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Central Nervous System Agents in Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 1871-5249
ISSN (Online): 1875-6166

Review Article

Noradrenergic Regulation of Hippocampus-Dependent Memory

Author(s): Peter V. Nguyen and Steven A. Connor*

Volume 19, Issue 3, 2019

Page: [187 - 196] Pages: 10

DOI: 10.2174/1871524919666190719163632

Abstract

Neuromodulation regulates critical functions of CNS synapses, ranging from neural circuit development to high-order cognitive processes, including learning and memory. This broad scope of action is generally mediated through alterations of the strength of synaptic transmission (i.e. synaptic plasticity). Changes in synaptic strength are widely considered to be a cellular representation of learned information. Noradrenaline is a neuromodulator that is secreted throughout the brain in response to novelty or increased arousal. Once released, noradrenaline activates metabotropic receptors, initiating intracellular signaling cascades that promote enduring changes in synaptic strength and facilitate memory storage. Here, we provide an overview of noradrenergic modulation of synaptic plasticity and memory formation within mammalian neural circuits, which has broad applicability within the neurotherapeutics community. Advances in our understanding of noradrenaline in the context of these processes may provide a foundation for refining treatment strategies for multiple brain diseases, ranging from post-traumatic stress disorder to Alzheimer’s Disease.

Keywords: Noradrenaline, memory, hippocampus, beta-adrenergic receptors, long-term potentiation, synaptic plasticity.

Graphical Abstract
[1]
Kandel, E.R. The molecular biology of memory storage: A dialogue between genes and synapses. Science, 2001, 294(5544), 1030-1038.
[http://dx.doi.org/10.1126/science.1067020] [PMID: 11691980]
[2]
Squire, L.R.; Zola-Morgan, S. The medial temporal lobe memory system. Science, 1991, 253(5026), 1380-1386.
[http://dx.doi.org/10.1126/science.1896849] [PMID: 1896849]
[3]
Sara, S.J. The locus coeruleus and noradrenergic modulation of cognition. Nat. Rev. Neurosci., 2009, 10(3), 211-223.
[http://dx.doi.org/10.1038/nrn2573] [PMID: 19190638]
[4]
Frey, S.; Bergado-Rosado, J.; Seidenbecher, T.; Pape, H.C.; Frey, J.U. Reinforcement of early long-term potentiation (early-LTP) in dentate gyrus by stimulation of the basolateral amygdala: Heterosynaptic induction mechanisms of late-LTP. J. Neurosci., 2001, 21(10), 3697-3703.
[http://dx.doi.org/10.1523/JNEUROSCI.21-10-03697.2001] [PMID: 11331399]
[5]
Walling, S.G.; Harley, C.W. Locus ceruleus activation initiates delayed synaptic potentiation of perforant path input to the dentate gyrus in awake rats: A novel beta-adrenergic- and protein synthesis-dependent mammalian plasticity mechanism. J. Neurosci., 2004, 24(3), 598-604.
[http://dx.doi.org/10.1523/JNEUROSCI.4426-03.2004] [PMID: 14736844]
[6]
Hasselmo, M.E. Neuromodulation and cortical function: Modeling the physiological basis of behavior. Behav. Brain Res., 1995, 67(1), 1-27.
[http://dx.doi.org/10.1016/0166-4328(94)00113-T] [PMID: 7748496]
[7]
Maity, S.; Jarome, T.J.; Blair, J.; Lubin, F.D.; Nguyen, P.V. Noradrenaline goes nuclear: Epigenetic modifications during long-lasting synaptic potentiation triggered by activation of β-adrenergic receptors. J. Physiol., 2016, 594(4), 863-881.
[http://dx.doi.org/10.1113/JP271432] [PMID: 26574176]
[8]
Moore, R.Y.; Bloom, F.E. Central catecholamine neuron systems: Anatomy and physiology of the norepinephrine and epinephrine systems. Annu. Rev. Neurosci., 1979, 2, 113-168.
[http://dx.doi.org/10.1146/annurev.ne.02.030179.000553] [PMID: 231924]
[9]
Bliss, T.V.; Lomo, T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol., 1973, 232(2), 331-356.
[http://dx.doi.org/10.1113/jphysiol.1973.sp010273] [PMID: 4727084]
[10]
Malenka, R.C.; Nicoll, R.A. Long-term potentiation--a decade of progress? Science, 1999, 285(5435), 1870-1874.
[http://dx.doi.org/10.1126/science.285.5435.1870] [PMID: 10489359]
[11]
Nicoll, R.A.; Malenka, R.C. Expression mechanisms underlying NMDA receptor-dependent long-term potentiation. Ann. N. Y. Acad. Sci., 1999, 868, 515-525.
[http://dx.doi.org/10.1111/j.1749-6632.1999.tb11320.x] [PMID: 10414328]
[12]
Whitlock, J.R.; Heynen, A.J.; Shuler, M.G.; Bear, M.F. Learning induces long-term potentiation in the hippocampus. Science, 2006, 313(5790), 1093-1097.
[http://dx.doi.org/10.1126/science.1128134] [PMID: 16931756]
[13]
Desmond, N.L.; Colbert, C.M.; Zhang, D.X.; Levy, W.B. NMDA receptor antagonists block the induction of long-term depression in the hippocampal dentate gyrus of the anesthetized rat. Brain Res., 1991, 552(1), 93-98.
[http://dx.doi.org/10.1016/0006-8993(91)90664-H] [PMID: 1833033]
[14]
Collingridge, G.L.; Peineau, S.; Howland, J.G.; Wang, Y.T. Long-term depression in the CNS. Nat. Rev. Neurosci., 2010, 11(7), 459-473.
[http://dx.doi.org/10.1038/nrn2867] [PMID: 20559335]
[15]
Bliss, T. Noradrenergic regulation of synaptic plasticity in the hippocampal CA1 region. J. Nneurophysiol., 1997, 77(6), 3013-20
[16]
Katsuki, H.; Izumi, Y.; Zorumski, C.F. Noradrenergic regulation of synaptic plasticity in the hippocampal CA1 region. J. Neurophysiol., 1997, 77(6), 3013-3020.
[http://dx.doi.org/10.1152/jn.1997.77.6.3013] [PMID: 9212253]
[17]
Pussinen, R.; Sirviö, J. Minor role for alpha1-adrenoceptors in the facilitation of induction and early maintenance of long-term potentiation in the CA1 field of the hippocampus. J. Neurosci. Res., 1998, 51(3), 309-315.
[http://dx.doi.org/10.1002/(SICI)1097-4547(19980201)51:3<309:AID-JNR4>3.0.CO;2-K] [PMID: 9486766]
[18]
Scanziani, M.; Gähwiler, B.H.; Thompson, S.M. Presynaptic inhibition of excitatory synaptic transmission mediated by alpha adrenergic receptors in area CA3 of the rat hippocampus in vitro. J. Neurosci., 1993, 13(12), 5393-5401.
[http://dx.doi.org/10.1523/JNEUROSCI.13-12-05393.1993] [PMID: 7504723]
[19]
O’Dell, T.J.; Kandel, E.R. Low-frequency stimulation erases LTP through an NMDA receptor-mediated activation of protein phosphatases. Learn. Mem., 1994, 1(2), 129-139.
[PMID: 10467591]
[20]
Pedarzani, P.; Storm, J.F. Interaction between alpha- and beta-adrenergic receptor agonists modulating the slow Ca2+-activated K+ current IAHP in hippocampal neurons. Eur. J. Neurosci., 1996, 8(10), 2098-2110.
[http://dx.doi.org/10.1111/j.1460-9568.1996.tb00731.x] [PMID: 8921301]
[21]
Boehm, S. Presynaptic alpha2-adrenoceptors control excitatory, but not inhibitory, transmission at rat hippocampal synapses. J. Physiol., 1999, 519(Pt 2), 439-449.
[http://dx.doi.org/10.1111/j.1469-7793.1999.0439m.x] [PMID: 10457061]
[22]
Reznikoff, G.A.; Manaker, S.; Rhodes, C.H.; Winokur, A.; Rainbow, T.C. Localization and quantification of beta-adrenergic receptors in human brain. Neurology, 1986, 36(8), 1067-1073.
[http://dx.doi.org/10.1212/WNL.36.8.1067] [PMID: 3016604]
[23]
Nicholas, A.P.; Pieribone, V.A.; Hökfelt, T. Cellular localization of messenger RNA for beta-1 and beta-2 adrenergic receptors in rat brain: An in situ hybridization study. Neuroscience, 1993, 56(4), 1023-1039.
[http://dx.doi.org/10.1016/0306-4522(93)90148-9] [PMID: 8284033]
[24]
Hillman, K.L.; Knudson, C.A.; Carr, P.A.; Doze, V.A.; Porter, J.E. Adrenergic receptor characterization of CA1 hippocampal neurons using real time single cell RT-PCR. Brain Res. Mol. Brain Res., 2005, 139(2), 267-276.
[http://dx.doi.org/10.1016/j.molbrainres.2005.05.033] [PMID: 16005103]
[25]
Minocherhomjee, A.M.; Roufogalis, B.D. Mechanisms of coupling of the beta-adrenergic receptor to adenylate cyclase--an overview. Gen. Pharmacol., 1982, 13(2), 87-93.
[http://dx.doi.org/10.1016/0306-3623(82)90061-1] [PMID: 6284585]
[26]
Raymond, J.R. Multiple mechanisms of receptor-G protein signaling specificity. Am. J. Physiol., 1995, 269(2 Pt 2), F141-F158.
[PMID: 7653589]
[27]
Munro, C.A.; Walling, S.G.; Evans, J.H.; Harley, C.W. Beta-adrenergic blockade in the dentate gyrus in vivo prevents high frequency-induced long-term potentiation of EPSP slope, but not long-term potentiation of population spike amplitude. Hippocampus, 2001, 11(3), 322-328.
[http://dx.doi.org/10.1002/hipo.1046] [PMID: 11769313]
[28]
Bramham, C.R.; Bacher-Svendsen, K.; Sarvey, J.M. LTP in the lateral perforant path is beta-adrenergic receptor-dependent. Neuroreport, 1997, 8(3), 719-724.
[http://dx.doi.org/10.1097/00001756-199702100-00028] [PMID: 9106754]
[29]
Dahl, D.; Sarvey, J.M. Norepinephrine induces pathway-specific long-lasting potentiation and depression in the hippocampal dentate gyrus. Proc. Natl. Acad. Sci. USA, 1989, 86(12), 4776-4780.
[http://dx.doi.org/10.1073/pnas.86.12.4776] [PMID: 2734319]
[30]
Dahl, D.; Sarvey, J.M. Beta-adrenergic agonist-induced long-lasting synaptic modifications in hippocampal dentate gyrus require activation of NMDA receptors, but not electrical activation of afferents. Brain Res., 1990, 526(2), 347-350.
[http://dx.doi.org/10.1016/0006-8993(90)91245-C] [PMID: 1979521]
[31]
Davis, H.P.; Squire, L.R. Protein synthesis and memory: A review. Psychol. Bull., 1984, 96(3), 518-559.
[http://dx.doi.org/10.1037/0033-2909.96.3.518] [PMID: 6096908]
[32]
Huang, Y.Y.; Nguyen, P.V.; Abel, T.; Kandel, E.R. Long-lasting forms of synaptic potentiation in the mammalian hippocampus. Learn. Mem., 1996, 3(2-3), 74-85.
[http://dx.doi.org/10.1101/lm.3.2-3.74] [PMID: 10456078]
[33]
Squire, L.R.; Barondes, S.H. Actinomycin-D: Effects on memory at different times after training. Nature, 1970, 225(5233), 649-650.
[http://dx.doi.org/10.1038/225649a0] [PMID: 5413374]
[34]
Hopkins, W.F.; Johnston, D. Frequency-dependent noradrenergic modulation of long-term potentiation in the hippocampus. Science, 1984, 226(4672), 350-352.
[http://dx.doi.org/10.1126/science.6091272] [PMID: 6091272]
[35]
Hopkins, W.F.; Johnston, D. Noradrenergic enhancement of long-term potentiation at mossy fiber synapses in the hippocampus. J. Neurophysiol., 1988, 59(2), 667-687.
[http://dx.doi.org/10.1152/jn.1988.59.2.667] [PMID: 2832552]
[36]
Huang, Y.Y.; Kandel, E.R. Modulation of both the early and the late phase of mossy fiber LTP by the activation of beta-adrenergic receptors. Neuron, 1996, 16(3), 611-617.
[http://dx.doi.org/10.1016/S0896-6273(00)80080-X] [PMID: 8785058]
[37]
Murchison, C.F.; Zhang, X.Y.; Zhang, W.P.; Ouyang, M.; Lee, A.; Thomas, S.A. A distinct role for norepinephrine in memory retrieval. Cell, 2004, 117(1), 131-143.
[http://dx.doi.org/10.1016/S0092-8674(04)00259-4] [PMID: 15066288]
[38]
Dunwiddie, T.V.; Roberson, N.L.; Worth, T. Modulation of long-term potentiation: Effects of adrenergic and neuroleptic drugs. Pharmacol. Biochem. Behav., 1982, 17(6), 1257-1264.
[http://dx.doi.org/10.1016/0091-3057(82)90130-7] [PMID: 6131436]
[39]
Sarvey, J.M.; Burgard, E.C.; Decker, G. Long-term potentiation: Studies in the hippocampal slice. J. Neurosci. Methods, 1989, 28(1-2), 109-124.
[http://dx.doi.org/10.1016/0165-0270(89)90016-2] [PMID: 2542698]
[40]
Swanson-Park, J.L.; Coussens, C.M.; Mason-Parker, S.E.; Raymond, C.R.; Hargreaves, E.L.; Dragunow, M.; Cohen, A.S.; Abraham, W.C. A double dissociation within the hippocampus of dopamine D1/D5 receptor and beta-adrenergic receptor contributions to the persistence of long-term potentiation. Neuroscience, 1999, 92(2), 485-497.
[http://dx.doi.org/10.1016/S0306-4522(99)00010-X] [PMID: 10408599]
[41]
Thomas, M.J.; Moody, T.D.; Makhinson, M.; O’Dell, T.J. Activity-dependent beta-adrenergic modulation of low frequency stimulation induced LTP in the hippocampal CA1 region. Neuron, 1996, 17(3), 475-482.
[http://dx.doi.org/10.1016/S0896-6273(00)80179-8] [PMID: 8816710]
[42]
Norman, E.D.; Thiels, E.; Barrionuevo, G.; Klann, E. Long-term depression in the hippocampus in vivo is associated with protein phosphatase-dependent alterations in extracellular signal-regulated kinase. J. Neurochem., 2000, 74(1), 192-198.
[http://dx.doi.org/10.1046/j.1471-4159.2000.0740192.x] [PMID: 10617120]
[43]
Gelinas, J.N.; Nguyen, P.V. Beta-adrenergic receptor activation facilitates induction of a protein synthesis-dependent late phase of long-term potentiation. J. Neurosci., 2005, 25(13), 3294-3303.
[http://dx.doi.org/10.1523/JNEUROSCI.4175-04.2005] [PMID: 15800184]
[44]
Winder, D.G.; Martin, K.C.; Muzzio, I.A.; Rohrer, D.; Chruscinski, A.; Kobilka, B.; Kandel, E.R. ERK plays a regulatory role in induction of LTP by theta frequency stimulation and its modulation by beta-adrenergic receptors. Neuron, 1999, 24(3), 715-726.
[http://dx.doi.org/10.1016/S0896-6273(00)81124-1] [PMID: 10595521]
[45]
Giovannini, M.G.; Blitzer, R.D.; Wong, T.; Asoma, K.; Tsokas, P.; Morrison, J.H.; Iyengar, R.; Landau, E.M. Mitogen-activated protein kinase regulates early phosphorylation and delayed expression of Ca2+/calmodulin-dependent protein kinase II in long-term potentiation. J. Neurosci., 2001, 21(18), 7053-7062.
[http://dx.doi.org/10.1523/JNEUROSCI.21-18-07053.2001] [PMID: 11549715]
[46]
Otto, T.; Eichenbaum, H.; Wiener, S.I.; Wible, C.G. Learning-related patterns of CA1 spike trains parallel stimulation parameters optimal for inducing hippocampal long-term potentiation. Hippocampus, 1991, 1(2), 181-192.
[http://dx.doi.org/10.1002/hipo.450010206] [PMID: 1669292]
[47]
Grigoryan, G.; Ardi, Z.; Albrecht, A.; Richter-Levin, G.; Segal, M. Juvenile stress alters LTP in ventral hippocampal slices: Involvement of noradrenergic mechanisms. Behav. Brain Res., 2015, 278, 559-562.
[http://dx.doi.org/10.1016/j.bbr.2014.09.047] [PMID: 25300466]
[48]
Harris, E.W.; Ganong, A.H.; Cotman, C.W. Long-term potentiation in the hippocampus involves activation of N-methyl-D-aspartate receptors. Brain Res., 1984, 323(1), 132-137.
[http://dx.doi.org/10.1016/0006-8993(84)90275-0] [PMID: 6151863]
[49]
Lee, H.K.; Barbarosie, M.; Kameyama, K.; Bear, M.F.; Huganir, R.L. Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity. Nature, 2000, 405(6789), 955-959.
[http://dx.doi.org/10.1038/35016089] [PMID: 10879537]
[50]
Gelinas, J.N.; Banko, J.L.; Hou, L.; Sonenberg, N.; Weeber, E.J.; Klann, E.; Nguyen, P.V. ERK and mTOR signaling couple beta-adrenergic receptors to translation initiation machinery to gate induction of protein synthesis-dependent long-term potentiation. J. Biol. Chem., 2007, 282(37), 27527-27535.
[http://dx.doi.org/10.1074/jbc.M701077200] [PMID: 17635924]
[51]
Qian, H.; Matt, L.; Zhang, M.; Nguyen, M.; Patriarchi, T.; Koval, O.M.; Anderson, M.E.; He, K.; Lee, H.K.; Hell, J.W. β2-Adrenergic receptor supports prolonged theta tetanus-induced LTP. J. Neurophysiol., 2012, 107(10), 2703-2712.
[http://dx.doi.org/10.1152/jn.00374.2011] [PMID: 22338020]
[52]
Abraham, W.C. Metaplasticity: Key element in memory and learning? News Physiol. Sci., 1999, 14, 85.
[53]
Tenorio, G.; Connor, S.A.; Guévremont, D.; Abraham, W.C.; Williams, J.; O’Dell, T.J.; Nguyen, P.V. ‘Silent’ priming of translation-dependent LTP by β -adrenergic receptors involves phosphorylation and recruitment of AMPA receptors. Learn. Mem., 2010, 17(12), 627-638.
[http://dx.doi.org/10.1101/lm.1974510] [PMID: 21097606]
[54]
Lin, Y.W.; Min, M.Y.; Chiu, T.H.; Yang, H.W. Enhancement of associative long-term potentiation by activation of beta-adrenergic receptors at CA1 synapses in rat hippocampal slices. J. Neurosci., 2003, 23(10), 4173-4181.
[http://dx.doi.org/10.1523/JNEUROSCI.23-10-04173.2003] [PMID: 12764105]
[55]
Frey, U.; Morris, R.G. Synaptic tagging and long-term potentiation. Nature, 1997, 385(6616), 533-536.
[http://dx.doi.org/10.1038/385533a0] [PMID: 9020359]
[56]
Connor, S.A.; Wang, Y.T.; Nguyen, P.V. Activation of beta-adrenergic receptors facilitates heterosynaptic translation-dependent long-term potentiation. J. Physiol., 2011, 589(17), 4321-4340.
[http://dx.doi.org/10.1113/jphysiol.2011.209379] [PMID: 21746789]
[57]
Watabe, A.M.; Zaki, P.A.; O’Dell, T.J. Coactivation of beta-adrenergic and cholinergic receptors enhances the induction of long-term potentiation and synergistically activates mitogen-activated protein kinase in the hippocampal CA1 region. J. Neurosci., 2000, 20(16), 5924-5931.
[http://dx.doi.org/10.1523/JNEUROSCI.20-16-05924.2000] [PMID: 10934239]
[58]
Connor, S.A.; Maity, S.; Roy, B.; Ali, D.W.; Nguyen, P.V. Conversion of short-term potentiation to long-term potentiation in mouse CA1 by coactivation of β-adrenergic and muscarinic receptors. Learn. Mem., 2012, 19(11), 535-542.
[http://dx.doi.org/10.1101/lm.026898.112] [PMID: 23077334]
[59]
Scheiderer, C.L.; Smith, C.C.; McCutchen, E.; McCoy, P.A.; Thacker, E.E.; Kolasa, K.; Dobrunz, L.E.; McMahon, L.L. Coactivation of M(1) muscarinic and alpha1 adrenergic receptors stimulates extracellular signal-regulated protein kinase and induces long-term depression at CA3-CA1 synapses in rat hippocampus. J. Neurosci., 2008, 28(20), 5350-5358.
[http://dx.doi.org/10.1523/JNEUROSCI.5058-06.2008] [PMID: 18480291]
[60]
Bouret, S.; Sara, S.J. Network reset: A simplified overarching theory of locus coeruleus noradrenaline function. Trends Neurosci., 2005, 28(11), 574-582.
[http://dx.doi.org/10.1016/j.tins.2005.09.002] [PMID: 16165227]
[61]
Sekeres, M.J.; Winocur, G.; Moscovitch, M. The hippocampus and related neocortical structures in memory transformation. Neurosci. Lett., 2018, 680, 39-53.
[http://dx.doi.org/10.1016/j.neulet.2018.05.006] [PMID: 29733974]
[62]
Runyan, J.D.; Dash, P.K. Intra-medial prefrontal administration of SCH-23390 attenuates ERK phosphorylation and long-term memory for trace fear conditioning in rats. Neurobiol. Learn. Mem., 2004, 82(2), 65-70.
[http://dx.doi.org/10.1016/j.nlm.2004.04.006] [PMID: 15341790]
[63]
Scoville, W.B.; Milner, B. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry, 1957, 20(1), 11-21.
[http://dx.doi.org/10.1136/jnnp.20.1.11] [PMID: 13406589]
[64]
Winocur, G.; Gilbert, M. The hippocampus, context, and information processing. Behav. Neural Biol., 1984, 40(1), 27-43.
[http://dx.doi.org/10.1016/S0163-1047(84)90146-8] [PMID: 6732705]
[65]
Joiner, M.L.; Lisé, M.F.; Yuen, E.Y.; Kam, A.Y.; Zhang, M.; Hall, D.D.; Malik, Z.A.; Qian, H.; Chen, Y.; Ulrich, J.D.; Burette, A.C.; Weinberg, R.J.; Law, P.Y.; El-Husseini, A.; Yan, Z.; Hell, J.W. Assembly of a beta2-adrenergic receptor--GluR1 signalling complex for localized cAMP signalling. EMBO J., 2010, 29(2), 482-495.
[http://dx.doi.org/10.1038/emboj.2009.344] [PMID: 19942860]
[66]
Davare, M.A.; Avdonin, V.; Hall, D.D.; Peden, E.M.; Burette, A.; Weinberg, R.J.; Horne, M.C.; Hoshi, T.; Hell, J.W. A beta2 adrenergic receptor signaling complex assembled with the Ca2+ channel Cav1.2. Science, 2001, 293(5527), 98-101.
[http://dx.doi.org/10.1126/science.293.5527.98] [PMID: 11441182]
[67]
Zhang, M.; Patriarchi, T.; Stein, I.S.; Qian, H.; Matt, L.; Nguyen, M.; Xiang, Y.K.; Hell, J.W. Adenylyl cyclase anchoring by a kinase anchor protein AKAP5 (AKAP79/150) is important for postsynaptic β-adrenergic signaling. J. Biol. Chem., 2013, 288(24), 17918-17931.
[http://dx.doi.org/10.1074/jbc.M112.449462] [PMID: 23649627]
[68]
Havekes, R.; Canton, D.A.; Park, A.J.; Huang, T.; Nie, T.; Day, J.P.; Guercio, L.A.; Grimes, Q.; Luczak, V.; Gelman, I.H.; Baillie, G.S.; Scott, J.D.; Abel, T. Gravin orchestrates protein kinase A and β2-adrenergic receptor signaling critical for synaptic plasticity and memory. J. Neurosci., 2012, 32(50), 18137-18149.
[http://dx.doi.org/10.1523/JNEUROSCI.3612-12.2012] [PMID: 23238728]
[69]
O’Dell, T.J.; Connor, S.A.; Gelinas, J.N.; Nguyen, P.V. Viagra for your synapses: Enhancement of hippocampal long-term potentiation by activation of beta-adrenergic receptors. Cell. Signal., 2010, 22(5), 728-736.
[http://dx.doi.org/10.1016/j.cellsig.2009.12.004] [PMID: 20043991]
[70]
Maity, S.; Rah, S.; Sonenberg, N.; Gkogkas, C.G.; Nguyen, P.V. Norepinephrine triggers metaplasticity of LTP by increasing translation of specific mRNAs. Learn. Mem., 2015, 22(10), 499-508.
[http://dx.doi.org/10.1101/lm.039222.115] [PMID: 26373828]
[71]
Gelinas, J.N.; Banko, J.L.; Peters, M.M.; Klann, E.; Weeber, E.J.; Nguyen, P.V. Activation of exchange protein activated by cyclic-AMP enhances long-lasting synaptic potentiation in the hippocampus. Learn. Mem., 2008, 15(6), 403-411.
[http://dx.doi.org/10.1101/lm.830008] [PMID: 18509114]
[72]
Brandwein, N.J.; Nguyen, P.V. Noradrenergic stabilization of heterosynaptic LTP requires activation of epac in the hippocampus. Learn. Mem., 2019, 26(2), 31-38.
[http://dx.doi.org/10.1101/lm.048660.118] [PMID: 30651375]
[73]
Jȩdrzejewska-Szmek, J.; Luczak, V.; Abel, T.; Blackwell, K.T. β-adrenergic signaling broadly contributes to LTP induction. PLOS Comput. Biol., 2017, 13(7)e1005657
[http://dx.doi.org/10.1371/journal.pcbi.1005657] [PMID: 28742159]
[74]
Brandwein, N.J.; Nguyen, P.V. A requirement for epigenetic modifications during noradrenergic stabilization of heterosynaptic LTP in the hippocampus. Neurobiol. Learn. Mem., 2019, 161, 72-82.
[http://dx.doi.org/10.1016/j.nlm.2019.03.008] [PMID: 30930287]
[75]
Moser, M.B.; Moser, E.I. Distributed encoding and retrieval of spatial memory in the hippocampus. J. Neurosci., 1998, 18(18), 7535-7542.
[http://dx.doi.org/10.1523/JNEUROSCI.18-18-07535.1998] [PMID: 9736671]
[76]
Zola-Morgan, S.; Squire, L.R. Medial temporal lesions in monkeys impair memory on a variety of tasks sensitive to human amnesia. Behav. Neurosci., 1985, 99(1), 22-34.
[http://dx.doi.org/10.1037/0735-7044.99.1.22] [PMID: 4041230]
[77]
O’Keefe, J.; Dostrovsky, J. The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res., 1971, 34(1), 171-175.
[http://dx.doi.org/10.1016/0006-8993(71)90358-1] [PMID: 5124915]
[78]
Grella, S.L.; Neil, J.M.; Edison, H.T.; Strong, V.D.; Odintsova, I.V.; Walling, S.G.; Martin, G.M.; Marrone, D.F.; Harley, C.W. Locus coeruleus phasic, but not tonic, activation initiates global remapping in a familiar environment. J. Neurosci., 2019, 39(3), 445-455.
[http://dx.doi.org/10.1523/JNEUROSCI.1956-18.2018] [PMID: 30478033]
[79]
Hendrickson, RC; Raskind, MA Noradrenergic dysregulation in the pathophysiology of PTSD. Exper. Neurol., 2016, 284((Pt B), 181-95.,
[http://dx.doi.org/10.1016/j.expneurol.2016.05.014]
[80]
Sirviö, J.; MacDonald, E. Central alpha1-adrenoceptors: Their role in the modulation of attention and memory formation. Pharmacol. Ther., 1999, 83(1), 49-65.
[PMID: 10501595]
[81]
Introini-Collison, I.; Saghafi, D.; Novack, G.D.; McGaugh, J.L. Memory-enhancing effects of post-training dipivefrin and epinephrine: Involvement of peripheral and central adrenergic receptors. Brain Res., 1992, 572(1-2), 81-86.
[http://dx.doi.org/10.1016/0006-8993(92)90454-H] [PMID: 1319277]
[82]
Puumala, T.; Greijus, S.; Narinen, K.; Haapalinna, A.; Riekkinen, P., Sr; Sirvio, J. Stimulation of alpha-1 adrenergic receptors facilitates spatial learning in rats. Eur. Neuropsychopharmacol., 1998, 8(1), 17-26.
[http://dx.doi.org/10.1016/S0924-977X(97)00040-0]
[83]
Riekkinen, M.; Kemppainen, S.; Riekkinen, P., Jr Effects of stimulation of alpha 1-adrenergic and NMDA/glycine-B receptors on learning defects in aged rats. Psychopharmacology (Berl.), 1997, 131(1), 49-56.
[http://dx.doi.org/10.1007/s002130050264] [PMID: 9181635]
[84]
Ji, J.Z.; Zhang, X.H.; Li, B.M. Deficient spatial memory induced by blockade of beta-adrenoceptors in the hippocampal CA1 region. Behav. Neurosci., 2003, 117(6), 1378-1384.
[http://dx.doi.org/10.1037/0735-7044.117.6.1378] [PMID: 14674855]
[85]
Ji, J.Z.; Wang, X.M.; Li, B.M. Deficit in long-term contextual fear memory induced by blockade of beta-adrenoceptors in hippocampal CA1 region. Eur. J. Neurosci., 2003, 17(9), 1947-1952.
[http://dx.doi.org/10.1046/j.1460-9568.2003.02620.x] [PMID: 12752794]
[86]
Mello-Carpes, P.B.; da Silva de Vargas, L.; Gayer, M.C.; Roehrs, R.; Izquierdo, I. Hippocampal noradrenergic activation is necessary for object recognition memory consolidation and can promote BDNF increase and memory persistence. Neurobiol. Learn. Mem., 2016, 127, 84-92.
[http://dx.doi.org/10.1016/j.nlm.2015.11.014] [PMID: 26691781]
[87]
Izquierdo, I.; Medina, J.H.; Izquierdo, L.A.; Barros, D.M.; de Souza, M.M.; Mello e Souza, T. Short- and long-term memory are differentially regulated by monoaminergic systems in the rat brain. Neurobiol. Learn. Mem., 1998, 69(3), 219-224.
[http://dx.doi.org/10.1006/nlme.1998.3825] [PMID: 9707486]
[88]
Barros, D.M.; Izquierdo, L.A.; Sant’Anna, M.K.; Quevedo, J.; Medina, J.H.; McGaugh, J.L.; Izquierdo, I. Stimulators of the cAMP cascade reverse amnesia induced by intra-amygdala but not intrahippocampal KN-62 administration. Neurobiol. Learn. Mem., 1999, 71(1), 94-103.
[http://dx.doi.org/10.1006/nlme.1998.3830] [PMID: 9889075]
[89]
Sara, S.J.; Roullet, P.; Przybyslawski, J. Consolidation of memory for odor-reward association: Beta-adrenergic receptor involvement in the late phase. Learn. Mem., 1999, 6(2), 88-96.
[PMID: 10327234]
[90]
McGaugh, J.L. Memory--a century of consolidation. Science, 2000, 287(5451), 248-251.
[http://dx.doi.org/10.1126/science.287.5451.248] [PMID: 10634773]
[91]
Izquierdo, I.; Medina, J.H. Memory formation: The sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol. Learn. Mem., 1997, 68(3), 285-316.
[http://dx.doi.org/10.1006/nlme.1997.3799] [PMID: 9398590]
[92]
Thomas, S.A.; Palmiter, R.D. Disruption of the dopamine beta-hydroxylase gene in mice suggests roles for norepinephrine in motor function, learning, and memory. Behav. Neurosci., 1997, 111(3), 579-589.
[http://dx.doi.org/10.1037/0735-7044.111.3.579] [PMID: 9189272]
[93]
Abel, T.; Lattal, K.M. Molecular mechanisms of memory acquisition, consolidation and retrieval. Curr. Opin. Neurobiol., 2001, 11(2), 180-187.
[http://dx.doi.org/10.1016/S0959-4388(00)00194-X] [PMID: 11301237]
[94]
Schiff, H.C.; Johansen, J.P.; Hou, M.; Bush, D.E.; Smith, E.K.; Klein, J.E. Beta-adrenergic receptors regulate the acquisition and consolidation phases of aversive memory formation through distinct, temporally regulated signaling pathways. Neuropsychopharmacology, 2017, 42(4), 895-903.
[95]
Barros, D.M.; Mello e Souza, T.; De David, T.; Choi, H.; Aguzzoli, A.; Madche, C.; Ardenghi, P.; Medina, J.H.; Izquierdo, I. Simultaneous modulation of retrieval by dopaminergic D(1), beta-noradrenergic, serotonergic-1A and cholinergic muscarinic receptors in cortical structures of the rat. Behav. Brain Res., 2001, 124(1), 1-7.
[http://dx.doi.org/10.1016/S0166-4328(01)00208-X] [PMID: 11423160]
[96]
Devauges, V.; Sara, S.J. Memory retrieval enhancement by locus coeruleus stimulation: Evidence for mediation by beta-receptors. Behav. Brain Res., 1991, 43(1), 93-97.
[http://dx.doi.org/10.1016/S0166-4328(05)80056-7] [PMID: 1650233]
[97]
Przybyslawski, J.; Roullet, P.; Sara, S.J. Attenuation of emotional and nonemotional memories after their reactivation: Role of beta adrenergic receptors. J. Neurosci., 1999, 19(15), 6623-6628.
[http://dx.doi.org/10.1523/JNEUROSCI.19-15-06623.1999] [PMID: 10414990]
[98]
Genoux, D.; Haditsch, U.; Knobloch, M.; Michalon, A.; Storm, D.; Mansuy, I.M. Protein phosphatase 1 is a molecular constraint on learning and memory. Nature, 2002, 418(6901), 970-975.
[http://dx.doi.org/10.1038/nature00928] [PMID: 12198546]
[99]
Doyère, V.; Laroche, S. Linear relationship between the maintenance of hippocampal long-term potentiation and retention of an associative memory. Hippocampus, 1992, 2(1), 39-48.
[http://dx.doi.org/10.1002/hipo.450020106] [PMID: 1308172]
[100]
Martin, S.J.; Morris, R.G. New life in an old idea: The synaptic plasticity and memory hypothesis revisited. Hippocampus, 2002, 12(5), 609-636.
[http://dx.doi.org/10.1002/hipo.10107] [PMID: 12440577]
[101]
Kitchigina, V.; Vankov, A.; Harley, C.; Sara, S.J. Novelty-elicited, noradrenaline-dependent enhancement of excitability in the dentate gyrus. Eur. J. Neurosci., 1997, 9(1), 41-47.
[http://dx.doi.org/10.1111/j.1460-9568.1997.tb01351.x] [PMID: 9042567]
[102]
Straube, T.; Korz, V.; Balschun, D.; Frey, J.U. Requirement of beta-adrenergic receptor activation and protein synthesis for LTP-reinforcement by novelty in rat dentate gyrus. J. Physiol., 2003, 552(Pt 3), 953-960.
[http://dx.doi.org/10.1113/jphysiol.2003.049452] [PMID: 12937286]
[103]
Lemon, N.; Aydin-Abidin, S.; Funke, K.; Manahan-Vaughan, D. Locus coeruleus activation facilitates memory encoding and induces hippocampal LTD that depends on beta-adrenergic receptor activation. Cereb. Cortex, 2009, 19(12), 2827-2837.
[http://dx.doi.org/10.1093/cercor/bhp065] [PMID: 19435710]
[104]
Hagena, H.; Manahan-Vaughan, D. Learning-facilitated long-term depression and long-term potentiation at mossy fiber-CA3 synapses requires activation of β-adrenergic receptors. Front. Integr. Nuerosci., 2012, 6, 23.
[http://dx.doi.org/10.3389/fnint.2012.00023] [PMID: 22654741]

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