Mechanisms of memory enhancement

Wiley Interdisciplinary Reviews: Systems Biology and Medicine

Volumn 5, Issue 1, 2013, Pages 37-53

  Stern, Sarah A ^a,b   Alberini, Cristina M ^a  

^a NEW YORK UNIVERSITY   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; ADRENALIN; AMPA RECEPTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DOPAMINE; GLUCOSE; HYDROCORTISONE; INSULIN; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

BEHAVIOR; GENE EXPRESSION; HUMAN; LONG TERM MEMORY; MEMORY; MEMORY CONSOLIDATION; NEUROMODULATION; NONHUMAN; REVIEW; SYNAPSE;

ANIMALS; COGNITIVE THERAPY; EXERCISE THERAPY; HUMANS; MEMORY; MEMORY DISORDERS; NEUROTRANSMITTER AGENTS;

ANIMALIA;

EID: 84871396748     PISSN: 19395094     EISSN: 1939005X     Source Type: Journal    
DOI: 10.1002/wsbm.1196     Document Type: Review

References (103)

1. Alberini CM. Transcription factors in long-term memory and synaptic plasticity. Physiol Rev 2009, 89:121-145.
2. Bliss TVP, Collingridge GL. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 1993, 361:31-39.
3. Ressler KJ, Mayberg HS. Targeting abnormal neural circuits in mood and anxiety disorders: from the laboratory to the clinic. Nature Neurosci 2007, 10: 1116-1124.
4. Lee Y-S, Silva AJ. The molecular and cellular biology of enhanced cognition. Nature Rev Neurosci 2009, 10: 126-140.
5. Cooke SF, Bliss TVP. Cellular and molecular life sciences visions & reflections the genetic enhancement of memory. Neuropharmacology 2003, 60:1-5.
6. Ebbinghaus H. Memory: A Contribution to Experimental Psychology. Teachers College, Columbia University; 1913.
7. Cowan N. What are the differences between long-term, short-term, and working memory? Prog Brain Res 2008, 169:323-338.
8. McGaugh JL. Memory-a century of consolidation. Science 2000, 287:248-251.
9. Nader K, Einarsson EO. Memory reconsolidation: an update. Ann N Y Acad Sci 2010, 1191:27-41.
10. Lynch G, Palmer LC, Gall CM. The likelihood of cognitive enhancement. Pharmacol Biochem Behav 2011, 99:116-129.
11. Simard M, Reekum RV. Memory assessment in studies of cognition-enhancing drugs for Alzheimer's disease. Drugs Aging 1999, 14:197-230.
12. Carlesimo GA, Oscar-Berman M. Memory deficits in Alzheimer's patients: a comprehensive review. Neuropsychol Rev 1992, 3:119-169.
13. Perry RJ, Hodges JR. Attention and executive deficits in Alzheimer's disease: a critical review. Brain 1999, 122:383-404.
14. Dubois B, Pillon B. Cognitive deficits in Parkinson's disease. J Neurol 1997, 244:2-8.
15. Cansino S. Episodic memory decay along the adult lifespan: a review of behavioral and neurophysiological evidence. Int J Psychophysiol 2009, 71:64-69.
16. Light LL. Memory and aging: four hypotheses in search of data. Annu Rev Psychol 1991, 42:333-376.
17. Squire LR. Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 1992, 99:195-231.
18. Corkin S, Amaral DG, Gonzalez RG, Johnson KA, Hyman BT. H.M.'s medial temporal lobe lesion: findings from magnetic resonance imaging. J Neurosci 1997, 17:3964-3979.
19. White NM, McDonald RJ. Multiple parallel memory systems in the brain of the rat. Neurobiol Learn Mem 2002, 77:125-184.
20. Davis HP, Squire LR. Protein synthesis and memory: a review. Psychol Bullet 1984, 96:518-559.
21. Villers A, Godaux E, Ris L. Long-lasting LTP requires neither repeated trains for its induction nor protein synthesis for its development. PloS One 2012, 7: e40823.
22. Alberini CM. The role of protein synthesis during the labile phases of memory: revisiting the skepticism. Neurobiol Learn Mem 2008, 89:234-246.
23. Sharma AV, Nargang FE, Dickson CT. Neurosilence: profound suppression of neural activity following intracerebral administration of the protein synthesis inhibitor anisomycin. J Neurosci 2012, 32: 2377-2387.
24. Alberini CM, Chen DY. Memory enhancement: consolidation, reconsolidation and insulin-like growth factor 2. TrendNeurosci 2012, 35:274-283.
25. Bartsch D, Ghirardi M, Skehel PA, Karl KA, Herder SP, Chen M, Bailey CH, Kandel ER. Aplysia CREB2 represses long-term facilitation: relief of repression converts transient facilitation into long-term functional and structural change. Cell 1995, 83:979-992.
26. Yin JC, Del Vecchio M, Zhou H, Tully T. CREB as a memory modulator: induced expression of a dCREB2 activator isoform enhances long-term memory in Drosophila. Cell 1995, 81:107-115.
27. Josselyn Sa, Shi C, Carlezon Wa, Neve RL, Nestler EJ, Davis M. Long-term memory is facilitated by cAMP response element-binding protein overexpression in the amygdala. J Neurosci 2001, 21:2404-2412.
28. Brightwell JJ, Smith Ca, Neve RL, Colombo PJ. Long-term memory for place learning is facilitated by expression of cAMP response element-binding protein in the dorsal hippocampus. Learn Mem 2007, 14: 195-199.
29. Lee J-A, Kim H, Kim K, Han J. Overexpression of and RNA interference with the CCAAT enhancer-binding protein on long-term facilitation of Aplysia sensory to motor synapses. Learn Mem 2001, 8:220-226.
30. Chen A, Muzzio Ia, Malleret G, Bartsch D, Verbitsky M, Pavlidis P, Yonan AL, Vronskaya S, Grody MB, Cepeda I, 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 2003, 39:655-669.
31. Xia M, Huang R, Guo V, Southall N, Cho M-H, Inglese J, Austin CP, Nirenberg M. Identification of compounds that potentiate CREB signaling as possible enhancers of long-term memory. Proc Natl Acad Sci 2008, 106:2412-2417.
32. Wang M, Gamo NJ, Yang Y, Jin LE, Wang XJ, Laubach M, Mazer JA, Lee D, Arnsten AF. Neuronal basis of age-related working memory decline. Nature 2011, 476:210-213.
33. Malleret G, Haditsch U, Genoux D, Jones MW, Bliss TV, Vanhoose aM, Weitlauf C, Kandel ER, Winder DG, Mansuy IM. Inducible and reversible enhancement of learning, memory, and long-term potentiation by genetic inhibition of calcineurin. Cell 2001, 104: 675-686.
34. Sharma SK, Bagnall MW, Sutton Ma, Carew TJ. Inhibition of calcineurin facilitates the induction of memory for sensitization in Aplysia: requirement of mitogen-activated protein kinase. Proc Natl Acad Sci U S A 2003, 100:4861-4866.
35. Tully T, Bourtchouladze R, Scott R, Tallman J. Targeting the CREB pathway for memory enhancers. Nature Rev Drug Disc 2003, 2:267-277.
36. Chen DY, Stern Sa, Garcia-Osta A, Saunier-Rebori B, Pollonini G, Bambah-Mukku D, Blitzer RD, Alberini CM. A critical role for IGF-II in memory consolidation and enhancement. Nature 2011, 469:491-497.
37. Barco A, Pittenger C, Kandel ER. CREB, memory enhancement and the treatment of memory disorders: promises, pitfalls and prospects. Expert OpinTherap Targets 2003, 7:101-114.
38. Lamprecht R, LeDoux J. Structural plasticity and memory. Nature Rev Neurosci 2004, 5:45-54.
39. Tang YP, Shimizu E, Dube GR, Rampon C, Kerchner Ga, Zhuo M, Liu G, Tsien JZ. Genetic enhancement of learning and memory in mice. Nature 1999, 401: 63-69.
40. Cui Y, Jin J, Zhang X, Xu H, Yang L, Du D, Zeng Q, Tsien JZ, Yu H, Cao X. Forebrain NR2B overexpression facilitating the prefrontal cortex long-term potentiation and enhancing working memory function in mice. PloS One 2011, 6:e20312.
41. Riedel G, Platt B, Micheau J. Glutamate receptor function in learning and memory. Behav Brain Res 2003, 140:1-47.
42. Danysz W, Zajaczkowski W, Parsons CG. Modulation of leaning processes by ionotropic glutamate receptor ligands. Behav Pharmocol 1995, 6:455-474.
43. Izquierdo I. Pharmacological in memory evidence for a role of long-term potentiation. FASEB J 1994, 8: 1139-1145.
44. Wang D, Cui Z, Zeng Q, Kuang H, Wang LP, Tsien JZ, Cao X. Genetic enhancement of memory and long-term potentiation but not CA1 long-term depression in NR2B transgenic rats. PloS One 2009, 4:e7486.
45. Burgdorf J, Zhang X-l, Weiss C, Matthews E, Disterhoft JF, Stanton PK, Moskal JR. The N-methyl-d-aspartate receptor modulator GLYX-13 enhances learning and memory in young adult and learning impaired aged rats. Neurobiol Aging 2011, 21: 698-706.
46. Kalisch R, Holt B, Petrovic P, De Martino B, Klöppel S, Büchel C, Dolan RJ. The NMDA agonist d-cycloserine facilitates fear memory consolidation in humans. Cerebral Cortex 2009, 19:187-196.
47. Yamamoto S, Morinobu S, Fuchikami M, Kurata A, Kozuru T, Yamawaki S. Effects of single prolonged stress and d-cycloserine on contextual fear extinction and hippocampal NMDA receptor expression in a rat model of PTSD. Neuropsychopharmacology 2008, 33: 2108-2116.
48. Rao VR, Finkbeiner S. NMDA and AMPA receptors: old channels, new tricks. Trends Neurosci 2007, 30: 284-291.
49. Migues PV, Hardt O, Wu DC, Gamache K, Sacktor TC, Wang YT, Nader K. PKMzeta maintains memories by regulating GluR2-dependent AMPA receptor trafficking. Nature Neurosci 2010, 13:630-634.
50. Shema R, Haramati S, Ron S, Hazvi S, Chen A, Sacktor TC, Dudai Y. Enhancement of consolidated long-term memory by overexpression of protein kinase Mzeta in the neocortex. Science 2011, 331:1207-1210.
51. Ehlers MD. Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting. Neuron 2000, 28:511-525.
52. Lynch G. Glutamate-based therapeutic approaches: ampakines. Curr Opin Pharmacol 2006, 6:82-88.
53. Slutsky I, Abumaria N, Wu L-J, Huang C, Zhang L, Li B, Zhao X, Govindarajan A, Zhao M-G, Zhuo M, et al. Enhancement of learning and memory by elevating brain magnesium. Neuron 2010, 65:165-177.
54. Hu H, Real E, Takamiya K, Kang M-G, Ledoux J, Huganir RL, Malinow R. Emotion enhances learning via norepinephrine regulation of AMPA-receptor trafficking. Cell 2007, 131:160-173.
55. Krugers HJ, Hoogenraad CC, Groc L. Stress hormones and AMPA receptor trafficking in synaptic plasticity and memory. Nature Rev Neurosci 2010, 11: 675-681.
56. McReynolds JR, Donowho K, Abdi A, McGaugh JL, Roozendaal B, McIntyre CK. Memory-enhancing corticosterone treatment increases amygdala norepinephrine and Arc protein expression in hippocampal synaptic fractions. Neurobiol Learn Mem 2010, 93:312-321.
57. Okuno H, Akashi K, Ishii Y, Yagishita-Kyo N, Suzuki K, Nonaka M, Kawashima T, Fujii H, Takemoto-Kimura S, Abe M, et al. Inverse synaptic tagging of inactive synapses via dynamic interaction of Arc/Arg3.1 with CaMKIIbeta. Cell 2012, 149: 886-898.
58. Diana G, Valentini G, Travaglione S, Falzano L, Pieri M, Zona C, Meschini S, Fabbri A, Fiorentini C. Enhancement of learning and memory after activation of cerebral Rho GTPases. Proc Natl Acad Sci 2007, 104:636-641.
59. Cambon K, Hansen SM, Venero C, Herrero aI, Skibo G, Berezin V, Bock E, Sandi C. A synthetic neural cell adhesion molecule mimetic peptide promotes synaptogenesis, enhances presynaptic function, and facilitates memory consolidation. J Neurosci 2004, 24: 4197-4204.
60. Bourne J, Harris KM. Do thin spines learn to be mushroom spines that remember? Curr Opin Neurobiol 2007, 17:381-386.
61. Kupfermann I. Modulatory actions of neurotransmitters. Ann Rev Neurosci 1979, 2:447-465.
62. Floresco SB, Jentsch JD. Pharmacological enhancement of memory and executive functioning in laboratory animals. Neuropsychopharmacol: Off Publ Am Coll Neuropsychopharmacol 2011, 36:227-250.
63. Mckeith IG, Burn D. Spectrum of Parkinson's disease, parkinson's dementia, and lewy body dementia. Neurol Clin 2000, 18:865-883.
64. Williams GV, Goldman-Rakic PS. Modulation of memory fields by dopamine D1 receptors in prefrontal cortex. Nature 1995, 376:572-575.
65. Castner Sa, Goldman-Rakic PS. Enhancement of working memory in aged monkeys by a sensitizing regimen of dopamine D1 receptor stimulation. J Neurosci 2004, 24:1446-1450.
66. Haycock JW, Van Buskirk R, Ryan JR, McGaugh JL. Enhancement of retention with centrally administered catecholamines. Exper Neurol 1977, 54:199-208.
67. de Lima MNM, Presti-Torres J, Dornelles A, Scalco FS, Roesler R, Garcia VA, Schröder N. Modulatory influence of dopamine receptors on consolidation of object recognition memory. Neurobiol Learn Mem 2011, 95:305-310.
68. Yang S-N. Sustained enhancement of AMPA receptor- and NMDA receptor-mediated currents induced by dopamine D1/D5 receptor activation in the hippocampus: an essential role of postsynaptic calcium. Hippocampus 2000, 10:57-63.
69. McGaugh JL, Roozendaal B. Role of adrenal stress hormones in forming lasting memories in the brain. Curr Opin Neurobiol 2002, 12:205-210.
70. Yehuda R. Post-traumatic stress disorder. New Engl J Med 2002, 346:109-114.
71. Eich TS, Metcalfe J. Effects of the stress of marathon running on implicit and explicit memory. Psych Bull Rev 2009, 16:475-479.
72. Roozendaal B, Okuda S, Van der Zee Ea, McGaugh JL. Glucocorticoid enhancement of memory requires arousal-induced noradrenergic activation in the basolateral amygdala. Proc Natl Acad Sci 2006, 103: 6741-6746.
73. Gold PE, Ruskirk RVAN. Effects of posttrial hormone injections on memory processed. Hormones Behav 1976, 7:509-517.
74. Roozendaal B, Nguyen BT, Power AE, Mcgaugh JL. Basolateral amygdala noradrenergic influence enables enhancement of memory consolidation induced by hippocampal glucocorticoid receptor activation. Proc Natl Acad Sci 1999, 96:11642-11647.
75. Linssen aMW, Vuurman EFPM, Sambeth A, Riedel WJ. Methylphenidate produces selective enhancement of declarative memory consolidation in healthy volunteers. Psychopharmacology 2011, 221:611-619.
76. Advokat C. What are the cognitive effects of stimulant medications? Emphasis on adults with attention-deficit/hyperactivity disorder (ADHD). Neurosci Biobehav Rev 2010, 34:1256-1266.
77. Deiana S, Platt B, Riedel G. The cholinergic system and spatial learning. Behav Brain Res 2011, 221:389-411.
78. Birks J. Cholinesterase inhibitors for Alzheimer's disease (review). Cochrane Library 2009, 1:CD005593.
79. Prickaerts J, Sik A, van der Staay FJ, de Vente J, Blokland A. Dissociable effects of acetylcholinesterase inhibitors and phosphodiesterase type 5 inhibitors on object recognition memory: acquisition versus consolidation. Psychopharmacology 2005, 177:381-390.
80. Lapp JE. Effects of glycemic alterations and noun imagery on the learning of paired associates. J Learn Disabilit 1981, 14:35-38.
81. Azari NP. Psychopharmacology effects of glucose on memory processes in young adults. Psychopharmacology 1991, 105:521-524.
82. Foster JK, Lidder PG, Sünram SI. Glucose and memory: fractionation of enhancement effects? Psychopharmacology 1998, 137:259-270.
83. Smith Ma, Riby LM, Eekelen JAMV, Foster JK. Glucose enhancement of human memory: a comprehensive research review of the glucose memory facilitation effect. Neurosci Biobehav Rev 2011, 35:770-783.
84. Gold PE, Vogt J, Hall JL. Glucose effects on memory: behavioral and pharmacological characteristics. Behav Neural Biol 1986, 46:145-155.
85. McNay EC, Ong CT, McCrimmon RJ, Cresswell J, Bogan JS, Sherwin RS. Hippocampal memory processes are modulated by insulin and high-fat-induced insulin resistance. NeurobiolLearn Mem 2010, 93: 546-553.
86. Benedict C, Hallschmid M, Hatke A, Schultes B, Fehm HL, Born J, Kern W. Intranasal insulin improves memory in humans. Psychoneuroendocrinology 2004, 29: 1326-1334.
87. Craft S, Asthana S, Newcomer JW, Wilkinson CW, Matos IT, Baker LD, Cherrier M, Lofgreen C, Latendresse S, Petrova a, et al. Enhancement of memory in Alzheimer disease with insulin and somatostatin, but not glucose. Arch General Psych 1999, 56: 1135-1140.
88. Craft S, Baker LD, Montine TJ, Minoshima S, Watson GS, Claxton A, Arbuckle M, Callaghan M, Tsai E, Plymate SR, et al. Intranasal insulin therapy for Alzheimer disease and amnestic mild cognitive impairment: a pilot clinical trial. Arch Neurol 2012, 69:29-38.
89. Agis-Balboa RC, Arcos-Diaz D, Wittnam J, Govindarajan N, Blom K, Burkhardt S, Haladyniak U, Agbemenyah HY, Zovoilis A, Salinas-Riester G, et al. A hippocampal insulin-growth factor 2 pathway regulates the extinction of fear memories. EMBO J 2011, 30: 4071-4083.
90. Roth Ra. Structure of the receptor for insulin-like growth factor II: the puzzle amplified. Science 1988, 239:1269-1271.
91. Hawkes C, Jhamandas JH, Harris KH, Fu W, MacDonald RG, Kar S. Single transmembrane domain insulin-like growth factor-II/mannose-6-phosphate receptor regulates central cholinergic function by activating a G-protein-sensitive, protein kinase C-dependent pathway. J Neurosci Off J Soc Neurosci 2006, 26:585-596.
92. Reinhardt RR, Bondy CA. Insulin-like growth factors cross the blood-brain barrier. Endocrinology 1994, 135:1753-1761.
93. van Praag H. Exercise and the brain: something to chew on. Trends Neurosci 2009, 32:283-290.
94. Lynch G. Memory enhancement: the search for mechanism-based drugs. Nature Neurosci 2002, 5 Suppl:1035-1038.
95. Bekinschtein P, Cammarota M, Igaz LM, Bevilaqua LR, Izquierdo I, Medina JH. Persistence of long-term memory storage requires a late protein synthesis- and BDNF-dependent phase in the hippocampus. Neuron 2007, 53:261-277.
96. Pinsker HM, Hening WA, Carew TJ, Kandel ER. Long-term sensitization of a defensive withdrawal reflex in Aplysia. Science 1973, 182:1039-1042.
97. Alberini CM, Milekic MH, Tronel S. Mechanisms of memory stabilization and de-stabilization. Cell Mol Life Sci 2006, 63:999-1008.
98. Sara SJ. Strengthening the shaky trace through retrieval. Nature Rev Neurosci 2000, 1:212-213.
99. Inda MC, Muravieva EV, Alberini CM. Memory retrieval and the passage of time: from reconsolidation and strengthening to extinction. J Neurosci: Off J Soc Neurosci 2011, 31:1635-1643.
100. Dȩbiec J, Bush DEa, LeDoux JE. Noradrenergic enhancement of reconsolidation in the amygdala impairs extinction of conditioned fear in rats-a possible mechanism for the persistence of traumatic memories in PTSD. Depression Anxiety 2011, 28:186-193.
101. Tian S, Huang F, Li P, Li Z, Zhou S, Deng H, Yang Y. Nicotine enhances contextual fear memory reconsolidation in rats. Neurosci Lett 2011, 487:368-371.
102. Leuner B, Shors TJ. New spines, new memories. Mol Neurobiol 2004, 29:117-130.
103. Mizuno K, Giese KP. Towards a molecular understanding of sex differences in memory formation. Trends Neurosci 2010, 33:285-291.