Pharmacological enhancement of memory or cognition in normal subjects

Frontiers in Systems Neuroscience

Volumn 8, Issue MAY, 2014, Pages

  Lynch, Gary ^a   Cox, Conor D ^a   Gall, Christine M ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Ampakine; BDNF; Cognitive enhancement; F actin; Learning; Long term potentiation; Positive AMPA receptor modulators; Synaptic plasticity

Indexed keywords

AMPA RECEPTOR; APAMIN; BRAIN DERIVED NEUROTROPHIC FACTOR; ESTROGEN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTROPHIN; PHYSOSTIGMINE; PREGNENOLONE SULFATE;

AFTERHYPERPOLARIZATION; CHOLINERGIC TRANSMISSION; COGNITION; DEPRESSION; FOREBRAIN; GENE EXPRESSION; HAPPY PUPPET SYNDROME; HIPPOCAMPAL CA1 REGION; HUMAN; HUNTINGTON CHOREA; LONG TERM POTENTIATION; MEMORY; NERVE CELL PLASTICITY; NEUROPATHOLOGY; NONHUMAN; NORMAL HUMAN; PROTEIN SYNTHESIS; REVIEW; SCHIZOPHRENIA; SCORING SYSTEM; SIMULATION; UPREGULATION;

EID: 84901268216     PISSN: 16625137     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnsys.2014.00090     Document Type: Review

References (163)

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. Abraham, W. C., and Williams, J. M. (2008). LTP maintenance and its protein synthesis-dependence. Neurobiol. Learn. Mem. 89, 260-268. doi: 10.1016/j.nlm.2007.10.001
3. Alarcon, J. M., Barco, A., and Kandel, E. R. (2006). Capture of the late phase of long-term potentiation within and across the apical and basilar dendritic compartments of CA1 pyramidal neurons: synaptic tagging is compartment restricted. J. Neurosci. 26, 256-264. doi: 10.1523/JNEUROSCI.3196-05.2006
4. Alkondon, M., and Albuquerque, E. X. (2001). Nicotinic acetylcholine receptor alpha7 and alpha4beta2 subtypes differentially control GABAergic input to CA1 neurons in rat hippocampus. J. Neurophysiol. 86, 3043-3055.
5. Andero, R., Daviu, N., Escorihuela, R. M., Nadal, R., and Armario, A. (2012). 7,8-dihydroxyflavone, a TrkB receptor agonist, blocks long-term spatial memory impairment caused by immobilization stress in rats. Hippocampus. 22, 399-408. doi: 10.1002/hipo.20906
6. Andero, R., Heldt, S. A., Ye, K., Liu, X., Armario, A., and Ressler, K. J. (2011). Effect of 7,8-dihydroxyflavone, a small-molecule TrkB agonist, on emotional learning. Am. J. Psychiatry 168, 163-172. doi: 10.1176/appi.ajp.2010.10030326
7. Arai, A., Black, J., and Lynch, G. (1994). Origins of the variations in long-term potentiation between synapses in the basal versus apical dendrites of hippocampal neurons. Hippocampus 4, 1-9. doi: 10.1002/hipo.450040103
8. Arai, A. C., Xia, Y. F., Rogers, G., Lynch, G., and Kessler, M. (2002). Benzamide-type AMPA receptor modulators form two subfamilies with distinct modes of action. J. Pharmacol. Exp. Ther. 303, 1075-1085. doi: 10.1124/jpet.102.040360
9. Arai, A., Kessler, M., Ambros-Ingerson, J., Quan, A., Yigiter, E., Rogers, G., et al. (1996). Effects of a centrally active benzoylpyrrolidine drug on AMPA receptor kinetics. Neuroscience 75, 573-585. doi: 10.1016/0306-4522(96)00263-1
10. Arai, A., and Lynch, G. (1998). The waveform of synaptic transmission at hippoca-pal synapses is not determined by AMPA receptor desensitization. Brain Res. 799, 230-234. doi: 10.1016/S0006-8993(98)00446-6
11. Araque, A., Parpura, V., Sanzgiri, R. P., and Haydon, P. G. (1999). Tripartite synapses: glia, the unacknowledged partner. Trends Neuro sci. 22, 208-215.doi: 10.1016/S0166-2236(98)01349-6
12. 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
13. Balkowiec, A., and Katz, D. M. (2000). Activity-dependent release of endogenous brain-derived neurotrophic factor from primary sensory neurons detected by ELISA in situ. J. Neurosci. 20, 7417-7423.
14. Bari, A., Dalley, J. W., and Robbins, T. W. (2008). The application of the 5-choice serial reaction time task for the assessment of visual attentional processes and impulse control in rats. Nat. Protoc. 3, 759-767. doi: 10.1038/nprot.2008.41
15. 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
16. Baumbarger, P. J., Muhlhauser, M., Zhai, J., Yang, R., and Nisenbaum, E. S. (2001). Positive modulation of alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid (AMPA) receptors in prefrontal cortical pyramidal neurons by a novel allosteric potentiator. J. Pharmacol. Exp. Ther. 298, 86-102.
17. Baxter, M. G., Lanthorn, T. H., Frick, K. M., Golski, S., Wan, R. Q., and Olton, D. S. (1994). C-cycloserine, a novel cognitive enhancer, improves spatial memory in aged rats. Neurobiol. Aging. 15, 207-213. doi: 10.1016/0197-4580(94)90114-7
18. Bernard, K., Danober, L., Thomas, J. Y., Lebrun, C., Munoz, C., Cordi, A., et al. (2010). Drug focus: S 18986: a positive allosteric modulator of AMPA-type glutamate receptors pharmacological profile of a novel cognitive enhancer. CNS Neurosci. Ther. 16, e193-212. doi: 10.1111/j.1755-5949.2009.00088.x
19. Bi, F., Broutman, G., Foy, M. R., Thompson, R. F., and Baudry, M. (2000). The tyro-sine kinase and mitogen-activated protein kinase pathways mediate multiple effects of estrogen in hippocampus. Proc. Natl. Acad. Sci. U.S.A. 97, 3606-3607. doi: 10.1073/pnas.97.7.3602
20. 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
21. Bliss, T. V. P., and Lomo, T. (1973). Long-lasting potentiation of synaptic transmission in the dentate area of the anesthetized rabbit following stimulation of the perforant path. J. Physiol. 232, 334-356.
22. Bollen, E., Vanmierlo, T., Akkerman, S., Wouters, C., Steinbusch, H. M., and Prickaerts, J. (2013). 7,8-dihydroxyflavone improves memory consolidation processes in rats and mice. Behav. Brain Res. 257, 8-12. doi: 10.1016/j.bbr.2013.09.029
23. Bouteiller, J. M., Allam, S. L., Hu, E. Y., Greget, R., Ambert, N., Keller, A. F., et al. (2011). Integrated multiscale modeling of the nervous system: predicting changes in hippocampal network activity by a positive AMPA receptor modulator. IEEE Trans. Biomed. Eng. 58, 3008-3011. doi: 10.1109/TBME.2011.2158605
24. Brennan, A. R., Dolinsky, B., Vu, M. A., Stanley, M., Yeckel, M. F., and Arnsten, A. F. (2008). Blockade of IP3-mediated SK channel signaling in the rat medial prefrontal cortex improves spatial working memory. Learn. Mem. 15, 93-96. doi: 10.1101/lm.767408
25. Brinton, R. D. (2009). Estrogen-induced plasticity from cells to circuits: predictions for cognitive function. Trends Pharmacol. Sci. 30, 212-222. doi: 10.1016/j.tips.2008.12.006
26. 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
27. Cajal, S. R. (1894). La fine structure des centres nerveux. Proc. R. Soc. Lond. 55, 444-468. doi: 10.1098/rspl.1894.0063
28. Capocchi, G., Zampolini, M., and Larson, J. (1992). Theta burst stimulation is optimal for induction of LTP at both apical and basal dendritic synapses on hippocampal CA1 neurons. Brain Res. 591, 332-336. doi: 10.1016/0006-8993(92)91715-Q
29. 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
30. Chang, F.-L. F., and Greenough, W. T. (1984). Transient and enduring morphological correlates of synaptic activity and efficacy change in the rat hippocampal slice. Brain Res. 309, 35-46. doi: 10.1016/0006-8993(84) 91008-4
31. 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
32. Chen, L. Y., Rex, C. S., Sanaiha, Y., Lynch, G., and Gall, C. M. (2010b). Learning induces neurotrophin signaling at hippocampal synapses. Proc. Natl. Acad. Sci. U.S.A. 107, 7030-7035. doi: 10.1073/pnas.0912973107
33. Chen, T. J., Gehler, S., Shaw, A. E., Bamburg, J. R., and Letourneau, P. C. (2006). Cdc42 participates in the regulation of ADF/cofilin and retinal growth cone filopodia by brain derived neurotrophic factor. J. Neurobiol. 66, 103-114. doi: 10.1002/neu.20204
34. Clarke, N. A., and Francis, P. T. (2005). Cholinergic and glutamatergic drugs in Alzheimer's disease therapy. Expert Rev. Neurother. 5, 671-682. doi: 10.1586/14737175.5.5.671
35. Commins, S., Cunningham, L., Harvey, D., and Walsh, D. (2003). Massed but not spaced training impairs spatial memory. Behav. Brain Res. 139, 215-223. doi: 10.1016/S0166-4328(02)00270-X
36. Cordoba Montoya, D. A., and Carrer, H. F. (1997). Estrogen facilitates induction of long term potentiation in the hippocampus of awake rats. Brain Res. 778, 430-438. doi: 10.1016/S0006-8993(97)01206-7
37. Cox, C. D., Rex, C. S., Palmer, L. C., Babayan, A. H., Pham, D. T., Corwin, S. D., et al. (2014). A map of LTP-related synaptic changes in dorsal hippocampus following unsupervised learning. J. Neurosci. 34, 3033-3041. doi: 10.1523/JNEUROSCI.4159-13.2014
38. Crystal, J. D., and Glanzman, D. L. (2013). A biological perspective on memory. Curr. Biol. 23, R728-731. doi: 10.1016/j.cub.2013.07.082
39. Dang, Y. H., Ma, X. C., Zhang, J. C., Ren, Q., Wu, J., Gao, C. G., et al. (2014). Targeting of NMDA receptors in the treatment of major depression. Curr. Pharm. Des. 19, 1-9. doi: 10.2174/1381612819666140110120435
40. Demeter, E., and Sarter, M. (2013). Leveraging the cortical choliner-gic system to enhance attention. Neuropharmacology 64, 294-304. doi: 10.1016/j.neuropharm.2012.06.060
41. 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
42. Dickinson, J. A., Kew, J. N., and Wonnacott, S. (2008). Presynaptic alpha 7-and beta 2-containing nicotinic acetylcholine receptors modulate excitatory amino acid release from rat prefrontal cortex nerve terminals via distinct cellular mechanisms. Mol. Pharmacol. 74, 348-359. doi: 10.1124/mol.108. 046623
43. Ding, Z. B., Wu, P., Luo, Y. X., Shi, H. S., Shen, H. W., Wang, S. J., et al. (2013). Region-specific role of Rac in nucleus accumbens core and basolateral amygdala in consolidation and reconsolidation of cocaine-associated cue memory in rats. Psychopharmacology (Berl). 228, 427-437. doi: 10.1007/s00213-013-3050-8
44. Dravid, S. M., Burger, P. B., Prakash, A., Gaballe, M. T., Yadav, R., Le, P., et al. (2010). Structural determinants of D-cycloserine efficacy at the NR1/NR2C NMDA receptors. J. Neurosci. 30, 2741-2754. doi: 10.1523/JNEUROSCI.5390-09.2010
45. Dunwiddie, T. V., and Haas, H. L. (1985). Adenosine increases synaptic facilitation in the in vitro rat hippocampus: evidence for a presynaptic site of action. J. Physiol. (Lond). 369, 365-377.
46. Eichenbaum, H., and Robitsek, R. J. (2009). Olfactory memory: a bridge between humans and animals in models of cognitive aging. Ann. N.Y. Acad. Sci. 1170, 658-663. doi: 10.1111/j.1749-6632.2009.04012.x
47. Fedulov, V., Rex, C. S., Simmons, D. A., Palmer, L., Gall, C. M., and Lynch, G. (2007). Evidence that long-term potentiation occurs within individual hippocampal synapses during learning. J. Neurosci. 27, 8031-8039. doi: 10.1523/JNEUROSCI.2003-07.2007
48. Flood, J. G., Morley, J. E., and Langhorn, T. H. (1992). Effect on memory processing by D-cycloserine, an agonist of the NMDA/glycine rceptor. Eur. J. Pharmacol. 221, 249-254. doi: 10.1016/0014-2999(92)90709-D
49. Foy, M. R., Xu, J., Xie, X., Brinton, R. D., Thompson, R. F., and Berger, T. W. (1999). 17beta-estradiol enhances NMDA receptor-mediated EPSPs and long-term potentiation. J. Neurophysiol. 81, 925-929.
50. Frey, U., and Morris, R. G. M. (1997). Synaptic tagging and long-term potentiation. Nature 385, 533-536. doi: 10.1038/385533a0
51. Frye, C. A., Duffy, C. K., and Walf, A. A. (2007). Estrogens and progestins enhance spatial learning of intact and ovariectomized rats in the object placement task. Neurobiol. Learn. Mem. 88, 208-216. doi: 10.1016/j.nlm.2007. 04.003
52. Gall, C. M. (1992). Regulation of brain neurotrophin expression by physiological activity. Trends Pharmacol. Sci. 13, 401-403. doi: 10.1016/0165-6147(92) 90123-N
53. Gioanni, Y., Rougeot, C., Clarke, P. B., Lepouse, C., Thierry, A. M., and Vidal, C. (1999). Nicotinic receptors in the rat prefrontal cortex: increase in glutamate release and facilitation of mediodorsal thalamo-cortical transmission. Eur. J. Neurosci. 11, 18-30. doi: 10.1046/j.1460-9568.1999.00403.x
54. Gold, P. E. (2008). Protein synthesis and memory. Introduction. Neurobiol. Learn. Mem. 89, 199-200. doi: 10.1016/j.nlm.2007.12.005
55. Gold, P. E., and Wrenn, S. M. (2012). Cycloheximide impairs and enhances memory depending on dose and footshock intensity. Behav. Brain Res. 233, 293-297. doi: 10.1016/j.bbr.2012.05.010
56. Granger, R., Deadwyler, S., Davis, M., Moskovitz, B., Kessler, M., Rogers, G., et al. (1996). Facilitation of glutamate receptors reverses an age-associated memory impairment in rats. Synapse 22, 332-337. doi: 10.1002/(SICI)1098-2396(199604)22:4%3C332::AID-SYN4%3E3.0.CO;2-C
57. Granger, R., Staubli, U., Davis, M., Perez, Y., Nilsson, 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
58. Grodstein, F. (2013). Hormone therapy in younger women and cognitive health. JAMA Intern. Med. 173, 1437-1438. doi: 10.1001/jamainternmed.20 13.6827
59. Guzowski, J. F., Setlow, B., Wagner, E. K., and McGaugh, J. L. (2001). Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c-fos, and zif268. J. Neurosci. 21, 5089-5098.
60. Haditsch, U., Anderson, M. P., Freewoman, J., Cord, B., Babu, H., Brakebusch, C., et al. (2013). Neuronal Rac1 is required for learning-evoked neurogenesis. J. Neurosci. 33, 12229-12241. doi: 10.1523/JNEUROSCI.2939-12.2013
61. Hall, R. A., Kessler, M., Quan, A., Ambros-Ingerson, J., and Lynch, G. (1993). Cyclothiazide decreases [3H]AMPA binding to rat brain membranes: evidence that AMPA receptor desensitization increases agonist affinity. Brain Res. 628, 345-348. doi: 10.1016/0006-8993(93)90978-V
62. Hampson, R. E., Song, D., Opris, L., Santos, L. M., Shin, D. C., Gerhardt, G. A., et al. (2013). Facilitation of memory encoding in primate hippocampus by a neuro-prosthesis that promotes task-specific neural firing. J. Neural Eng. 10, 066013. doi: 10.1088/1741-2560/10/6/066013
63. Hampson, R., Rogers, G., Lynch, G., and Deadwyler, S. (1998a). Facilitative effects of the ampakine CX516 on short-term memory in rats: enhancement of delayed-nonmatch-to-sample performance. J. Neurosci. 18, 2740-2747.
64. Hampson, R., Rogers, G., Lynch, G., and Deadwyler, S. (1998b). Facilitative effects of the ampakine CX516 on short-term memory in rats: correlations with hippocampal neuronal activity. J. Neurosci. 18, 2748-2763.
65. Hara, Y., Yuk, F., Puri, R., Janssen, W. G., Rapp, P. R., and Morrison, J. H. (2014). Presynaptic mitochondrial morphology in monkey prefrontal cortex correlates with working memory and is improved with estrogen treatment. Proc. Natl. Acad. Sci. U.S.A. 111, 486-491. doi: 10.1073/pnas.1311310110
66. Harvey, C. D., and Svoboda, K. (2007). Locally dynamic synaptic learning rules in pyramidal neuron dendrites. Nature 450, 1195-1200. doi: 10.1038/nature 06416
67. Hasselmo, M. E. (2006). The role of acetylcholine in learning and memory. Curr. Opin. Neurobiol. 16, 710-715. doi: 10.1016/j.conb.2006.09.002
68. Hess, U. S., Whalen, S. P., Sandoval, L. M., Lynch, G., and Gall, C. M. (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
69. Hintzman, D. L. (1976). "Repetition and memory," in The Psychology of Learning and Motivation, ed G. H. Bower (New York, NY: Academic Press; Elsevier), 47-91.
70. Holmes, A. D., Copland, D. A., Silburn, P. A., and Chenery, H. J. (2011). Acute nicotine enhances strategy-based semantic processing in Parkinson's disease. Int. J. Neuropsychopharmacol. 14, 877-885. doi: 10.1017/S14611457100 01665
71. Hosseini, R., Benton, D. C., Dunn, P. M., Jenkinson, D. H., and Moss, G. W. (2001). SK3 is an important component of K(+) channels mediating the after-hyperpolarization in cultured rat SCG neurones. J. Physiol. 535, 323-334. doi: 10.1111/j.1469-7793.2001.00323.x
72. Ikonen, S., and Riekkinen, P. Jr. (1999). Effects of apamin on memory processing of hippocampal-lesioned mice. Eur. J. Pharmacol. 382, 151-156. doi: 10.1016/S0014-2999(99)00616-0
73. Ingvar, M., Ambros-Ingerson, J., Davis, M., Granger, R., Kessler, M., Rogers, G. A., et al. (1997). Enhancement by an ampakine of memory encoding in humans. Exp. Neurol. 146, 553-559. doi: 10.1006/exnr.1997.6581
74. 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
75. Jia, Y., Gall, C. M., and Lynch, G. (2010). Presynaptic BDNF promotes postsynaptic long-term potentiation in the dorsal striatum. J. Neurosci. 30, 14440-14445. doi: 10.1523/JNEUROSCI.3310-10.2010
76. Jiang, M., Peng, Q., Liu, X., Jin, J., Hou, Z., Zhang, J., et al. (2013). Small-molecule TrkB receptor agonists improve motor function and extend survival in a mouse model of Huntington's disease. Hum. Mol. Genet. 22, 2462-2470. doi: 10.1093/hmg/ddt098
77. 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
78. Jung, M. W., Larson, J., and Lynch, G. (1990). Long-term potentiation of monosynaptic EPSPs in rat piriform cortex in vitro. Synapse 6, 279-283. doi: 10.1002/syn.890060307
79. Katche, C., Bekinschtein, P., Slipczuk, L., Goldin, A., Izquierdo, I. A., Cammarota, M., et al. (2010). Delayed wave of c-Fos expression in the dorsal hippocampus involved specifically in persistence of long-term memory storage. Proc. Natl. Acad. Sci. U.S.A. 107, 349-354. doi: 10.1073/pnas.09129 31107
80. Katche, C, Goldin, A., Gonzalez, C, Bekinschtein, P., and Medina, J. H. (2012). Maintenance of long-term memory storage is dependent on late posttraining Egr-1 expression. Neurobiol Learn. Mem. 98, 220-227. doi: 10.1016/j.nlm.2012.08.001
81. Kessler, M., Baudry, M., and Lynch, G. (1989). Quinoxaline derivatives are high-affinity antagonists of the NMDA receptor-associated glycine sites. Brain Res. 489, 377-382. doi: 10.1016/0006-8993(89) 90875-5
82. ;-nucleotidase (CD73) reveals direct action potential-dependent adenosine release. J. Neurosci. 32, 3842-3847. doi: 10.1523/JNEUROSCI.6052-11.2012
83. 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
84. Kowalczyk, T., Bocian, R., andKonopacki, J. (2013). The generation of thetarhythm in hippocampal formation maintained in vitro. Eur. J. Neurosci. 37, 679-699. doi: 10.1111/ejn.12091
85. 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
86. Kramar, E. A., Chen, L. Y., Brandon, N. J., Rex, C. S., Liu, F., Gall, C. M., et al. (2009). Cytoskeletal changes underlie estrogen's acute effects on synaptic transmission and plasticity. J. Neurosci. 29, 12982-12993. doi: 10.1523/JNEUROSCI.3059-09.2009
87. 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
88. Kramar, E. A., Lin, B., Lin, C. Y., Arai, A. C, Gall, C. M., and Lynch, G. (2004). A novel mechanism for the facilitation of theta-induced long-term potentiation by brain-derived neurotrophic factor. J. Neurosci. 24, 5151-5161. doi: 10.1523/JNEUROSCI.0800-04.2004
89. 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
90. Kramar, E. A., and Lynch, G. (2003). Developmental and regional differences in the consolidation of long-term potentiation. Neuroscience 118, 387-398. doi: 10.1016/S0306-4522(02)00916-8
91. Labrie, V., and Roder, J. C. (2010). The involvement of the NMDA receptor d-serine/glycine site in the pathophysiology and treatment of schizophrenia. Neurosci. Biobehav. Rev. 34, 351-372. doi: 10.1016/j.neubiorev.2009. 08.002
92. 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
93. 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.
94. Lee, K., Oliver, M., Schottler, F., Creager, R., and Lynch, G. (1979). Ultrastructural effects of repetitive synaptic stimulation in the hippocampal slice preparation: a preliminary report. Exp. Neurol 65, 478-480. doi: 10.1016/0014-4886(79)90114-6
95. Lee, K., Schottler, F., Oliver, M., and Lynch, G. (1980). Brief bursts of high-frequency stimulation produce two types of structural changes in rat hippocampus. J. Neurophysiol. 44, 247-258.
96. 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
97. Liu, F., Day, M., Muniz, L. C, Bitran, D., Arias, R., Revilla-Sanchez, R., et al. (2008). Activation of estrogen receptor-beta regulates hippocampal synaptic plasticity and improves memory. Nat Neurosci. 11, 334-343. doi: 10.1038/ nn2057
98. Lynch, G. (1998). Memory and the brain: unexpected chemistries and a new pharmacology. Neurobiol Learn. Mem. 70, 82-100. doi: 10.1006/nlme.19 98.3840
99. Lynch, G. (2004a). AMPA receptor modulators as cognitive enhancers. Curr. Opin. Pharmacol 4, 4-11. doi: 10.1016/j.coph.2003.09.009
100. Lynch, G., and Gall, C. M. (2013). Mechanism based approaches for rescuing and enhancing cognition. Front. Neurosci. 7:143. doi: 10.3389/fnins.2013. 00143
101. Lynch, G., Kramar, E. A., Babayan, A. H., Rumbaugh, G., and Gall, C. M. (2013). Differences between synaptic plasticity thresholds result in new timing rules for maximizing long-term potentiation. Neuropharmacology 64, 27-36. doi: 10.1016/j.neuropharm.2012.07.006
102. 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
103. Lynch, M. A. (2004b). Long-term potentiation and memory. Physiol. Rev. 84, 87-136. doi: 10.1152/physrev.00014.2003
104. Madau, P., Clark, A. G., Neale, S. A., Smith, L., Hamilton, N., Thompson, F., et al. and Lambert, J. J. (2009). "Program no. 613.2. Org 1, Org 2, and Org 3 potentiate NMDA-receptor mediated responses in vitro," in Society for Neuroscience Annual Meeting Planner (Chicago, IL: Society for Neuroscience).
105. 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
106. McQuown, S. C., Barrett, R. M., Matheos, D. P., Post, R. J., Rogge, G. A., Alenghat, T., et al. (2011). HDAC3 is a critical negative regulator of long-term memory formation. J. Neurosci. 31, 764-774. doi: 10.1523/JNEUROSCI.5052-10.2011
107. Monaghan, D. T., Irvine, M. W., Costa, B. M., Fang, G., and Jane, D. E. (2012). Pharmacological modulation of NMDA receptor activity and the advent of negative and positive allosteric modulators. Neurochem. Int. 61, 581-592. doi: 10.1016/j.neuint.2012.01.004
108. Morris, R. G. (2003). Long-term potentiation and memory. Philos. Trans. R. Soc. Lond. B Biol. Sci. 358, 643-647. doi: 10.1098/rstb.20 02.1230
109. Noetzli, M., and Eap, C. B. (2013). Pharmacodynamic, pharmacokinetic and pharmacogenetic aspects of drugs used in the treatment of Alzheimer's disease. Clin. Pharmacokinet. 52, 225-241. doi: 10.1007/s40262-013-0038-9
110. Normann, C., and Berger, M. (2008). Neuroenhancement: status quo and perspectives. Eur. Arch. Psychiatry Clin. Neurosci. 258(Suppl. 5), 110-114. doi: 10.1007/s00406-008-5022-2
111. Oliver, M. W., Kessler, M., Larson, J., Schottler, F., and Lynch, G. (1990). Glycine site associated with the NMDA receptor modulates long-term potentation. Synapse 5, 265-270. doi: 10.1002/syn.890050403
112. Olpe, H. R., Klebs, K., Kung, E., Campiche, P., Glatt, A., Ortmann, R., et al. (1987). Cholinomimetics induce theta rhythm and reduce hippocampal pyramidal cell excitability. Eur. J. Pharmacol. 142, 275-283. doi: 10.1016/0014-2999(87) 90117-8
113. Ooishi, Y., Kawato, S., Hojo, Y., Hatanaka, Y., Higo, S., Murakami, G., et al. (2012). Modulation of synaptic plasticity in the hippocampus by hippocampus-derived estrogen and androgen. J. Steroid Biochem. Mol. Biol. 131, 37-51. doi: 10.1016/j.jsbmb.2011.10.004
114. 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
115. Paul, S. M., Doherty, J. J., Robichaud, A. J., Belfort, G. M., Chow, B. Y., Hammond, R. S., et al. (2013). The major brain cholesterol metabolite 24(s)-hydroxycholesterol is a potent allosteric modulator of n-methyl-d-aspartate receptors. J. Neurosci. 33, 17290-17300. doi: 10.1523/JNEUROSCI.2619-13.2013
116. Perlmutter, L. S., Siman, R., Gall, C., Seubert, P., Baudry, M., and Lynch, G. (1988). The ultrastructural localization of calcium-activated protease 'calpain' in rat brain. Synapse 2, 79-88. doi: 10.1002/syn.890020111
117. Peters, J., and De Vries, T. J. (2013). D-cycloserine administration directly to infralimbic medial prefrontal cortex enhances extinction memory in sucrose-seeking animals. Neuroscience 230, 24-30. doi: 10.1016/j.neuroscience.2012. 11.004
118. Plath, N., Ohana, O., Dammermann, B., Errington, M. L., Schmitz, D., Gross, C., et al. (2006). Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories. Neuron 52, 437-444. doi: 10.1016/j.neuron.2006.08.024
119. 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
120. 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
121. 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
122. 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
123. 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
124. 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
125. Rioult-Pedotti, M. S., Friedman, D., and Donoghue, J. P. (2000). Learning-induced LTP in neocortex. Science 290, 533-536. doi: 10.1126/science.290.5491.533
126. Roman, F., Staubli, U., and Lynch, G. (1987). Evidence for synaptic potentiation in a cortical network during learning. Brain Res. 418, 221-226. doi: 10.1016/0006-8993(87)90089-8
127. Routtenberg, A. (2008). The substrate for long-lasting memory: if not protein synthesis, then what? Neurobiol. Learn. Mem. 89, 225-233. doi: 10.1016/j.nlm.2007.10.012
128. Sarter, M., Parikh, V., and Howe, W. M. (2009). Nachr agonist-induced cognition enhancement: integration of cognitive and neuronal mechanisms. Biochem. Pharmacol. 78, 658-667. doi: 10.1016/j.bcp.2009.04.019
129. Schmid, D. A., Yang, T., Ogier, M., Adams, I., Mirakhur, Y., Wang, Q., et al. (2012). A TrkB small molecule partial agonist rescues TrkB phosphory-lation deficits and improves respiratory function in a mouse model of Rett syndrome. J. Neurosci. 32, 1803-1810. doi: 10.1523/JNEUROSCI.0865-11.2012
130. Schmitz, D., Mellor, J., Breustedt, J., and Nicoll, R. A. (2003). Presynaptic kainate receptors impart an associative property to hippocampal mossy fiber long-term potentiation. Nat. Neurosci. 6, 1058-1063. doi: 10.1038/nn1116
131. 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
132. Seese, R. R., Chen, L. Y., Cox, C. D., Schulz, D., Babayan, A. H., Bunney, W. E., et al. (2013). Synaptic abnormalities in the infralimbic cortex of a model of congenital depression. J. Neurosci. 33, 13441-13448. doi: 10.1523/JNEUROSCI.2434-13.2013
133. Sheinin, A., Shavit, S., and Benveniste, M. (2001). Subunit specificity and mechanism of action of NMDA partial agonist D-cycloserine. Neuropharmacology 41, 151-158. doi: 10.1016/S0028-3908(01)00073-9
134. Shires, K. L., Da Silva, B. M., Hawthorne, J. P., Morris, R. G. M., and Martin, S. J. (2012). Synaptic tagging and capture in the living rat. Nature Comm. 3:1246. doi: 10.1038/ncomms2250
135. 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
136. Simmons, D. A., Belichenko, N. P., Yang, T., Condon, C., Monbureau, M., Shamloo, M., et al. (2013). A small molecule TrkB ligand reduces motor impairment and neuropathology in R6/2 and BACHD mouse models of Huntington's disease. J. Neurosci. 33, 18712-18727. doi: 10.1523/JNEUROSCI.1310-13.2013
137. 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 pheno-types in R6/2 mice. Neurobiol. Dis. 41, 436-444. doi: 10.1016/j.nbd.2010.10.015
138. 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
139. Sirvio, J., Larson, J., Quach, C. N., Rogers, G. A., and Lynch, G. (1996). Effects of pharmacologically facilitating glutamatergic transmission in the trisynap-tic intrahippocampal circuit. Neuroscience 74, 1025-1035. doi: 10.1016/0306-4522(96)00170-4
140. Snider, J., Plank, M., Lynch, G., Halgren, E., and Poizner, H. (2013). Human cortical theta during free exploration encodes space and predicts subsequent memory. J. Neurosci. 33, 15056-15068. doi: 10.1523/JNEUROSCI.0268-13.2013
141. Staubli, U. (1992). A peculiar form of potentiation in mossy fiber synapses. Epilepsy Res. Suppl. 7, 151-157.
142. Staubli, U., and Lynch, G. (1987). Stable hippocampal long-term potentia-tion elicited by 'theta' pattern stimulation. Brain Res. 435, 227-234. doi: 10.1016/0006-8993(87)91605-2
143. Staubli, U., Rogers, G., and Lynch, G. (1994). Facilitation of glutamate receptors enhances memory. Proc. Natl. Acad. Sci. U.S.A. 91, 777-781. doi: 10.1073/pnas.91.2.777
144. Staubli, U., and Xu, F. B. (1995). Effects of 5-HT3 receptor antagonism on hip-pocampal theta rhythm, memory, and LTP induction in the freely moving rat. J. Neurosci. 15, 2445-2452.
145. Stefanko, D. P., Barrett, R. M., Ly, A. R., Reolon, G. K., and Wood, M. A. (2009). Modulation of long-term memory for object recognition via HDAC inhibition. Proc. Natl. Acad. Sci. U.S.A. 106, 9447-9452. doi: 10.1073/pnas.0903964106
146. Stephan, H., Frahm, H., and Baron, G. (1981). New and revised data on volumes of brain structures in insectivores and primates. Folia Primatol. 35, 1-29. doi: 10.1159/000155963
147. Sugrue, L. P., Corrado, G. S., and Newsome, W. T. (2005). Choosing the greater of two goods: neural currencies for valuation and decision making. Nat. Rev. Neurosci. 6, 363-375. doi: 10.1038/nrn1666
148. Sun, Y., Olson, R., Horning, M., Armstrong, N., Mayer, M., and Gouaux, E. (2002). Mechanism of glutamate receptor desensitization. Nature 417, 245-253. doi: 10.1038/417245a
149. Swanson, L. W. (1995). Mapping the human brain: past, present, and future. Tr e n d s Neurosci. 18, 471-474. doi: 10.1016/0166-2236(95)92766-J
150. Thompson, R. F., Berger, T. W., Cegavske, C. F., Patterson, M. M., Roemer, R. A., Teyler, T. J., et al. (1976). The search for the engram. Am. Psychol. 31, 209-226. doi: 10.1037/0003-066X.31.3.209
151. Thompson, R. F., and Krupa, D. J. (1994). Organization of memory traces in the mammalian brain. Ann. Rev. Neurosci. 17, 519-549. doi: 10.1146/annurev.ne.17.030194.002511
152. Tsai, G. E., Falk, W. E., Gunther, J., and Coyle, J. T. (1999). Improved cognition in Alzheimer's disease with sort-term D-cycloserine treatment. Am. J. Psychiatry 156, 467-469.
153. Tsunada, J., and Sawaguchi, T. (2012). Neuronal categorization and discrimination of social behaviors in primate prefrontal cortex. PLoS ONE 7:e52610. doi: 10.1371/journal.pone.0052610
154. Tully, T., Bourtchouladze, R., Scott, R., and Tallman, J. (2003). Targeting the CREB pathway for memory enhancers. Nat. Rev. Drug Discov. 2, 267-277. doi: 10.1038/nrd1061
155. Turner, D. C., Clark, L., Pomarol-Clotet, E., McKenna, P., Robbins, T. W., and Sahakian, B. J. (2004). Modafinil improves cognition and attentional set shifting in patients with chronic schizophrenia. europsychopharmacology 29, 1363-1373. doi: 10.1038/sj.npp.1300457
156. Vertes, R. P. (2005). Hippocampal theta rhythm: a tag for short-term memory. Hippocampus. 15, 923-935. doi: 10.1002/hipo.20118
157. Vick, K. A. T., Guidi, M., and Stackman, R. W. Jr. (2010). In vivo pharmacological manipulation of small conductance Ca(2+)-activated K(+) channels influences motor behavior, object memory and fear conditioning. Neuropharmacology 58, 650-659. doi: 10.1016/j.neuropharm.2009.11.008
158. Vierk, R., Glassmeier, G., Zhou, L., Brandt, N., Fester, L., Dudzinski, D., et al. (2012). Aromatase inhibition abolishes LTP generation in female but not in male mice. J. Neurosci. 32, 8116-8126. doi: 10.1523/JNEUROSCI.5319-11.2012
159. Wall, M. J., and Dale, N. (2013). Neuronal transporter and astrocytic ATP exocyto-sis underlie activity-dependent adenosine release in the hippocampus. J. Physiol. 591, 3853-3871. doi: 10.1113/jphysiol.2013.253450
160. Whitlock, J. R., Heynen, A. J., Shuler, M. G., and Bear, M. F. (2006). Learning induces long-term potentiation in the hippocampus. Science 313, 1093-1097. doi: 10.1126/science.1128134
161. Wonnacott, S. (1997). Presynaptic nicotinic ACh receptors. Trends Neuro sci. 20, 92-98. doi: 10.1016/S0166-2236(96)10073-4
162. Wu, F. S., Gibbs, T. T., and Farb, D. H. (1991). Pregnenolone sulfate: a positive allosteric modulator at the n-methyl-d-aspartate receptor. Mol. Pharmacol. 40, 333-336.
163. Zeeb, F. D., Robbins, T. W., and Winstanley, C. A. (2009). Serotonergic and dopaminergic modulation of gambling behavior as assessed using a novel rat gambling task. Neuropsychopharmacology 34, 2329-2343. doi: 10.1038/npp.2009.62