to the actin cytoskeleton. Curr. Opin. Cell Biol. 15, 572-582. doi: 10.1016/S0955-0674(03)00109-1
34. Demeter, E., Sarter, M., and Lustig, C. (2008). Rats and humans paying attention: cross-species task development for translational research. Neuropsychology 22, 787-799. doi: 10.1037/a0013712
35. Dragunow, M., Beilharz, E., Mason, B., Lawlor, P., Abraham, W., and Gluckman, P. (1993). Brain-derived neurotrophic factor expression after long-term potentiation. Neurosci. Lett. 160, 232-236. doi: 10.1016/0304-3940(93)90420-P
36. Ehninger, D., Han, S., Shilyansky, C., Zhou, Y., Li, W., Kwiatkowski, D. J., et al. (2008). Reversal of learning deficits in a Tsc2+/- mouse model of tuberous sclerosis. Nat. Med. 14, 843-848. doi: 10.1038/nm1788
37. Enoki, R., Hu, Y. L., Hamilton, D., and Fine, A. (2009). Expression of long-term plasticity at individual synapses in hippocampus is graded, bidirectional, and mainly presynaptic: optical quantal analysis. Neuron 62, 242-253. doi: 10.1016/j.neuron.2009.02.026
38. Farah, M. J., Haimm, C., Sankoorikal, G., Smith, M. E., and Chatterjee, A. (2009). When we enhance cognition with Adderall, do we sacrifice creativity. A preliminary study. Psychopharmacology (Berl.) 202, 541-547. doi: 10.1007/s00213-008-1369-3
39. Forlini, C., Hall, W., Maxwell, B., Outram, S. M., Reiner, P. B., Repantis, D., et al. (2013). Navigating the enhancement landscape. Ethical issues in research on cognitive enhancers for healthy individuals. EMBO Rep. 14, 123-128. doi: 10.1038/embor.2012.225
40. Frey, U., Schollmeier, K., Reymann, K. G., and Seidenbecher, T. (1995). Asymptotic hippocampal long-term potentiation in rats does not preclude additional potentiation at later phases. Neuroscience 67, 799-807. doi: 10.1016/0306-4522(95)00117-2
41. Fulton, J. (1941). Encephalization of motor functions during the evolution of the primate nervous system. Ohio J. Sci. 41, 173-182.
42. Gall, C. (1992). Regulation of brain neurotrophin expression by physiological activity. Trends Pharmacol. Sci. 13, 401-403. doi: 10.1016/0165-6147(92)90123-N
43. Gavin, C. F., Rubio, M. D., Young, E., Miller, C., and Rumbaugh, G. (2012). Myosin II motor activity in the lateral amygdala is required for fear memory consolidation. Learn. Mem. 19, 9-14. doi: 10.1101/lm.024042.111
44. Granger, R., Staubli, U., Davis, M., Perez, Y., Nillson, L., Rogers, G. A., et al. (1993). A drug that facilitates glutamatergic transmission reduces exploratory activity and improves performance in a learning-dependent task. Synapse 15, 326-329. doi: 10.1002/syn.890150409
45. Hamlyn, E., Brand, L., Shahid, M., and Harvey, B. H. (2009). The ampakine, Org 26576, bolsters early spatial reference learning and retrieval in the morris water maze: a subchronic, dose-ranging study in rats. Behav. Pharmacol. 20, 662-667. doi: 10.1097/FBP.0b013e328331ba1b
46. Hampson, R. E., Espana, R. A., Rogers, G. A., Porrino, L. J., and Deadwyler, S. A. (2009). Mechanisms underlying cognitive enhancement and reversal of cognitive deficits in nonhuman primates by the ampakine CX717. Psychopharmacology (Berl.) 202, 355-369. doi: 10.1007/s00213-008-1360-z
47. Hampson, R. E., Rogers, G., Lynch, G., and Deadwyler, S. A. (1998). Facilitative effects of the ampakine CX516 on short-term memory in rats: enhancement of delayed-nonmatch-to-sample performance. J. Neurosci. 18, 2740-2747.
48. Harvey, C. D., and Svoboda, K. (2007). Locally dynamic synaptic learning rules in pyramidal neuron dendrites. Nature. 450, 1195-1200. doi: 10.1038/nature06416
49. Harvey, C. D., Yasuda, R., Zhong, H., and Svoboda, K. (2008). The spread of Ras activity triggered by activation of a single dendritic spine. Science. 321, 136-140. doi: 10.1126/science.1159675
50. Hess, U., Whalen, S., Sandoval, L., Lynch, G., and Gall, C. (2003). Ampakines reduce methamphetamine-driven rotation and activate neocortex in a regionally selective fashion. Neuroscience 121, 509-521. doi: 10.1016/S0306-4522(03)00423-8
51. Hsu, Y. F., Liao, K. K., Lee, P. L., Tsai, Y. A., Yeh, C. L., Lai, K. L., et al. (2011). Intermittent theta burst stimulation over primary motor cortex enhances movement-related beta synchronisation. Clin. Neurophysiol. 122, 2260-2267. doi: 10.1016/j.clinph.2011.03.027
52. Huang, C. C., Liang, Y. C., and Hsu, K. S. (1999). A role for extracellular adenosine in time-dependent reversal of long-term potentiation by low-frequency stimulation at hippocampal CA1 synapses. J. Neurosci. 19, 9728-9738.
53. Huang, Y. Z., Rothwell, J. C., Chen, R. S., Lu, C. S., and Chuang, W. L. (2011). The theoretical model of theta burst form of repetitive transcranial magnetic stimulation. Clin. Neurophysiol. 122, 1011-1018. doi: 10.1016/j.clinph.2010.08.016
54. Huang, Z., Shimazu, K., Woo, N. H., Zang, K., Muller, U., Lu, B., et al. (2006). Distinct roles of the beta 1-class integrins at the developing and the mature hippocampal excitatory synapse. J. Neurosci. 26, 11208-11219. doi: 10.1523/JNEUROSCI.3526-06.2006
55. Hyman, S. E. (2011). Cognitive enhancement: promises and perils. Neuron 69, 595-598. doi: 10.1016/j.neuron.2011.02.012
56. Isackson, P. J., Murray, K., Huntsman, M., and Gall, C. M. (1991). BDNF mRNA expression is increased in adult rat forebrain after limbic seizures: temporal patterns of induction distinct from NGF. Neuron 6, 937-948. doi: 10.1016/0896-6273(91)90234-Q
57. Jiang, Y. H., Armstrong, D., Albrecht, U., Atkins, C. M., Noebels, J. L., Eichele, G., et al. (1998). Mutation of the Angelman ubiquitin ligase in mice causes increased cytoplasmic p53 and deficits of contextual learning and long-term potentiation. Neuron 21, 799-811. doi: 10.1016/S0896-6273(00)80596-6
58. Jin, R., Clark, S., Weeks, A. M., Dudman, J. T., Gouaux, E., and Partin, K. M. (2005). Mechanism of positive allosteric modulators acting on AMPA receptors. J. Neurosci. 25, 9027-9036. doi: 10.1523/JNEUROSCI.2567-05.2005
59. Kant, I. (1987) Critique of Judgement, Translated by Werner S. Pluhar. Indianapolis: Hackett Publishing Co.
60. Karlsson, M. P., and Frank, L. M. (2008). Network dynamics underlying the formation of sparse, informative, representations in the hippocampus. J. Neurosci. 28, 14271-14281. doi: 10.1523/JNEUROSCI.4261-08.2008
61. Kornell, N., and Bjork, R. A. (2008). Learning concepts and categories: is spacing the "Enemy of induction." Psychol. Sci. 19, 585-592. doi: 10.1111/j.1467-9280.2008.02127.x
62. Kovalchuk, Y., Hanse, E., Kafitz, K. W., and Konnerth, A. (2002). Postsynaptic induction of BDNF-mediated long-term potentiation. Science 295, 1729-1735. doi: 10.1126/science.1067766
63. Kramar, E. A., Babayan, A. H., Gall, C. M., and Lynch, G. (2013). Estrogen promotes learning-related plasticity by modifying the synaptic cytoskeleton. Neuroscience 239, 3-16. doi: 10.1016/j.neuroscience.2012.10.038.
64. Kramar, E. A., Chen, L. Y., Lauterborn, J. C., Simmons, D. A., Gall, C. M., and Lynch, G. (2012a). BDNF upregulation rescues synaptic plasticity in middle-aged ovariectomized rats. Neurobiol. Aging 33, 708-719. doi: 10.1016/j.neurobiolaging.2010.06.008
65. Kramar, E. A., Babayan, A. H., Gavin, C. F., Cox, C. D., Jafari, M., Gall, C. M., et al. (2012b). Synaptic evidence for the efficacy of spaced learning. Proc. Natl. Acad. Sci. U.S.A. 109, 5121-5126. doi: 10.1073/pnas.1120700109
66. Kramar, E. A., Bernard, J. A., Gall, C. M., and Lynch, G. (2002). Alpha3 integrin receptors contribute to the consolidation of long-term potentiation. Neuroscience 110, 29-39. doi: 10.1016/S0306-4522(01)00540-1
67. Kramar, E. A., Chen, L. Y., Rex, C. S., Gall, C. M., and Lynch, G. (2009a). Estrogen's place in the family of synaptic modulators. Mol. Cell Pharmacol. 1, 258-262.
68. Kramar, E. A., Chen, L. Y., Brandon, N. J., Rex, C. S., Liu, F., Gall, C. M., et al. (2009b). Cytoskeletal changes underlie estrogen's acute effects on synaptic transmission and plasticity. J. Neurosci. 29, 12982-12993. doi: 10.1523/JNEUROSCI.3059-09.2009
69. Kramar, E. A., Lin, B., Rex, C. S., Gall, C. M., and Lynch, G. (2006). Integrin-driven actin polymerization consolidates long-term potentiation. Proc. Natl. Acad. Sci. U.S.A. 103, 5579-5584. doi: 10.1073/pnas.0601354103
70. Krucker, T., Siggins, G. R., and Halpain, S. (2000). Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 97, 6856-6861. doi: 10.1073/pnas.100139797
71. Lamprecht, R. (2011). The roles of the actin cytoskeleton in fear memory formation. Front. Behav. Neurosci. 5:39. doi: 10.3389/fnbeh.2011.00039
72. Larson, J., and Lynch, G. (1986). Induction of synaptic potentiation in hippocampus by patterned stimulation involves two events. Science 232, 985-988. doi: 10.1126/science.3704635
73. Larson, J., Wong, D., and Lynch, G. (1986). Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res. 368, 347-350. doi: 10.1016/0006-8993(86)90579-2
74. Larson, J., Xiao, P., and Lynch, G. (1993). Reversal of LTP by theta frequency stimulation. Brain Res. 600, 97-102. doi: 10.1016/0006-8993(93)90406-D
75. Lauterborn, J., Troung, G., Baudry, M., Bi, X., Lynch, G., and Gall, C. (2003). Chronic elevation of brain-derived neurotrophic factor by ampakines. J. Pharmacol. Exp. Ther. 307, 297-305. doi: 10.1124/jpet.103.053694
76. Lauterborn, J. C., Lynch, G., Vanderklish, P., Arai, A., and Gall, C. M. (2000). Positive modulation of AMPA receptors increases neurotrophin expression by hippocampal and cortical neurons. J. Neurosci. 20, 8-21.
77. Lauterborn, J. C., Rex, C. S., Kramar, E., Chen, L. Y., Pandyarajan, V., Lynch, G., et al. (2007). Brain-derived neurotrophic factor rescues synaptic plasticity in a mouse model of fragile X syndrome. J. Neurosci. 27, 10685-10694. doi: 10.1523/JNEUROSCI.2624-07.2007
78. Lee, H. Y., Ge, W. P., Huang, W., He, Y., Wang, G. X., Rowson-Baldwin, A., et al. (2011). Bidirectional regulation of dendritic voltage-gated potassium channels by the fragile X mental retardation protein. Neuron 72, 630-642. doi: 10.1016/j.neuron.2011.09.033
79. Lin, B., Kramar, E. A., Bi, X., Brucher, F. A., Gall, C. M., and Lynch, G. (2005). Theta stimulation polymerizes actin in dendritic spines of hippocampus. J. Neurosci. 25, 2062-2069. doi: 10.1523/JNEUROSCI.4283-04.2005
80. Lynch, G. (2004a). AMPA receptor modulators as cognitive enhancers. Curr. Opin. Pharmacol. 4, 4-11. doi: 10.1016/j.coph.2003.09.009
81. Lynch, M. A. (2004b). Long-term potentiation and memory. Physiol. Rev. 84, 87-136. doi: 10.1152/physrev.00014.2003
82. Lynch, G., and Baudry, M. (1988). The biochemistry of memory: a new and specific hypothesis. Science 224, 1057-1063. doi: 10.1126/science.6144182
83. Lynch, G., and Gall, C. M. (2006). Ampakines and the threefold path to cognitive enhancement. Trends Neurosci. 29, 554-562. doi: 10.1016/j.tins.2006.07.007
84. Lynch, G., and Granger, R. (2008). Big Brain: The Origins and Future of Human Intelligence. New York, NY: Palgrave Macmillan Press.
85. Lynch, G., Kramar, E. A., Rex, C. S., Jia, Y., Chappas, D., Gall, C. M., et al. (2007). Brain-derived neurotrophic factor restores synaptic plasticity in a knock-in mouse model of Huntington's disease. J. Neurosci. 27, 4424-4434. doi: 10.1523/JNEUROSCI.5113-06.2007
86. Lynch, G., Palmer, L. C., and Gall, C. M. (2011). The likelihood of cognitive enhancement. Pharmacol. Biochem. Behav. 99, 116-129. doi: 10.1016/j.pbb.2010.12.024
87. Lynch, G., Rex, C. S., Chen, L. Y., and Gall, C. M. (2008). The substrates of memory: defects, treatments, and enhancement. Eur. J. Pharmacol. 585, 2-13. doi: 10.1016/j.ejphar.2007.11.082
88. Lynch, G., Rex, C. S., Chen, L. Y., and Gall, C. M. (2010). "Synaptic mechanisms for encoding memory," in Encyclopedia of Behavioral Neuroscience, Vol. 3, eds G. Koob, R. F. Thompson, and M. Le Moal (Section ed) T. Shors (London: Academic Press, an imprint of Elsevier Ltd.), 356-364.
89. Matsuzaki, M., Honkura, N., Ellis-Davies, G. C., and Kasai, H. (2004). Structural basis of long-term potentiation in single dendritic spines. Nature 429, 761-766. doi: 10.1038/nature02617
90. Menache, A. (2012). Are animal models relevant in modern psychiatry. Psychiatr. Times 29, 1-5.
91. Miranti, C. K., and Brugge, J. S. (2002). Sensing the environment: a historical perspective on integrin signal transduction. Nat. Cell Biol. 4, E83-E90. doi: 10.1038/ncb0402-e83
92. Moretti, P., Levenson, J. M., Battaglia, F., Atkinson, R., Teague, R., Antalffy, B., et al. (2006). Learning and memory and synaptic plasticity are impaired in a mouse model of rett syndrome. J. Neurosci. 26, 319-327. doi: 10.1523/JNEUROSCI.2623-05.2006
93. Morris, R. G. (2003). Long-term potentiation and memory. Philos.Trans. R. Soc. Lond. B Biol. Sci. 358, 643-647. doi: 10.1098/rstb.2002.1230
94. Murray, C. A., and Lynch, M. A. (1998). Evidence that increased hippocampal expression of the cytokine interleukin1ß is a common trigger for age- and stress-induced impairments in long-term potentiation. J. Neurosci. 18, 2974-2981.
95. Murphy, K. P., Carter, R. J., Lione, L. A., Mangiarini, L., Mahal, A., Bates, G. P., et al. (2000). Abnormal synaptic plasticity and impaired spatial cognition in mice transgenic for exon 1 of the human huntington's disease mutation. J. Neurosci. 20, 5115-5123.
96. Nagy, V., Bozdagi, O., and Huntley, G. W. (2007). The extracellular protease matrix metalloproteinase-9 is activated by inhibitory avoidance learning and required for long-term memory. Learn. Mem. 14, 655-664. doi: 10.1101/lm.678307
97. Nagy, V., Bozdagi, O., Matynia, A., Balcerzyk, M., Okulski, P., Dzwonek, J., et al. (2006). Matrix metalloproteinase-9 is required for hippocampal late-phase long-term potentiation and memory. J. Neurosci. 26, 1923-1934. doi: 10.1523/JNEUROSCI.4359-05.2006
98. Otto, T., Eichenbaum, H., Wiener, S. I., and Wible, C. G. (1991). Learning-related patterns of CA1 spike trains parallel stimulation parameters optimal for inducing hippocampal long-term potentiation. Hippocampus 1, 181-192. doi: 10.1002/hipo.450010206
99. Porrino, L., Daunais, J., Rogers, G., Hampson, R., and Deadwyler, S. (2005). Facilitation of task performance and removal of the effects of sleep deprivation by an ampakine (CX717) in nonhuman primates. PLoS Biol. 3:e299. doi: 10.1371/journal.pbio.0030299
100. Rex, C. S., Chen, L. Y., Sharma, A., Liu, J., Babayan, A. H., Gall, C. M., et al. (2009). Different Rho GTPase-dependent signaling pathways initiate sequential steps in the consolidation of long-term potentiation. J. Cell Biol. 186, 85-97. doi: 10.1083/jcb.200901084
101. Rex, C. S., Gavin, C. F., Rubio, M. D., Kramar, E. A., Chen, L. Y., Jia, Y., et al. (2010). Myosin IIb regulates actin dynamics during synaptic plasticity and memory formation. Neuron 67, 603-617. doi: 10.1016/j.neuron.2010.07.016
102. Rex, C. S., Kramar, E. A., Colgin, L. L., Lin, B., Gall, C. M., and Lynch, G. (2005). Long-term potentiation is impaired in middle-aged rats: regional specificity and reversal by adenosine receptor antagonists. J. Neurosci. 25, 5956-5966. doi: 10.1523/JNEUROSCI.0880-05.2005
103. Rex, C. S., Lauterborn, J. C., Lin, C. Y., Kramar, E. A., Rogers, G. A., Gall, C. M., et al. (2006). Restoration of long-term potentiation in middle-aged hippocampus after induction of brain-derived neurotrophic factor. J. Neurophysiol. 96, 677-685. doi: 10.1152/jn.00336.2006
104. Rex, C. S., Lin, C. Y., Kramar, E. A., Chen, L. Y., Gall, C. M., and Lynch, G. (2007). Brain-derived neurotrophic factor promotes long-term potentiation-related cytoskeletal changes in adult hippocampus. J. Neurosci. 27, 3017-3029. doi: 10.1523/JNEUROSCI.4037-06.2007
105. Rogan, M. T., Staubli, U. V., and LeDoux, J. E. (1997). AMPA receptor facilitation accelerates fear learning without altering the level of conditioned fear acquired. J. Neurosci. 17, 5928-5935.
106. Sacktor, T. C. (2008). PKMzeta, LTP maintenance, and the dynamic molecular biology of memory storage. Prog. Brain Res. 169, 27-40. doi: 10.1016/S0079-612300002-7
107. Sahakian, B. J., and Morein-Zamir, S. (2011). Neuroethical issues in cognitive enhancement. J. Psychopharmacol. 25, 197-204. doi: 10.1177/0269881109106926
108. Sarter, M., Martinez, V., and Kozak, R. (2009). A neurocognitive animal model dissociating between acute illness and remission periods of schizophrenia. Psychopharmacology (Berl.) 202, 237-258. doi: 10.1007/s00213-008-1216-6
109. Sauvage, M. M. (2010). Roc in animals: uncovering the neural substrates of recollection and familiarity in episodic recognition memory. Conscious. Cogn. 19, 816-828. doi: 10.1016/j.concog.2010.06.023
110. Sauvage, M. M., Fortin, N. J., Owens, C. B., Yonelinas, A. P., and Eichenbaum, H. (2008). Recognition memory: opposite effects of hippocampal damage on recollection and familiarity. Nat. Neurosci. 11, 16-18. doi: 10.1038/nn2016
111. Scharf, M. T., Woo, N. H., Lattal, K. M., Young, J. Z., Nguyen, P. V., and Abel, T. (2002). Protein synthesis is required for the enhancement of long-term potentiation and long-term memory by spaced training. J. Neurophysiol. 87, 2770-2777.
112. Seese, R. R., Babayan, A. H., Katz, A. M., Cox, C. D., Lauterborn, J. C., Lynch, G., et al. (2012). LTP induction translocates cortactin at distant synapses in wild-type but not Fmr1 knock-out mice. J. Neurosci. 32, 7403-7413. doi: 10.1523/JNEUROSCI.0968-12.2012
113. Semendeferi, K., Armstrong, E., Schleicher, A., Zilles, K., and Van Hoesen, G. W. (2001). Prefrontal cortex in humans and apes: a comparative study of area 10. Am. J. Phys. Anthropol. 114, 224-241.
114. Shieh, P. B., Hu, S.-C., Bobb, K., Timmusk, T., and Ghosh, A. (1998). Identification of a signaling pathway involved in calcium regulation of BDNF expression. Neuron 20, 727-740. doi: 10.1016/S0896-6273(00)81011-9
115. Shors, T. J., Servatius, R. J., Thompson, R. F., Rogers, G., and Lynch, G. (1995). Enhanced glutamatergic neurotransmission facilitates classical conditioning in the freely-moving rat. Neurosci. Lett. 186, 153-156. doi: 10.1016/0304-3940(95)11309-K
116. Simmons, D. A., Mehta, R. A., Lauterborn, J. C., Gall, C. M., and Lynch, G. (2011). Brief ampakine treatments slow the progression of Huntington's disease phenotypes in R6/2 mice. Neurobiol. Dis. 41, 436-444. doi: 10.1016/j.nbd.2010.10.015
117. Simmons, D. A., Rex, C. S., Palmer, L., Pandyarajan, V., Fedulov, V., Gall, C. M., et al. (2009). Up-regulating BDNF with an ampakine rescues synaptic plasticity and memory in Huntington's disease knockin mice. Proc. Natl. Acad. Sci. U.S.A. 106, 4906-4911. doi: 10.1073/pnas.0811228106
118. Sirvio, J., Larson, J., Quach, C. N., Rogers, G. A., and Lynch, G. (1996). Effects of pharmacologically facilitating glutamatergic transmission in the trisynaptic intrahippocampal circuit. Neuroscience 74, 1025-1035.
119. Staubli, U., Chun, D., and Lynch, G. (1998). Time-dependent reversal of long-term potentiation by an integrin antagonist. J. Neurosci. 18, 3460-3469.
120. Staubli, U., and Lynch, G. (1987). Stable hippocampal long-term potentiation elicited by 'theta' pattern stimulation. Brain Res. 435, 227-234. doi: 10.1016/0006-8993(87)91605-2
121. Staubli, U., Rogers, G., and Lynch, G. (1994a). Facilitation of glutamate receptors enhances memory. Proc. Natl. Acad. Sci. U.S.A. 91, 777-781. doi: 10.1073/pnas.91.2.777
122. Staubli, U., Perez, Y., Xu, F., Rogers, G., Ingvar, M., Stone-Elander, S., et al. (1994b). Centrally active modulators of glutamate (AMPA) receptors facilitate the induction of LTP in vivo. Proc. Natl. Acad. Sci. U.S.A. 91, 11158-11162. doi: 10.1073/pnas.91.23.11158
123. Staubli, U., Vanderklish, P. W., and Lynch, G. (1990). An inhibitor of integrin receptors blocks LTP. Behav. Neural Biol. 53, 1-5. doi: 10.1016/0163-1047(90)90712-F
124. Tong, L., Prieto, G. A., Kramar, E. A., Smith, E. D., Cribbs, D. H., Lynch, G., et al. (2012). Brain-derived neurotrophic factor-dependent synaptic plasticity is suppressed by interleukin-1ß via p38 mitogen-activated protein kinase. J. Neurosci. 32, 17714-17724. doi: 10.1523/JNEUROSCI.1253-12.2012
125. Turner, D. C., Robbins, T. W., Clark, L., Aron, A. R., Dowson, J., and Sahakian, B. J. (2003). Cognitive enhancing effects of modafinil in healthy volunteers. Psychopharmacology (Berl.) 165, 260-269.
126. van der Worp, H. B., Howells, D. W., Sena, E. S., Porritt, M. J., Rewell, S., O'Collins, V., et al. (2010). Can animal models of disease reliably inform human studies. PLoS Med. 7:e1000245. doi: 10.1371/journal.pmed.1000245
127. von der Brelie, C., Waltereit, R., Zhang, L., Beck, H., and Kirschstein, T. (2006). Impaired synaptic plasticity in a rat model of tuberous sclerosis. Eur. J. Neurosci. 23, 686-692. doi: 10.1111/j.1460-9568.2006.04594.x
128. Warren, M. S., Bradley, W. D., Gourley, S. L., Lin, Y. C., Simpson, M. A., Reichardt, L. F., et al. (2012). Integrin beta1 signals through arg to regulate postnatal dendritic arborization, synapse density, and behavior. J. Neurosci. 32, 2824-2834. doi: 10.1523/JNEUROSCI.3942-11.2012
129. Wickelgren, W. A. (1974). Single-trace fragility theory of memory dynamics. Mem. Cogn. 2, 775-780. doi: 10.3758/BF03198154.
130. Wiesner, S., Legate, K. R., and Fassler, R. (2005). Integrin-actin interactions. Cell Mol. Life Sci. 62, 1081-1099. doi: 10.1007/s00018-005-4522-8
131. Xiao, P., Bahr, B., Staubli, U., Vanderklish, P., and Lynch, G. (1991). Evidence that matrix recognition contributes to stabilization but not induction of LTP. Neuroreport 2, 461-464. doi: 10.1097/00001756-199108000-00013
132. Zuccato, C., Ciammola, A., Rigamonti, D., Leavitt, B. R., Goffredo, D., Conti, L., et al. (2001). Loss of huntingtin-mediated BDNF gene transcription in Huntington's disease. Science 293, 493-498. doi: 10.1126/science.1059581