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. 2014 Feb 13;30(3):505–514. doi: 10.1007/s12264-013-1399-7

Roles of somatic A-type K+ channels in the synaptic plasticity of hippocampal neurons

Yoon-Sil Yang 1, Kyeong-Deok Kim 1, Su-Yong Eun 1, Sung-Cherl Jung 1,2,
PMCID: PMC5562601  PMID: 24526657

Abstract

In the mammalian brain, information encoding and storage have been explained by revealing the cellular and molecular mechanisms of synaptic plasticity at various levels in the central nervous system, including the hippocampus and the cerebral cortices. The modulatory mechanisms of synaptic excitability that are correlated with neuronal tasks are fundamental factors for synaptic plasticity, and they are dependent on intracellular Ca2+-mediated signaling. In the present review, the A-type K+ (I A) channel, one of the voltage-dependent cation channels, is considered as a key player in the modulation of Ca2+ influx through synaptic NMDA receptors and their correlated signaling pathways. The cellular functions of I A channels indicate that they possibly play as integral parts of synaptic and somatic complexes, completing the initiation and stabilization of memory.

Keywords: A-type K+ channels, intrinsic excitability, synaptic plasticity, NMDA receptors, Kv4.2

References

  • [1].Aizenman CD, Linden DJ. Rapid, synaptically driven increases in the intrinsic excitability of cerebellar deep nuclear neurons. Nat Neurosci. 2000;3:109–111. doi: 10.1038/72049. [DOI] [PubMed] [Google Scholar]
  • [2].Jung SC, Hoffman DA. Biphasic somatic A-type K+ channel downregulation mediates intrinsic plasticity in hippocampal CA1 pyramidal neurons. PLoS One. 2009;4:e6549. doi: 10.1371/journal.pone.0006549. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [3].Kim SJ, Linden DJ. Ubiquitous plasticity and memory storage. Neuron. 2007;56:582–592. doi: 10.1016/j.neuron.2007.10.030. [DOI] [PubMed] [Google Scholar]
  • [4].Xu J, Kang N, Jiang L, Nedergaard M, Kang J. Activity-dependent long-term potentiation of intrinsic excitability in hippocampal CA1 pyramidal neurons. J Neurosci. 2005;25:1750–1760. doi: 10.1523/JNEUROSCI.4217-04.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [5].Zhang W, Linden DJ. The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat Rev Neurosci. 2003;4:885–900. doi: 10.1038/nrn1248. [DOI] [PubMed] [Google Scholar]
  • [6].Franks KM, Isaacson JS. Synapse-specific downregulation of NMDA receptors by early experience: a critical period for plasticity of sensory input to olfactory cortex. Neuron. 2005;47:101–114. doi: 10.1016/j.neuron.2005.05.024. [DOI] [PubMed] [Google Scholar]
  • [7].Lapointe V, Morin F, Ratte S, Croce A, Conquet F, Lacaille JC. Synapse-specific mGluR1-dependent long-term potentiation in interneurones regulates mouse hippocampal inhibition. J Physiol. 2004;555:125–135. doi: 10.1113/jphysiol.2003.053603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [8].Singla S, Kreitzer AC, Malenka RC. Mechanisms for synapse specificity during striatal long-term depression. J Neurosci. 2007;27:5260–5264. doi: 10.1523/JNEUROSCI.0018-07.2007. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [9].Bliss TV, 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;232:331–356. doi: 10.1113/jphysiol.1973.sp010273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [10].Campanac E, Debanne D. Spike timing-dependent plasticity: a learning rule for dendritic integration in rat CA1 pyramidal neurons. J Physiol. 2008;586:779–793. doi: 10.1113/jphysiol.2007.147017. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [11].Bergquist S, Dickman DK, Davis GW. A hierarchy of cell intrinsic and target-derived homeostatic signaling. Neuron. 2010;66:220–234. doi: 10.1016/j.neuron.2010.03.023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [12].Tsunoda S, Salkoff L. Genetic analysis of Drosophila neurons: Shal, Shaw, and Shab encode most embryonic potassium currents. J Neurosci. 1995;15:1741–1754. doi: 10.1523/JNEUROSCI.15-03-01741.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [13].Solc CK, Zagotta WN, Aldrich RW. Single-channel and genetic analyses reveal two distinct A-type potassium channels in Drosophila. Science. 1987;236:1094–1098. doi: 10.1126/science.2437657. [DOI] [PubMed] [Google Scholar]
  • [14].Cash S, Yuste R. Input summation by cultured pyramidal neurons is linear and position-independent. J Neurosci. 1998;18:10–15. doi: 10.1523/JNEUROSCI.18-01-00010.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [15].Goldberg JH, Tamas G, Yuste R. Ca2+ imaging of mouse neocortical interneurone dendrites: Ia-type K+ channels control action potential backpropagation. J Physiol. 2003;551:49–65. doi: 10.1113/jphysiol.2003.042580. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [16].Hoffman DA, Magee JC, Colbert CM, Johnston D. K+ channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature. 1997;387:869–875. doi: 10.1038/42571. [DOI] [PubMed] [Google Scholar]
  • [17].Kim J, Wei DS, Hoffman DA. Kv4 potassium channel subunits control action potential repolarization and frequency-dependent broadening in rat hippocampal CA1 pyramidal neurones. J Physiol. 2005;569:41–57. doi: 10.1113/jphysiol.2005.095042. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [18].Ramakers GM, Storm JF. A postsynaptic transient K(+) current modulated by arachidonic acid regulates synaptic integration and threshold for LTP induction in hippocampal pyramidal cells. Proc Natl Acad Sci U S A. 2002;99:10144–10149. doi: 10.1073/pnas.152620399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [19].Schoppa NE, Westbrook GL. Regulation of synaptic timing in the olfactory bulb by an A-type potassium current. Nat Neurosci. 1999;2:1106–1113. doi: 10.1038/16033. [DOI] [PubMed] [Google Scholar]
  • [20].Chen X, Yuan LL, Zhao C, Birnbaum SG, Frick A, Jung WE, et al. Deletion of Kv4.2 gene eliminates dendritic A-type K+ current and enhances induction of long-term potentiation in hippocampal CA1 pyramidal neurons. J Neurosci. 2006;26:12143–12151. doi: 10.1523/JNEUROSCI.2667-06.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [21].Frick A, Magee J, Johnston D. LTP is accompanied by an enhanced local excitability of pyramidal neuron dendrites. Nat Neurosci. 2004;7:126–135. doi: 10.1038/nn1178. [DOI] [PubMed] [Google Scholar]
  • [22].Jung SC, Kim J, Hoffman DA. Rapid, bidirectional remodeling of synaptic NMDA receptor subunit composition by A-type K+ channel activity in hippocampal CA1 pyramidal neurons. Neuron. 2008;60:657–671. doi: 10.1016/j.neuron.2008.08.029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [23].Kim J, Jung SC, Clemens AM, Petralia RS, Hoffman DA. Regulation of dendritic excitability by activity-dependent trafficking of the A-type K+ channel subunit Kv4.2 in hippocampal neurons. Neuron. 2007;54:933–947. doi: 10.1016/j.neuron.2007.05.026. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [24].Watanabe S, Hoffman DA, Migliore M, Johnston D. Dendritic K+ channels contribute to spike-timing dependent long-term potentiation in hippocampal pyramidal neurons. Proc Natl Acad Sci U S A. 2002;99:8366–8371. doi: 10.1073/pnas.122210599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [25].Cooper EC, Milroy A, Jan YN, Jan LY, Lowenstein DH. Presynaptic localization of Kv1.4-containing A-type potassium channels near excitatory synapses in the hippocampus. J Neurosci. 1998;18:965–974. doi: 10.1523/JNEUROSCI.18-03-00965.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [26].Kampa BM, Stuart GJ. Calcium spikes in basal dendrites of layer 5 pyramidal neurons during action potential bursts. J Neurosci. 2006;26:7424–7432. doi: 10.1523/JNEUROSCI.3062-05.2006. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [27].Losonczy A, Makara JK, Magee JC. Compartmentalized dendritic plasticity and input feature storage in neurons. Nature. 2008;452:436–441. doi: 10.1038/nature06725. [DOI] [PubMed] [Google Scholar]
  • [28].Sheng M, Tsaur ML, Jan YN, Jan LY. Subcellular segregation of two A-type K+ channel proteins in rat central neurons. Neuron. 1992;9:271–284. doi: 10.1016/0896-6273(92)90166-B. [DOI] [PubMed] [Google Scholar]
  • [29].Hagiwara S. Nervous activities of the heart in Crustacea. Ergeb Biol. 1961;24:287–311. doi: 10.1007/978-3-642-94805-3_8. [DOI] [PubMed] [Google Scholar]
  • [30].Johnston D, Narayanan R. Active dendrites: colorful wings of the mysterious butterflies. Trends Neurosci. 2008;31:309–316. doi: 10.1016/j.tins.2008.03.004. [DOI] [PubMed] [Google Scholar]
  • [31].Marsh SJ, Brown DA. Potassium currents contributing to action potential repolarization in dissociated cultured rat superior cervical sympathetic neurones. Neurosci Lett. 1991;133:298–302. doi: 10.1016/0304-3940(91)90593-I. [DOI] [PubMed] [Google Scholar]
  • [32].Sah P, McLachlan EM. Potassium currents contributing to action potential repolarization and the afterhyperpolarization in rat vagal motoneurons. J Neurophysiol. 1992;68:1834–1841. doi: 10.1152/jn.1992.68.5.1834. [DOI] [PubMed] [Google Scholar]
  • [33].Lorincz A, Notomi T, Tamas G, Shigemoto R, Nusser Z. Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nat Neurosci. 2002;5:1185–1193. doi: 10.1038/nn962. [DOI] [PubMed] [Google Scholar]
  • [34].Notomi T, Shigemoto R. Immunohistochemical localization of Ih channel subunits, HCN1–4, in the rat brain. J Comp Neurol. 2004;471:241–276. doi: 10.1002/cne.11039. [DOI] [PubMed] [Google Scholar]
  • [35].Sanguinetti MC, Jurkiewicz NK. Role of external Ca2+ and K+ in gating of cardiac delayed rectifier K+ currents. Pflugers Arch. 1992;420:180–186. doi: 10.1007/BF00374988. [DOI] [PubMed] [Google Scholar]
  • [36].Snyders DJ. Structure and function of cardiac potassium channels. Cardiovasc Res. 1999;42:377–390. doi: 10.1016/S0008-6363(99)00071-1. [DOI] [PubMed] [Google Scholar]
  • [37].Varro A, Papp JG. The impact of single cell voltage clamp on the understanding of the cardiac ventricular action potential. Cardioscience. 1992;3:131–144. [PubMed] [Google Scholar]
  • [38].Lei M, Honjo H, Kodama I, Boyett MR. Characterisation of the transient outward K+ current in rabbit sinoatrial node cells. Cardiovasc Res. 2000;46:433–441. doi: 10.1016/S0008-6363(00)00036-5. [DOI] [PubMed] [Google Scholar]
  • [39].Shibasaki T. Conductance and kinetics of delayed rectifier potassium channels in nodal cells of the rabbit heart. J Physiol. 1987;387:227–250. doi: 10.1113/jphysiol.1987.sp016571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [40].Carrasquillo Y, Burkhalter A, Nerbonne JM. A-type K+ channels encoded by Kv4.2, Kv4.3 and Kv1.4 differentially regulate intrinsic excitability of cortical pyramidal neurons. J Physiol. 2012;590:3877–3890. doi: 10.1113/jphysiol.2012.229013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [41].Coetzee WA, Amarillo Y, Chiu J, Chow A, Lau D, McCormack T, et al. Molecular diversity of K+ channels. Ann N Y Acad Sci. 1999;868:233–285. doi: 10.1111/j.1749-6632.1999.tb11293.x. [DOI] [PubMed] [Google Scholar]
  • [42].Song WJ. Genes responsible for native depolarization-activated K+ currents in neurons. Neurosci Res. 2002;42:7–14. doi: 10.1016/S0168-0102(01)00305-4. [DOI] [PubMed] [Google Scholar]
  • [43].Lauver A, Yuan LL, Jeromin A, Nadin BM, Rodriguez JJ, Davies HA, et al. Manipulating Kv4.2 identifies a specific component of hippocampal pyramidal neuron A-current that depends upon Kv4.2 expression. J Neurochem. 2006;99:1207–1223. doi: 10.1111/j.1471-4159.2006.04185.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [44].Malinow R, Malenka RC. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci. 2002;25:103–126. doi: 10.1146/annurev.neuro.25.112701.142758. [DOI] [PubMed] [Google Scholar]
  • [45].Nicoll RA, Malenka RC. Expression mechanisms underlying NMDA receptor-dependent long-term potentiation. Ann N Y Acad Sci. 1999;868:515–525. doi: 10.1111/j.1749-6632.1999.tb11320.x. [DOI] [PubMed] [Google Scholar]
  • [46].Stuart G, Spruston N, Sakmann B, Hausser M. Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci. 1997;20:125–131. doi: 10.1016/S0166-2236(96)10075-8. [DOI] [PubMed] [Google Scholar]
  • [47].Lisman J, Spruston N. Postsynaptic depolarization requirements for LTP and LTD: a critique of spike timing-dependent plasticity. Nat Neurosci. 2005;8:839–841. doi: 10.1038/nn0705-839. [DOI] [PubMed] [Google Scholar]
  • [48].Magee JC, Johnston D. A synaptically controlled, associative signal for Hebbian plasticity in hippocampal neurons. Science. 1997;275:209–213. doi: 10.1126/science.275.5297.209. [DOI] [PubMed] [Google Scholar]
  • [49].Stuart GJ, Sakmann B. Active propagation of somatic action potentials into neocortical pyramidal cell dendrites. Nature. 1994;367:69–72. doi: 10.1038/367069a0. [DOI] [PubMed] [Google Scholar]
  • [50].Bellone C, Nicoll RA. Rapid bidirectional switching of synaptic NMDA receptors. Neuron. 2007;55:779–785. doi: 10.1016/j.neuron.2007.07.035. [DOI] [PubMed] [Google Scholar]
  • [51].Kerchner GA, Nicoll RA. Silent synapses and the emergence of a postsynaptic mechanism for LTP. Nat Rev Neurosci. 2008;9:813–825. doi: 10.1038/nrn2501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [52].Kim E, Hoffman DA. Dynamic regulation of synaptic maturation state by voltage-gated A-type K+ channels in CA1 hippocampal pyramidal neurons. J Neurosci. 2012;32:14427–14432. doi: 10.1523/JNEUROSCI.2373-12.2012. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [53].Campanac E, Daoudal G, Ankri N, Debanne D. Downregulation of dendritic I(h) in CA1 pyramidal neurons after LTP. J Neurosci. 2008;28:8635–8643. doi: 10.1523/JNEUROSCI.1411-08.2008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [54].Daoudal G, Debanne D. Long-term plasticity of intrinsic excitability: learning rules and mechanisms. Learn Mem. 2003;10:456–465. doi: 10.1101/lm.64103. [DOI] [PubMed] [Google Scholar]
  • [55].Disterhoft JF, Oh MM. Learning, aging and intrinsic neuronal plasticity. Trends Neurosci. 2006;29:587–599. doi: 10.1016/j.tins.2006.08.005. [DOI] [PubMed] [Google Scholar]
  • [56].Storm JF. Potassium currents in hippocampal pyramidal cells. Prog Brain Res. 1990;83:161–187. doi: 10.1016/S0079-6123(08)61248-0. [DOI] [PubMed] [Google Scholar]
  • [57].Alkon DL, Sakakibara M, Forman R, Harrigan J, Lederhendler I, Farley J. Reduction of two voltage-dependent K+ currents mediates retention of a learned association. Behav Neural Biol. 1985;44:278–300. doi: 10.1016/S0163-1047(85)90296-1. [DOI] [PubMed] [Google Scholar]
  • [58].Fan Y, Fricker D, Brager DH, Chen X, Lu HC, Chitwood RA, et al. Activity-dependent decrease of excitability in rat hippocampal neurons through increases in I(h) Nat Neurosci. 2005;8:1542–1551. doi: 10.1038/nn1568. [DOI] [PubMed] [Google Scholar]
  • [59].Hess G, Gustafsson B. Changes in field excitatory postsynaptic potential shape induced by tetanization in the CA1 region of the guinea-pig hippocampal slice. Neuroscience. 1990;37:61–69. doi: 10.1016/0306-4522(90)90192-7. [DOI] [PubMed] [Google Scholar]
  • [60].Jester JM, Campbell LW, Sejnowski TJ. Associative EPSP-spike potentiation induced by pairing orthodromic and antidromic stimulation in rat hippocampal slices. J Physiol. 1995;484(Pt3):689–705. doi: 10.1113/jphysiol.1995.sp020696. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [61].Reyes A. Influence of dendritic conductances on the input-output properties of neurons. Annu Rev Neurosci. 2001;24:653–675. doi: 10.1146/annurev.neuro.24.1.653. [DOI] [PubMed] [Google Scholar]
  • [62].Bayliss DA, Viana F, Bellingham MC, Berger AJ. Characteristics and postnatal development of a hyperpolarization-activated inward current in rat hypoglossal motoneurons in vitro. J Neurophysiol. 1994;71:119–128. doi: 10.1152/jn.1994.71.1.119. [DOI] [PubMed] [Google Scholar]
  • [63].Chetkovich DM, Gray R, Johnston D, Sweatt JD. N-methyl-D-aspartate receptor activation increases cAMP levels and voltage-gated Ca2+ channel activity in area CA1 of hippocampus. Proc Natl Acad Sci U S A. 1991;88:6467–6471. doi: 10.1073/pnas.88.15.6467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [64].Havik B, Rokke H, Bardsen K, Davanger S, Bramham CR. Bursts of high-frequency stimulation trigger rapid delivery of pre-existing alpha-CaMKII mRNA to synapses: a mechanism in dendritic protein synthesis during long-term potentiation in adult awake rats. Eur J Neurosci. 2003;17:2679–2689. doi: 10.1046/j.1460-9568.2003.02712.x. [DOI] [PubMed] [Google Scholar]
  • [65].Huang YY, Kandel ER. Postsynaptic induction and PKA-dependent expression of LTP in the lateral amygdala. Neuron. 1998;21:169–178. doi: 10.1016/S0896-6273(00)80524-3. [DOI] [PubMed] [Google Scholar]
  • [66].Kirkwood A, Rioult MC, Bear MF. Experience-dependent modification of synaptic plasticity in visual cortex. Nature. 1996;381:526–528. doi: 10.1038/381526a0. [DOI] [PubMed] [Google Scholar]
  • [67].Nishiyama M, Hong K, Mikoshiba K, Poo MM, Kato K. Calcium stores regulate the polarity and input specificity of synaptic modification. Nature. 2000;408:584–588. doi: 10.1038/35046067. [DOI] [PubMed] [Google Scholar]
  • [68].Perkel DJ, Petrozzino JJ, Nicoll RA, Connor JA. The role of Ca2+ entry via synaptically activated NMDA receptors in the induction of long-term potentiation. Neuron. 1993;11:817–823. doi: 10.1016/0896-6273(93)90111-4. [DOI] [PubMed] [Google Scholar]
  • [69].Li XM, Gu Y, She JQ, Zhu DM, Niu ZD, Wang M, et al. Lead inhibited N-methyl-D-aspartate receptor-independent long-term potentiation involved ryanodine-sensitive calcium stores in rat hippocampal area CA1. Neuroscience. 2006;139:463–473. doi: 10.1016/j.neuroscience.2005.12.033. [DOI] [PubMed] [Google Scholar]
  • [70].Mellentin C, Jahnsen H, Abraham WC. Priming of long-term potentiation mediated by ryanodine receptor activation in rat hippocampal slices. Neuropharmacology. 2007;52:118–125. doi: 10.1016/j.neuropharm.2006.07.009. [DOI] [PubMed] [Google Scholar]
  • [71].Welsby P, Rowan M, Anwyl R. Nicotinic receptor-mediated enhancement of long-term potentiation involves activation of metabotropic glutamate receptors and ryanodine-sensitive calcium stores in the dentate gyrus. Eur J Neurosci. 2006;24:3109–3118. doi: 10.1111/j.1460-9568.2006.05187.x. [DOI] [PubMed] [Google Scholar]
  • [72].Xie CW. Calcium-regulated signaling pathways: role in amyloid beta-induced synaptic dysfunction. Neuromolecular Med. 2004;6:53–64. doi: 10.1385/NMM:6:1:053. [DOI] [PubMed] [Google Scholar]
  • [73].Chen J, Sroubek J, Krishnan Y, Li Y, Bian J, McDonald TV. PKA phosphorylation of HERG protein regulates the rate of channel synthesis. Am J Physiol Heart Circ Physiol. 2009;296:H1244–1254. doi: 10.1152/ajpheart.01252.2008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [74].Hammond RS, Lin L, Sidorov MS, Wikenheiser AM, Hoffman DA. Protein kinase a mediates activity-dependent Kv4.2 channel trafficking. J Neurosci. 2008;28:7513–7519. doi: 10.1523/JNEUROSCI.1951-08.2008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [75].Lin L, Sun W, Wikenheiser AM, Kung F, Hoffman DA. KChIP4a regulates Kv4.2 channel trafficking through PKA phosphorylation. Mol Cell Neurosci. 2010;43:315–325. doi: 10.1016/j.mcn.2009.12.005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [76].Nuwer MO, Picchione KE, Bhattacharjee A. PKA-induced internalization of slack KNa channels produces dorsal root ganglion neuron hyperexcitability. J Neurosci. 2010;30:14165–14172. doi: 10.1523/JNEUROSCI.3150-10.2010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [77].Hoffman DA, Johnston D. Downregulation of transient K+ channels in dendrites of hippocampal CA1 pyramidal neurons by activation of PKA and PKC. J Neurosci. 1998;18:3521–3528. doi: 10.1523/JNEUROSCI.18-10-03521.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • [78].Esteban JA, Shi SH, Wilson C, Nuriya M, Huganir RL, Malinow R. PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nat Neurosci. 2003;6:136–143. doi: 10.1038/nn997. [DOI] [PubMed] [Google Scholar]
  • [79].Sokolova IV, Lester HA, Davidson N. Postsynaptic mechanisms are essential for forskolin-induced potentiation of synaptic transmission. J Neurophysiol. 2006;95:2570–2579. doi: 10.1152/jn.00617.2005. [DOI] [PubMed] [Google Scholar]

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