Selective tuning of hippocampal oscillations by phasic locus coeruleus activation in awake male rats

Hippocampus

Volumn 21, Issue 11, 2011, Pages 1250-1262

  Walling, Susan G ^a   Brown, Robert A M ^a   Milway, J Stephen ^a   Earle, Avery G ^a   Harley, Carolyn W ^a  

^a MEMORIAL UNIVERSITY OF NEWFOUNDLAND   (Canada)

Author keywords

EEG; Gamma; Noradrenaline; Norepinephrine; Theta

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITION; ELECTROENCEPHALOGRAM; HIPPOCAMPUS; HIPPOCAMPUS THETA RHYTHM; LOCUS CERULEUS; LONG TERM POTENTIATION; MALE; NONHUMAN; NORADRENALIN RELEASE; OSCILLATION; PRIORITY JOURNAL; RAT;

ANIMALS; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS; GLUTAMIC ACID; HIPPOCAMPUS; LOCUS COERULEUS; LONG-TERM POTENTIATION; MALE; NOREPINEPHRINE; RATS; RATS, SPRAGUE-DAWLEY; WAKEFULNESS;

EID: 80054860919     PISSN: 10509631     EISSN: 10981063     Source Type: Journal    
DOI: 10.1002/hipo.20816     Document Type: Article

References (54)

1. Adams LM, Foote SL. 1988. Effects of locally infused pharmacological agents on spontaneous and sensory-evoked activity of locus coeruleus neurons. Brain Res Bull 21: 395-400.
2. Aston-Jones G, Bloom FE. 1981a. Activity of norepinephrine-containing locus coeruleus neurons in behaving rats anticipates fluctuations in the sleep-waking cycle. J Neurosci 1: 876-886.
3. Aston-Jones G, Bloom FE. 1981b. Norepinephrine-containing locus coeruleus neurons in behaving rats exhibit pronounced responses to non-noxious environmental stimuli. J Neurosci 1: 887-900.
4. Aston-Jones G, Cohen JD. 2005. An integrative theory of locus coeruleus-norepinephrine function: Adaptive gain and optimal performance. Annu Rev Neurosci 28: 403-450.
5. Aston-Jones G, Chiang C, Alexinsky T. 1991. Discharge of noradrenergic locus coeruleus neurons in behaving rats and monkeys suggests a role in vigilance. Prog Brain Res 88: 501-520.
6. Axmacher N, Mormann F, Fernandez G, Elger CE, Fell J. 2006. Memory formation by neuronal synchronization. Brain Res Rev 52: 170-182.
7. Berridge CW. 2008. Noradrenergic modulation of arousal. Brain Res Rev 58: 1-17.
8. Berridge CW, Foote SL. 1991. Effects of locus coeruleus activation on electroencephalographic activity in neocortex and hippocampus. J Neurosci 11: 3135-3145.
9. Berridge CW, Foote SL. 1994. Locus coeruleus-induced modulation of forebrain electroencephalographic (EEG) state in halothane-anesthetized rat. Brain Res Bull 35: 597-605.
10. Berridge CW, Foote SL. 1996. Enhancement of behavioral and electroencephalographic indices of waking following stimulation of noradrenergic beta-receptors within the medial septal region of the basal forebrain. J Neurosci 16: 6999-7009.
11. Berridge CW, Wifler K. 2000. Contrasting effects of noradrenergic β-receptor blockade within the medial septal area on forebrain electroencephalographic and behavioral activity state in anesthetized and unanesthetized rat. Neuroscience 97: 543-552.
12. Berridge CW, Bolen SJ, Manley MS, Foote SL. 1996. Modulation of forebrain electroencephalographic activity in halothane-anesthetized rat via actions of noradrenergic beta-receptors within the medial septal region. J Neurosci 16: 7010-7020.
13. Bouret S, Sara SJ. 2004. Reward expectation, orientation of attention and locus coeruleus-medial frontal cortex interplay during learning. Eur J Neurosci 20: 791-802.
14. Bouret S, Sara SJ. 2005. Network reset: A simplified overarching theory of locus coeruleus noradrenaline function. Trends Neurosci 28: 574-582.
15. Brown RAM, Walling SG, Milway JS, Harley CW. 2005. Locus ceruleus activation suppresses feedforward interneurons and reduces beta-gamma electroencephalogram frequencies while it enhances theta frequencies in rat dentate gyrus. J Neurosci 25: 1985-1991.
16. Buzsáki G. 2006. Rhythms of the Brain. NY: Oxford University Press.
17. Buzsáki G, Draguhn A. 2004. Neuronal oscillations in cortical networks. Science 304: 1926-1929.
18. Christie BR, Stellwagen D, Abraham WC. 1995. Reduction of the threshold for long-term potentiation by prior theta-frequency synaptic activity. Hippocampus 5: 52-59.
19. Gengler S, Mallot HA, Holscher C. 2005. Inactivation of the rat dorsal striatum impairs performance in spatial tasks and alters hippocampal theta in the freely moving rat. Behav Brain Res 164: 73-82.
20. Gray CM, Konig P, Engel AK, Singer W. 1989. Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338: 334-337.
21. Gray JA. 1971. Medial septal lesions, hippocampal theta rhythm and the control of vibrissal movement in the freely moving rat. Electroencephalogr Clin Neurophysiol 30: 189-197.
22. Gray JA. 1978. The neuropsychology of anxiety. Br J Psychol 69: 417-434.
23. Gray JA, Ball GG. 1970. Frequency-specific relation between hippocampal theta rhythm, behavior, and amobarbital action. Science 168: 1246-1248.
24. Gray JA, McNaughton N, James DT, Kelly PH. 1975. Effect of minor tranquillisers on hippocampal theta rhythm mimicked by depletion of forebrain noradrenaline. Nature 258: 424-425.
25. Gray JA, Davis N, Feldon J, Nicholas J, Rawlins P, Owen SR. 1981. Animal models of anxiety. Prog Neuropsychopharmacol 5: 143-157.
26. Greenstein YJ, Pavlides C, Winson J. 1988. Long-term potentiation in the dentate gyrus is preferentially induced at theta rhythm periodicity. Brain Res 438: 331-334.
27. Hajós M, Hoffmann WE, Robinson DD, Yu JH, Hajós-Korcsok E. 2003. Norepinephrine but not serotonin reuptake inhibitors enhance theta and gamma activity of the septo-hippocampal system. Neuropsychopharm 28: 857-864.
28. Harley CW. 2007. Norepinephrine and the dentate gyrus. Prog Brain Res 163: 299-318.
29. Harley CW, Milway JS. 1986. Glutamate ejection in the locus coeruleus enhances the perforant path-evoked population spike in the dentate gyrus. Exp Brain Res 63: 143-150.
30. Harley CW, Sara SJ. 1992. Locus coeruleus bursts induced by glutamate trigger delayed perforant path spike amplitude potentiation in the dentate gyrus. Exp Brain Res 89: 581-587.
31. Harley CW, Milway JS, Lacaille JC. 1989. Locus coeruleus potentiation of dentate gyrus responses: Evidence for two systems. Brain Res Bull 22: 643-650.
32. Harley CW, Lalies MD, Nutt DJ. 1996. Estimating the synaptic concentration of norepinephrine in dentate gyrus which produces β-receptor mediated long-lasting potentiation in vivo using microdialysis and intracerebroventricular norepinephrine. Brain Res 710: 293-298.
33. Herve-Minvielle A, Sara SJ. 1995. Rapid habituation of auditory responses of locus coeruleus cells in anaesthetized and awake rats. Neuroreport 6: 1363-1368.
34. McNaughton N, Gray JA. 2000. Anxiolytic action on the behavioural inhibition system implies multiple types of arousal contribute to anxiety. J. Affect Disord 61: 161-176.
35. McNaughton N, James DTD, Stewart J, Gray JA, Valero I, Drewnowski A. 1977. Septal driving of hippocampal theta rhythm as a function of frequency in the male rat: Effects of drugs. Neuroscience 2: 1019-1027.
36. McNaughton N, Ruan M, Woodnorth MA. 2006. Restoring theta-like rhythmicity in rats restores initial learning in the Morris water maze. Hippocampus 16: 1102-1110.
37. Miura Y, Ito T, Kadokawa T. 1987. Effects of intraseptally injected dopamine and noradrenaline on hippocampal synchronized theta wave activity in rats. Jpn J Pharmacol 44: 471-479.
38. Olvera-Cortes E, Cervantes M, Gonzalez-Burgos I. 2002. Place-learning, but not cue-learning training, modifies the hippocampal theta rhythm in rats. Brain Res Bull 58: 261-270.
39. Orr G, Rao G, Houston FP, McNaughton BL, Barnes CA. 2001. Hippocampal synaptic plasticity is modulated by theta rhythm in the fascia dentata of adult and aged freely behaving rats. Hippocampus 11: 647-654.
40. Palamarchouk VS, Zhang J, Zhou G, Swiergiel AH, Dunn AJ. 2000. Hippocampal norepinephrine-like voltammetric responses following infusion of corticotropin-releasing factor into the locus coeruleus. Brain Res Bull 51: 319-326.
41. Palamarchouk VS, Swiergiel AH, Dunn AJ. 2002. Hippocampal noradrenergic responses to CRF injected into the locus coeruleus of unanesthetized rats. Brain Res 950: 31-38.
42. Pavlides C, Greenstein YJ, Grudman M, Winson J. 1988. Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta-rhythm. Brain Res 439: 383-387.
43. Quintero S, Mellanby J, Thompson MR, Nordeen H, Nutt D, McNaughton N, Gray JA. 1985. Septal driving of hippocampal theta rhythm: Role of gamma-aminobutyrate-benzodiazepine receptor complex in mediating effects of anxiolytics. Neuroscience 16: 875-884.
44. Reid AT, Harley CW. 2009. An associativity requirement for locus coeruleus-induced long-term potentiation in the dentate gyrus of the urethane-anesthetized rat. Exp Brain Res 200: 151-159.
45. Robinson TE, Vanderwolf CH. 1978. Electrical stimulation of the brain stem in freely moving rats: II. Effects on hippocampal and neocortical electrical activity, and relations to behavior. Exp Neurol 61: 485-515.
46. Robinson TE, Vanderwolf CH, Pappas BA. 1977. Are the dorsal noradrenergic bundle projections from the locus coeruleus important for neocortical or hippocampal activation? Brain Res 138: 75-98.
47. Sara SJ. 2009. The locus coeruleus and noradrenergic modulation of cognition. Nat Rev Neurosci 10: 211-223.
48. Sara SJ, Segal M. 1991. Plasticity of sensory responses of locus coeruleus neurons in the behaving rat: implications for cognition. Prog Brain Res 88: 571-585.
49. Shiekhattar R, Aston-Jones G, Chiang C. 1991. Local infusion of calcium-free solutions in vivo activates locus coeruleus neurons. Brain Res Bull 27: 5-12.
50. Stone EA, Zhang Y, Carr KD. 1995. Massive activation of c-fos in forebrain after mechanical stimulation of the locus coeruleus. Brain Res Bull 36: 77-80.
51. Vanderwolf CH. 1969. Hippocampal electrical activity and voluntary movement in the rat. Electroencephalogr Clin Neurophysiol 26: 407-418.
52. Vankov A, Herve-Minvielle A, Sara SJ. 1995. Response to novelty and its rapid habituation in locus coeruleus neurons of the freely exploring rat. Eur J Neurosci 7: 1180-1187.
53. Walling SG, Harley CW. 2004. 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. J Neurosci 24: 598-604.
54. Walling SG, Nutt DJ, Lalies MD, Harley CW. 2004. Orexin-A infusion in the locus ceruleus triggers norepinephrine (NE) release and NE-induced long-term potentiation in the dentate gyrus. J Neurosci 24: 7421-7426.