Locus Ceruleus Activation Initiates Delayed Synaptic Potentiation of Perforant Path Input to the Dentate Gyrus in Awake Rats: A Novel β-Adrenergic- and Protein Synthesis-Dependent Mammalian Plasticity Mechanism

Journal of Neuroscience

Volumn 24, Issue 3, 2004, Pages 598-604

  Walling, Susan G ^a   Harley, Carolyn W ^a  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

Author keywords

cAMP; Dentate; Hippocampus; Locus ceruleus; LTP; Norepinephrine

Indexed keywords

ANISOMYCIN; CYCLIC AMP; GLUTAMIC ACID; NORADRENALIN; PROPRANOLOL;

ADRENERGIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL TISSUE; APLYSIA; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; EVOKED RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; GRANULE CELL; HORMONE RECEPTOR INTERACTION; IN VITRO STUDY; IN VIVO STUDY; LOCUS CERULEUS; MALE; MAMMAL; MEMORY; NERVE CELL PLASTICITY; NONHUMAN; NORADRENALIN RELEASE; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RAT; RECEPTOR BINDING; SYNAPTIC POTENTIAL; WAKEFULNESS;

ANIMALS; DENTATE GYRUS; ELECTRODES, IMPLANTED; EXCITATORY POSTSYNAPTIC POTENTIALS; GLUTAMIC ACID; INJECTIONS, INTRAVENTRICULAR; LOCUS COERULEUS; LONG-TERM POTENTIATION; MALE; NEURONAL PLASTICITY; PERFORANT PATHWAY; PROTEIN SYNTHESIS INHIBITORS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, BETA; SYNAPTIC TRANSMISSION; TIME FACTORS; WAKEFULNESS;

EID: 0842327275     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4426-03.2004     Document Type: Article

References (59)

1. Abel T, Nguyen PV, Barad M, Deuel TA, Kandel ER, Bourtchouladze R (1997) Genetic demonstration of a role for PKA in the late phase of LTP and in hippocampus-based long-term memory. Cell 88:615-626.
2. Barea-Rodriguez EJ, Rivera DT, Jaffe DB, Martinez Jr JL (2000) Protein synthesis inhibition blocks the induction of mossy fiber long-term potentiation in vivo. J Neurosci 20:8528-8532.
3. Berman DE, Dudai Y (2001) Memory extinction, learning anew, and learning the new: dissociations in the molecular machinery of learning in cortex. Science 291:2417-2419.
4. Berman DE, Hasvi S, Neduva V, Dudai Y (2000) The role of identified neurotransmitter systems in the response of insular cortex to unfamiliar taste: activation of ERK1-2 and formation of a memory trace. J Neurosci 20:7017-7023.
5. Bernabeu R, Schmitz P, Faillace MP, Izquierdo I, Medina JH (1996) Hippocampal cGMP and cAMP are differentially involved in memory processing of inhibitory avoidance learning. NeuroReport 31:585-588.
6. Berridge CW, Foote SL (1991) Effects of locus ceruleus activation on electroencephalographic activity in neocortex and hippocampus. J Neurosci 11:3135-3145.
7. Berridge CW, Waterhouse BD (2003) The locus ceruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes. Brain Res Brain Res Rev 42:33-84.
8. Bramham CR, Bacher SK, Sarvey JM (1997) LTP in the lateral perforant path is β-adrenergic receptor-dependent. NeuroReport 8:719-724.
9. Brunelli M, Castellucci V, Kandel ER (1976) Synaptic facilitation and behavioral sensitization in Aplysia: possible role of serotonin and cyclic AMP. Science 194:1178-1181.
10. Cahill L, Prins B, Weber M, McGaugh JL (1994) Beta-adrenergic activation and memory for emotional events. Nature 371:702-704.
11. Clayton EC, Williams CL (2000) Posttraining inactivation of excitatory afferent input to the locus ceruleus impairs retention in an inhibitory avoidance learning task. Neurobiol Learn Mem 73:127-140.
12. Dahl D, Li J (1994) Induction of long-lasting potentiation by sequenced applications of isoproterenol. NeuroReport 5:657-660.
13. Dahl D, Sarvey JM (1989) Norepinephrine induces pathway-specific long-lasting potentiation and depression in the hippocampal dentate gyrus. Proc Natl Acad Sci USA 86:4776-4780.
14. Dale N, Kandel ER, Schacher S (1987) Serotonin produces long-term changes in the excitability of Aplysia sensory neurons in culture that depend on new protein synthesis. J Neurosci 7:2232-2238.
15. Emptage NJ, Carew TJ (1993) Long-term synaptic facilitation in the absence of short-term facilitation in Aplysia neurons. Science 262:253-256.
16. Frey U, Krug M, Reymann KG, Matthies H (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.
17. Harley CW, Milway JS (1986) Glutamate ejection in the locus ceruleus enhances the perforant path-evoked population spike in the dentate gyrus. Exp Brain Res 63:143-150.
18. Harley CW, Sara SJ (1992) Locus ceruleus bursts induced by glutamate trigger delayed perforant path spike amplitude potentiation in the dentate gyrus. Exp Brain Res 89:581-587.
19. Harley CW, Milway JS, Lacaille J-C (1989) Locus ceruleus potentiation of dentate gyrus responses: evidence for two systems. Brain Res Bull 22:643-650.
20. Huang YY, Kandel ER (1996) Modulation of both the early and the late phase of mossy fiber LTP by the activation of β-adrenergic receptors. Neuron 16:611-617.
21. Huang YY, Nguyen PV, Abel T, Kandel ER (1996) Long-lasting forms of synaptic potentiation in the mammalian hippocampus. Learn Mem 3:74-85.
22. Huang YY, Martin KC, Kandel ER (2000) Both protein kinase A and mitogen-activated protein kinase are required in the amygdala for the macromolecular synthesis-dependent late phase of long-term potentiation. J Neurosci 20:6317-6325.
23. Izquierdo I, Beamish DG, Anisman H (1979) Effect of an inhibitor of dopamine-β-hydroxylase on the acquisition and retention of four different avoidance tasks in mice. Psychopharmacology (Berl) 63:173-178.
24. Izquierdo I, Medina JH, Izquierdo LA, Barros DM, de Souza MM, Souza T (1998) Short- and long-term memory are differentially regulated by monominergic systems in the rat brain. Neurobiol Learn Mem 69:219-224.
25. Izquierdo LA, Barros DM, Vianna MR, Coitinho A, deDavid e Silva T, Choi H, Moletta B, Medina JH, Izquierdo I (2002) Molecular pharmacological dissection of short- and long-term memory. Cell Mol Neurobiol 22:269-287.
26. Kety SS (1970) The biogenic amines in the central nervous system: their possible roles in arousal, emotion and learning. In: The neurosciences: second study program (Schmidt FO, ed), pp 324-335. New York: Rockefeller Press.
27. Klukowski G, Harley CW (11994) Locus ceruleus activation induces perforant path-evoked population spike potentiation in the dentate gyrus of awake rat. Exp Brain Res 102:165-170.
28. Kobayashi K, Noda Y, Matsushita N, Nishii K, Sawada H, Nagatsu T, Nakahara D, Fukabori R, Yasoshima Y, Yamamoto T, Miura M, Kano M, Mamiya T, Miyamoto Y, Nabeshima T (2000) Modest neuropsychological deficits caused by reduced noradrenaline metabolism in mice heterozygous for a mutated tyrosine hydroxylase gene. J Neurosci 20:2418-2426.
29. Koh MT, Thiele TE, Bernstein IL (2002) Inhibition of protein kinase A activity interferes with long-term, but not short-term, memory of conditioned taste aversions. Behav Neurosci 116:1070-1074.
30. Krug M, Lossner B, Ott T (1984) Anisomycin blocks the late phase of long-term potentiation in the dentate gyrus of freely moving rats. Brain Res Bull 13:39-42.
31. Lacaille J-C, Harley CW (1985) The action of norepinephrine in the dentate gyrus: beta-mediated facilitation of evoked potentials in vitro. Brain Res 358:210-220.
32. Mauelshagen J, Sherff CM, Carew TJ (1998) Differential induction of long-term synaptic facilitation by spaced and massed applications of serotonin at sensory neuron synapses of Aplysia californica. Learn Mem 5:246-256.
33. McIntyre CK, Hatfield T, McGaugh JL (2002) Amygdala norepinephrine levels after training predict inhibitory avoidance retention performance in rats. Eur J Neurosci 16:1223-1226.
34. Montarolo PG, Goelet P, Castellucci VF, Morgan J, Kandel ER, Schacher S (1986) A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science 234:1249-1254.
35. Neuman RS, Harley CW (1983) Long-lasting potentiation of the dentate gyrus population spike by norepinephrine. Brain Res 273:162-165.
36. Nguyen PV, Kandel ER (1996) A macromolecular synthesis-dependent late phase of long-term potentiation requiring cAMP in the medial perforant pathway of rat hippocampal slices. J Neurosci 16:3189-3198.
37. Nguyen PV, Kandel ER (1997) Brief theta-burst stimulation induces a transcription-dependent late phase of LTP requiring cAMP in area CA1 of the mouse hippocampus. Learn Mem 4:230-243.
38. Nielson KA, Jensen RA (1994) Beta-adrenergic receptor antagonist antihypertensive medications impair arousal-induced modulation of working memory in elderly humans. Behav Neural Biol 62:190-200.
39. Quevedo J, Sant' Anna MK, Madruga M, Lovato I, de Paris F, Kapczinski F, Izquierdo I, Cahill L (2003) Differential effects of emotional arousal in short-term and long-term memory in healthy adults. Neurobiol Learn Mem 79:132-135.
40. Roullet P, Sara S (1998) Consolidation of memory after its reactivation: involvement of beta noradrenergic receptors in the late phase. Neural Plast 6:63-68.
41. Sara SJ, Roullet P, Przybyslawksi J (1999) Consolidation of memory for odor-reward association: beta-adrenergic receptor involvement in the late phase. Learn Mem 6:88-96.
42. Sarvey JM, Burgard EC, Decker G (1989) Long-term potentiation: studies in the hippocampal slice. J Neurosci Methods 28:109-124.
43. Schacher S, Castellucci VF, Kandel ER (1988) CAMP evokes long-term facilitation in Aplysia sensory neurons that requires new protein synthesis. Science 240:1667-1669.
44. Schulz S, Siemer H, Krug M, Hollt V (1999) Direct evidence for biphasic cAMP responsive element-binding protein phosphorylation during long-term potentiation in the rat dentate gyrus in vivo. J Neurosci 19:5682-5692.
45. Seidenbecher T, Reymann KG, Balschun D (1997) Post-tetanic time window for the reinforcement of long-term potentiation by appetitive and aversive stimuli. Proc Natl Acad Sci USA 94:1494-1499.
46. Sherff CM, Carew TJ (1999) Coincident induction of long-term facilitation in Aplysia: cooperativity between cell bodies and remote synapses. Science 285:1911-1914.
47. Silva AJ, Kogan JH, Frankland PW, Kida S (1998) CREB science memory. Annu Rev Neurosci 21:127-148.
48. Stone EA, Zhang Y, Carr KD (1995) Massive activation of c-fos in forebrain after mechanical stimulation of the locus ceruleus. Brain Res Bull 36:77-80.
49. Straube T, Frey JU (2003) Involvement of β-adrenergic receptors in protein synthesis-dependent late long-term potentiation (LTP) in the dentate gyrus of freely moving rats: the critical role of the LTP induction strength. Neuroscience 119:473-479.
50. Straube T, Korz Z, Balshun D and Frey JU (2003) Requirement of β-adrenergic receptor activation and protein synthesis for LTP-reinforcement by novelty in rat dentate gyrus. J Physiol (Lond), 552:953-960.
51. Sullivan EV, Sagar HJ (1991) Double dissociation of short-term and long-term memory for nonverbal material in Parkinson's disease and global amnesia, A further analysis. Brain 114:893-906.
52. Sullivan RM, Wilson DM, Leon M (1989) Norepinephrine and learning-induced plasticity in infant rat olfactory system. J Neurosci 9:3998-4006.
53. Sullivan RM, Stackenwalt G, Nasr F, Lemon C, Wilson DA (2000) Association of an odor with activation of olfactory bulb noradrenergic β-receptors or locus ceruleus stimulation is sufficient to produce learned approach responses to that odor in neonatal rats. Behav Neurosci 114:957-962.
54. Vankov A, Hervé-Minvielle A, Sara SJ (1995) Response to novelty and its rapid habituation in locus ceruleus neurons of the freely exploring rat. Eur J Neurosci 7:1180-1187.
55. van Stegeren AH, Everaerd W, Cahill L, McGaugh JL, Gooren LJ (1998) Memory for emotional events: differential effects of centrally versus peripherally acting β-blocking agents. Psychopharmacology (Berl) 138:305-310.
56. Warrington EK (1979) Neuropsychological evidence for multiple memory systems. Ciba Found Symp 153-166.
57. 2-receptor-mediated inhibition of norepinephrine release at locus ceruleus synapses in dentate gyrus. J Neurosci 9:2131-2140.
58. Yuan Q, Harley CW, Bruce JC, Darby-King A, Mclean JH (2000) Isoproterenol increases CREB phosphorylation and olfactory nerve potentials in normal and 5-HT-depleted olfactory bulbs in rat pups only at doses that produce odor preference learning. Learn Mem 7:413-421.
59. 2A receptor colocalization and cAMP coregulation: a new model of norepinephrine-induced learning in the olfactory bulb. Learn Mem 10:5-15.