Andersen P, Sundberg SH, Sveen O, Wigstro¨m H (1977) Specific longlasting
potentiation of synaptic transmission in hippocampal slices.
Nature 266:736 –737.
Bito H, Deisseroth K, TsienRW (1996) CREB phosphorylation and dephosphorylation:
a Ca 2- and stimulus duration-dependent switch for hippocampal
gene expression. Cell 87:1203–1214.
Bliss TV, Lomo T (1973) Long-lasting potentiation of synaptic transmission
in the dentate area of the anaesthetized rabbit following stimulation of the
perforant path. J Physiol 232:331–356.
Braun AP, Schulman H (1995) The multifunctional calcium/calmodulindependent
protein kinase: from form to function. Annu Rev Physiol
57:417– 445.
Erondu NE, Kennedy MB (1985) Regional distribution of type II Ca2/
calmodulin-dependent protein kinase in rat brain. J Neurosci 5:3270–
3277.
Fonseca R, Na¨gerl UV, Morris RG, Bonhoeffer T (2004) Competing for
memory: hippocampal LTP under regimes of reduced protein synthesis.
Neuron 44:1011–1020.
Fonseca R, Na¨gerl UV, Bonhoeffer T (2006) Neuronal activity determines
the protein synthesis dependence of long-term potentiation. Nat Neurosci
9:478–480.
Frey U, Morris RGM (1997) Synaptic tagging and long-term potentiation.
Nature 385:533–536.
Frey U, MorrisRGM (1998a) Weak before strong: dissociating synaptic tagging
and plasticity-factor accounts of late-LTP. Neuropharmacology
37:545–552.
Frey U, Morris RGM (1998b) Synaptic tagging: implications for late maintenance
of hippocampal long-term potentiation. Trends Neurosci
21:181–188.
Frey U, Krug M, Reymann KG, MatthiesH (1988) Anisomycin, an inhibitor
of protein synthesis, blocks late phases of LTP phenomena in the hippocampal
CA1 region in vitro. Brain Res 452:57– 65.
Giese KP, Fedorov NB, Filipkowski RK, Silva AJ (1998) Autophosphorylation
at Thr286 of the alpha calcium-calmodulin kinase II in LTP and
learning. Science 279:870–873.
Hansel C, de Jeu M, Belmeguenai A, Houtman SH, Buitendijk GH, Andreev
D, De Zeeuw CI, Elgersma Y (2006) alphaCaMKII Is essential for cerebellar
LTD and motor learning. Neuron 51:835– 843.
Hanson PI, Meyer T, Stryer L, Schulman H (1994) Dual role of calmodulin
in autophosphorylation of multifunctional CaM kinase may underlie decoding
of calcium signals. Neuron 12:943–956.
Ho N, Liauw JA, Blaeser F, Wei F, Hanissian S, Muglia LM, Wozniak DF,
Nardi A, Arvin KL, Holtzman DM, Linden DJ, Zhuo M, Muglia LJ,
Chatila TA (2000) Impaired synaptic plasticity and cAMP response
element-binding protein activation in Ca2/calmodulin-dependent protein
kinase type IV/Gr-deficient mice. J Neurosci 20:6459–6472.
Ho OH, Delgado JY, O’Dell TJ (2004) Phosphorylation of proteins involved
in activity-dependent forms of synaptic plasticity is altered in hippocampal
slices maintained in vitro. J Neurochem 91:1344 –1357.
Ishida A, Kameshita I, Okuno S, Kitani T, Fujisawa H (1995) A novel highly
specific and potent inhibitor of calmodulin-dependent protein kinase II.
Biochem Biophys Res Commun 212:806–812.
Kang H, Sun LD, Atkins CM, Soderling TR, Wilson MA, Tonegawa S (2001)
An important role of neural activity-dependent CaMKIV signaling in the
consolidation of long-term memory. Cell 106:771–783.
Kawashima T, Okuno H, Nonaka M, Adachi-Morishima A, Kyo N, Okamura
M, Takemoto-Kimura S, Worley PF, Bito H (2009) Synaptic activityresponsive
element in the Arc/Arg3.1 promoter essential for synapse-tonucleus
signaling in activated neurons. Proc Natl Acad Sci U S A
106:316 –321.
Krug M, Lo¨ssner B, Ott T (1984) Anisomycin blocks the late phase of longterm
potentiation in the dentate gyrus of freely moving rats. Brain Res
Bull 13:39–42.
Leutgeb JK, Frey JU, Behnisch T (2003) LTP in cultured hippocampalentorhinal
cortex slices from young adult (P25-30) rats. J Neurosci Methods
130:19 –32.
Lisman J, Schulman H, Cline H (2002) The molecular basis of CaMKII
function in synaptic and behavioural memory. Nat Rev Neurosci
3:175–190.
Lisman JE, Goldring MA (1988) Feasibility of long-term storage of graded
information by the Ca2/calmodulin-dependent protein kinase molecules
of the postsynaptic density. Proc Natl Acad SciU S A 85:5320 –5324.
Lisman JE, Zhabotinsky AM (2001) A model of synaptic memory: a
CaMKII/PP1 switch that potentiates transmission by organizing an
AMPA receptor anchoring assembly. Neuron 31:191–201.
Malenka RC, Kauer JA, Perkel DJ, Mauk MD, Kelly PT, Nicoll RA, Waxham
MN (1989) An essential role for postsynaptic calmodulin and protein
kinase activity in long-term potentiation. Nature 340:554 –557.
Malinow R, Schulman H, Tsien RW (1989) Inhibition of postsynaptic PKC
or CaMKII blocks induction but not expression of LTP. Science
245:862– 866.
Martin KC, Casadio A, Zhu H, Yaping E, Rose JC, Chen M, Bailey CH, Kandel
ER (1997) Synapse-specific, long-term facilitation of aplysia sensory to
motor synapses: a function for local protein synthesis in memory storage.
Cell 91:927–938.
Meyer T, Hanson PI, Stryer L, Schulman H (1992) Calmodulin trapping by
calcium-calmodulin-dependent protein kinase. Science 256:1199 –1202.
Miller P, Zhabotinsky AM, Lisman JE, Wang XJ (2005) The stability of a
stochastic CaMKII switch: dependence on the number of enzyme molecules
and protein turnover. PLoS Biol 3:e107.
Miller SG, Kennedy MB (1986) Regulation of brain type II Ca2/
calmodulin-dependent protein kinase by autophosphorylation: a Ca 2-
triggered molecular switch. Cell 44:861– 870.
Moncada D, ViolaH (2007) Induction of long-term memory by exposure to
novelty requires protein synthesis: evidence for a behavioral tagging.
J Neurosci 27:7476 –7481.
Navakkode S, Sajikumar S, Frey JU (2007) Synergistic requirements for the
induction of dopaminergic D1/D5-receptor-mediated LTP in hippocampal
slices of rat CA1 in vitro. Neuropharmacology 52:1547–1554.
O’Carroll CM, Morris RGM (2004) Heterosynaptic co-activation of glutamatergic
and dopaminergic afferents is required to induce persistent
long-term potentiation. Neuropharmacology 47:324 –332.
Ouyang Y, Kantor D, Harris KM, Schuman EM, Kennedy MB (1997) Visualization
of the distribution of autophosphorylated calcium/calmodulindependent
protein kinase II after tetanic stimulation in the CA1 area of
the hippocampus. J Neurosci 17:5416 –5427.
Reymann KG, Frey JU (2007) The late maintenance of hippocampal LTP:
requirements, phases, “synaptic tagging”, “late-associativity” and implications.
Neuropharmacology 52:24–40.
Rose J, Jin SX, CraigAM (2009) Heterosynaptic molecular dynamics: locally
induced propagating synaptic accumulation of CaM kinase II. Neuron
61:351–358.
Sajikumar S, Navakkode S, Frey JU (2005) Protein synthesis-dependent
long-term functional plasticity: methods and techniques. Curr Opin Neurobiol
15:607– 613.
Sajikumar S, Navakkode S, Frey JU (2007) Identification of compartmentand
process-specific molecules required for “synaptic tagging” during
long-term potentiation and long-term depression in hippocampal CA1.
J Neurosci 27:5068 –5080.
Sajikumar S, Navakkode S, Frey JU (2008) Distinct single but not necessarily
repeated tetanization is required to induce hippocampal late-LTP in the
rat CA1. Learn Mem 15:46–49.
Sanhueza M, McIntyre CC, Lisman JE (2007) Reversal of synaptic memory
by Ca2/calmodulin-dependent protein kinase II inhibitor. J Neurosci
27:5190 –5199.
Schurr A, Reid KH, Tseng MT, Edmonds HL Jr, West CA, Rigor BM (1986)
Effect of electrical stimulation on the viability of the hippocampal slice
preparation. Brain Res Bull 16:299 –301.
Schwartzkroin PA, Wester K (1975) Long-lasting facilitation of a synaptic
potential following tetanization in the in vitro hippocampal slice. Brain
Res 89:107–119.
Sumi M, Kiuchi K, Ishikawa T, Ishii A, Hagiwara M, Nagatsu T, Hidaka H
(1991) The newly synthesized selective Ca2/calmodulin dependent
protein kinase II inhibitor KN-93 reduces dopamine contents in PC12h
cells. Biochem Biophys Res Commun 181:968 –975.
Tokumitsu H, Inuzuka H, Ishikawa Y, Ikeda M, Saji I, Kobayashi R (2002)
STO-609, a specific inhibitor of the Ca2�/calmodulin-dependent protein
kinase kinase. J Biol Chem 277:15813–15818.
Yamauchi T (2005) Neuronal Ca2/calmodulin-dependent protein kinase
II—discovery, progress in a quarter of a century, and perspective: implication
for learning and memory. Biol Pharm Bull 28:1342–1354.
Zhang YP, Holbro N, Oertner TG (2008) Optical induction of plasticity at
single synapses reveals input-specific accumulation of CaMKII. Proc
Natl Acad Sci U S A 105:12039 –12044.