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Cited by 92Neuroscience and Neuropharmacology ResearchMemory and Neural MechanismsNeural dynamics and brain function

Hippocampal long‐term potentiation that is elicited by perforant path stimulation or that occurs in conjunction with spatial learning is tightly controlled by beta‐adrenoreceptors and the locus coeruleus

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Hansen, Niels, Manahan‐Vaughan, Denise·2015·Hippocampus
DOI 10.1002/hipo.22436PMC PMC6680149
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Abstract

The noradrenergic system, driven by locus coeruleus (LC) activation, plays a key role in the regulating and directing of changes in hippocampal synaptic efficacy. The LC releases noradrenaline in response to novel experience and LC activation leads to an enhancement of hippocampus‐based learning, and facilitates synaptic plasticity in the form of long‐term depression (LTD) and long‐term potentiation (LTP) that occur in association with spatial learning. The predominant receptor for mediating these effects is the β‐adrenoreceptor. Interestingly, the dependency of synaptic plasticity on this receptor is different in the hippocampal subfields whereby in the CA1 in vivo, LTP, but not LTD requires β‐adrenoreceptor activation, whereas in the mossy fiber synapse LTP and LTD do not depend on this receptor. By contrast, synaptic plasticity that is facilitated by spatial learning is highly dependent on β‐adrenoreceptor activation in both hippocampal subfields. Here, we explored whether LTP induced by perforant‐path (pp) stimulation in vivo or that is facilitated by spatial learning depends on β‐adrenoreceptors. We found that under both LTP conditions, antagonising the receptors disabled the persistence of LTP. β‐adrenoreceptor‐antagonism also prevented spatial learning. Strikingly, activation of the LC before high‐frequency stimulation (HFS) of the pp prevented short‐term potentiation but not LTP, and LC stimulation after pp‐HFS‐induced depotentiation of LTP. This depotentiation was prevented by β‐adrenoreceptor‐antagonism. These data suggest that β‐adrenoreceptor‐activation, resulting from noradrenaline release from the LC during enhanced arousal and learning, comprises a mechanism whereby the duration and degree of LTP is regulated and fine tuned. This may serve to optimize the creation of a spatial memory engram by means of LTP and LTD. This process can be expected to support the special role of the dentate gyrus as a crucial subregional locus for detecting and processing novelty within the hippocampus. © 2015 The Authors Hippocampus Published by Wiley Periodicals, Inc.

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  • Isoproterenol is a β1 and β2 adrenergic receptor agonist known to activate adenylyl cyclase via Gs proteins.

    “we applied 1 μM isoproterenol, a β1 and β2 adrenergic receptor agonist, known to activate AC via Gs proteins (Fig 2D–2K) [52–54].”

    From Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons (2024) · cites this paper as [53]

    The Materials and Methods section identifies isoproterenol as a β-adrenoreceptor agonist. The Discussion says β-adrenoreceptor activation stimulates the cAMP/PKA cascade and mentions β1 and β2 receptors, but our copy does not specify that isoproterenol acts at both subtypes or activates adenylyl cyclase via Gs proteins. Page numbers are unavailable in our copy. (LLM, conf=0.86)

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References 100 · Cited by 92

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  1. Abraham WC, McNaughton N. 1984 Differences in synaptic transmission between medial and lateral components of the perforant path. Brain Res 303: 251– 260. 6331573
  2. Almaguer‐Melian W, Rojas‐Reyes Y, Alvare A, Rosillo JC, Frey JU, Bergado JA. 2005 Long‐term potentiation in the dentate gyrus in freely moving rats is reinforced by intraventricular application of norepinephrine, but not oxotremorine. Neurobiol Learn Mem 83: 72– 78. 15607691
  3. 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. 16022602
  4. Bashir ZI, Bortolotto ZA, Davies CH, Berretta N, Irving AJ, Seal AJ, Henley JM, Jane DE, Watkins JC, Collingridge GL. 1993 Induction of LTP in the hippocampus needs synaptic activation of glutamate metabotropic receptors. Nature 363: 347– 350. 8388549
  5. Bliss TV, Collingridge GL. 1993 A synaptic model of memory: Long‐term potentiation in the hippocampus. Nature 361: 31– 39. 8421494
  6. Bliss TV, Gardner‐Medwin AR. 1973 Long‐lasting potentiation of synaptic transmission in the dentate area of the unanaestetized rabbit following stimulation of the perforant path. J Physiol 232: 357‐3 74. 4727085 PMC1350459
  7. 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: 331‐3 56. 4727084 PMC1350458
  8. Booze RM, Crisostomo EA, Davis JN. 1993 Beta‐adrenergic receptors in the hippocampal and retrohippocampal regions of rats and guinea pigs: Autoradiographic and immunohistochemical studies. Synapse 13: 206– 214. 8098879
  9. Bramham CR, Bacher‐Svendsen K, Sarvey JM. 1997 LTP in the lateral perforant path is beta‐adrenergic receptor‐dependent. Neuroreport 8: 719– 724. 9106754
  10. Bramham CR. 2008 Local protein synthesis, actin dynamics, and LTP consolidation. Curr Opin Neurobiol 18: 524– 531. 18834940
  11. Bronzino JD, Kehoe P, Mallinson K, Fortin DA. 2001 Increased extracellular release of hippocampal NE is associated with tetanization of the medial perforant pathway in the freely moving adult male rat. Hippocampus 11: 423– 429. 11530847
  12. Bouret S, Sara SJ. 2005 Network reset: A simplified overarching theory of locus coeruleus noradrenaline function. Trends Neurosci 28: 574– 582. 16165227
  13. Brown RA, 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. 15728838 PMC6726066
  14. Cheng S. 2013 The CRISP theory of hippocampal function in episodic memory. Frontiers in Neural Circuits 7: 1– 14. 23653597 PMC3644677
  15. Connor SA, Wang YT, Nguyen PV. 2011 Activation of {beta}‐adrenergic receptors facilitates heterosynaptic translation‐dependent long‐term potentiation. J Physiol 589: 4321– 4340. 21746789 PMC3180585
  16. Connor SA, Maity S, Roy B, Ali DW, Nguyen PV. 2012 Conversion of short‐term potentiation to long‐term potentiation in mouse CA1 by coactivation of β‐adrenergic and muscarinic receptors. Learn Mem 19: 535– 542. 23077334
  17. Cox DJ, Racca C, Lebeau FEN. 2008 adrenergic receptors are differentially expressed in distinct interneuron subtypes in the rat hippocampus. The J Comp Neurol 509: 551– 565. 18546278
  18. Dahl D, Winson J. 1985 Action of norepinephrine in the dentate gyrus. I. Stimulation of locus coeruleus. Exp Brain Res 53: 491– 496. 4029325
  19. Devauges V, Sara SJ. 1991 Memory retrieval enhancement by locus coeruleus stimulation: evidence for mediation by beta‐receptors 43: 93– 97. 1650233
  20. Ezrokhi VL, Zosimovskii VA, Korshunov VA, Markevich VA. 1999 Restoration of decaying long‐term potentiation in the hippocampal formation by stimulation of neuromodulatory nuclei in freely moving rats. Neuroscience 88: 741– 753. 10363814
  21. Fallon JH, Loughlin SE. 1987 Monoamine innervation of cerebral cortex and a theory of the role of monoamines in cerebral cortex and basal ganglia In: Jones EG, Peters A, editors. Cerebral Cortex, Vol. 6 New York: Plenum pp 41– 127.
  22. Gelinas JN, Nguyen PV. 2005 Beta‐adrenergic receptor activation facilitates induction of a protein synthesis‐dependent late phase of long‐term potentiation. J Neurosci 25: 3294– 3303. 15800184 PMC6724894
  23. Gibbs ME, Hutchinson DS, Summers RJ. 2010 Noradrenaline release in the locus coeruleus modulates memory formation and consolidation; roles for α‐ and β‐adrenergic receptors. Neuroscience 170: 1209– 1222. 20709158
  24. Gilbert PE, Brushfield AM. 2009 The role of the CA3 hippocampal subregion in spatial memory: A process oriented behavioral assessment. Prog Neuropsychopharamcol Biol Psychiatry 33: 774– 781. PMC2743458 19375477
  25. Goh JJ, Manahan‐Vaughan D. 2012 Spatial object recognition enables endogenous LTD that curtails LTP in the mouse hippocampus. Cereb Cortex 23: 1118‐ 1122. 22510536 PMC3615348
  26. Goh JJ, Manahan‐Vaughan D. 2013 Hippocampal long‐term depression in freely behaving mice requires the activation of beta‐adrenergic receptors. Hippocampus 23: 1299– 1308. 23878012
  27. Gold AE, Kesner RP. 2005 The role of the CA3 subregion of the dorsal hippocampus in spatial pattern completion in the rat. Hippocampus 15: 808– 814. 16010664
  28. Gray R, Johnston D. 1987 Noradrenaline and beta‐adrenoreceptor agonists increase activity of voltage‐dependent calcium channels in hippocampal neurons. Nature 327: 620– 622. 2439913
  29. Guo NN, Li BM. 2007 Cellular and subcellular distributions of ß1‐and ß2adrenoreceptors in the CA1 and CA3 regions of the rat hippocampus. Neuroscience 146: 298– 305. 17337326
  30. Hagena H, Manahan‐Vaughan D. 2011 Learning‐facilitated synaptic plasticity at CA3 mossy fiber and commissural‐associational synapses reveals different roles in information processing. Cereb Cortex 21: 2442– 2449. 21493717 PMC3183418
  31. Hagena H, Manahan‐Vaughan D. 2012 Learning‐facilitated long‐term depression and long‐term potentiation at mossy fiber‐CA3 synapses requires activation of β‐adrenergic receptors. Frontiers Integr Neurosci 6: 23. PMC3358719 22654741
  32. Hansen N, Manahan‐Vaughan D. 2014 Locus coeruleus stimulation facilitates long‐term depression in the dentate gyrus that requires activation of β‐adrenergic receptors. Cereb Cortex 2014 Jan 23. (Epub ahead of print). PMID: 24464942. PMC4459289 24464942
  33. Harley C. 1991 Noradrenergic and locus coeruleus modulation of the perforant path‐evoked potential in rat dentate gyrus supports a role for the locus coeruleus in attentional and memorial processes. Prog Brain Res 88: 307– 321. 1687619
  34. Harley C, Milway JS, Lacaille JC. 1989 Locus coeruleus potentiation of dentate gyrus responses: Evidence for two systems. Brain Res Bull 22: 643– 650. 2544246
  35. Harris EW, Cotman CW. 1986 Long‐term potentiation of guinea pig mossy fiber responses is not blocked by N‐methyl D‐aspartate antagonists. Neurosci Lett 70: 132– 137. 3022192
  36. Hoang LT, Kesner RP. 2008 Dorsal hippocampus, CA3, and CA1 lesions disrupt temporal sequence completion. Behav Neurosci 122: 9– 15. 18298244
  37. Huang YY, Levine A, Kandel DB, Yin D, Colnaghi L, Drisaldi B, Kandel ER. 2014 D1/D5 receptors and histone deacetylation mediate the gateway effect of LTP in hippocampal dentate gyrus. Learn Mem 21: 153– 160. 24549570 PMC3929850
  38. Hunsaker MR, Rosenberg JS, Kesner RP. 2008 The role of the dentate gyrus, CA3a,b, and CA3c for detecting spatial and environmental novelty. Hippocampus 18: 1064– 1073. 18651615
  39. Kemp A, Manahan‐Vaughan D. 2004 Hippocampal long‐term depression and long‐term potentiation encode different aspects of novelty acquisition. Proc Natl Acad Sci USA 101: 8192– 8197. 15150407 PMC419579
  40. Kemp A, Manahan‐Vaughan D. 2007 Hippocampal long‐term depression: Master or minion in declarative memory processes?. Trends Neurosci 30: 111– 118. 17234277
  41. Kemp A, Manahan‐Vaughan D. 2008a Beta‐adrenoreceptors comprise a critical element in learning‐facilitated long‐term plasticity. Cereb Cortex 18: 1326– 1334. 17906333
  42. Kemp A, Manahan‐Vaughan D. 2008b The hippocampal CA1 region and dentate gyrus differentiate between environmental and spatial feature encoding through long‐term depression. Cereb Cortex 18: 968– 977. 17702951
  43. Kemp A, Manahan‐Vaughan D. 2012 Passive spatial perception facilitates the expression of persistent hippocampal long‐term depression. Cereb Cortex 22: 1614– 1621. 21917740 PMC3377964
  44. Kennard JT, Guévremont D, Mason‐Parker SE, Abraham WC, Williams JM. 2014 Redistribution of ionotropic glutamate receptors detected by laser microdissection of the rat dentate gyrus 48 h following LTP induction in vivo. PLoS One 9: e92972. 24667777 PMC3965487
  45. Kenney J, Manahan‐Vaughan VD. 2013 Learning‐facilitated synaptic plasticity occurs in the intermediate hippocampus in association with spatial learning. Front Synaptic Neurosci 5: 1– 7. 24194716 PMC3810593
  46. Kesner RP. 2013a A process analysis of the CA3 subregion of the hippocampus. Front Cell Neurosci 7: 1– 17. 23750126 PMC3664330
  47. Kesner RP. 2013b An analysis of the dentate gyrus function. Behav Brain Res 254: 1– 7. 23348108
  48. Kitchigina V, Vankov A, Harley C, Sara SJ. 1997 Novelty‐elicited, noradrenaline‐dependent enhancement of excitability in the dentate gyrus. Eur J Neurosci 9: 41– 47. 9042567
  49. Klukowski G, Harley CW. 1994 Locus coeruleus activation induces perforant path‐evoked population spike potentiation in the dentate gyrus of awake rat. Exp Brain Res 102: 165– 170. 7895793
  50. Lashgari R, Khakpour‐Taleghani B, Motamedi F, Shahidi S. 2008 Effects of reversible inactivation of locus coeruleus on long‐term potentiation in perforant path‐DG synapses in rats. Neurobiol Learn Mem 90: 309– 316. 18577458
  51. Lee I, Yoganarasimha D, Rao G, Knierim JJ. 2004 Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature 430: 456– 459. 15229614
  52. Lemon N, Manahan‐Vaughan D. 2006 Dopamine D1/D5 receptors gate the acquisition of novel information through hippocampal long‐term potentiation and long‐term depression. J Neurosci 26: 7723– 7729. 16855100 PMC6674280
  53. Lemon N, Manahan‐Vaughan D. 2012 Dopamine D1/D5 receptors contribute to de novo hippocampal LTD mediated by novel spatial exploration or locus coeruleus activity. Cereb Cortex 22: 2131– 2138. 22038910 PMC3412443
  54. Lemon N, Aydin‐Abidin S, Funke K, Manahan‐Vaughan D. 2009 Locus coeruleus activation facilitates memory encoding and induces hippocampal LTD that depends on beta‐adrenergic receptor activation. Cereb Cortex 19: 2827– 2837. 19435710 PMC2774396
  55. Lisman JE. 2001 Three Ca2+ levels affect plasticity differently: The LTP zone, the LTD zone and no man's land. J Physiol 532: 285. 11306649 PMC2278561
  56. Lisman JE, Otmakhova NA. 2001 Storage, recall, and novelty detection of sequences by the hippocampus: Elaborating on the SOCRATIC model to account for normal and aberrant effects of dopamine. Hippocampus 11: 551– 568. 11732708
  57. Loy R, Koziell DA, Lindsey JD, Moore RY. 1980 Noradrenergic innervation of the adult rat hippocampal formation. J Comp Neurol 189: 699– 710. 7381046
  58. Malenka RC, Nicoll RA. 1993 NMDA‐receptor‐dependent synaptic plasticity: Multiple forms and mechanisms. Trends Neurosci 16: 521– 527. 7509523
  59. 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. 2549423
  60. Manahan‐Vaughan D. 1997 Group 1 and 2 metabotropic glutamate receptors play differential roles in hippocampal long‐term depression and long‐term potentiation in freely moving rats. J Neurosci 17: 3303– 3311. 9096163 PMC6573649
  61. Manahan‐Vaughan D, Braunewell KH. 1999 Novelty acquisition is associated with induction of hippocampal long‐term depression. Proc Natl Acad Sci USA 96: 8739– 8744. 10411945 PMC17586
  62. Manahan‐Vaughan D, Reymann KG, Brown RE. 1998 In vivo electrophysiological investigations into the role of histamine in the dentate gyrus of the rat. Neuroscience 84: 783– 90. 9579783
  63. Manahan‐Vaughan D, Kulla A. 2003 Regulation of depotentiation and long‐term potentiation in the dentate gyrus of freely moving rats by dopamine D2‐like receptors. Cereb Cortex 13: 123‐1 35. 12507943
  64. McNaughton BL, Barnes A. 1977 Physiological identification and analysis of dentate granule cell responses to stimulation of the medial and lateral perforant pathways in the rat. J Comp Neurol 175: 439– 454. 915033
  65. Mello‐Carpes PB, Izquierdo I. 2013 The nucleus of the solitary tract → nucleus paragigantocellularis → locus coeruleus → CA1 region of dorsal hippocampus pathway is important for consolidation of object recognition memory. Neurobiol Learn Mem 100: 56– 63. 23246466
  66. Milner TA, Shah P, Pierce JP. 2000 Beta‐adrenergic receptors primarily are located on the dendrites of granule cells and interneurons but also are found on astrocytes and a few presynaptic profiles in the rat dentate gyrus. Synapse 36: 178– 193. 10819898
  67. Munro CA, Walling SG, Evans JH, Harley CW. 2001 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 11: 322– 328. 11769313
  68. Nabavi S, Fox R, Proulx CD, Lin JY, Tsien RY, Malinow R. 2014 Engineering a memory with LTD and LTP. Nature 511: 348‐3 52. 24896183 PMC4210354
  69. Nakashiba T, Cushman JD, Pelkey KA, Renaudineau S, Buhl DL, McHugh TJ, Rodriguez Barrera V, Chittajallu R, Iwamoto KS, McBain CJ, Fanselow MS, Tonegawa S. 2012 Young dentate granule cells mediate pattern separation, whereas old granule cells facilitate pattern completion. Cell 149: 188– 201. 22365813 PMC3319279
  70. Neunuebel JP, Knierim JJ. 2014 CA3 retrieves coherent representations from degraded input: Direct evidence for CA3 pattern completion and dentate gyrus pattern separation. Neuron 81: 416– 427. 24462102 PMC3904133
  71. O'Dell TJ, Connor SA, Gelinas JN, Nguyen PV. 2010 Viagra for your synapses: Enhancement of hippocampal long‐term potentiation by activation of beta‐adrenergic receptors. Cell Signal 22: 728– 736. 20043991 PMC2826554
  72. Paxinos G, Watson C. 1998 The Rat Brain in Stereotaxic Coordinates, 4th ed New York: Aacademic Press.
  73. Popkirov SG, Manahan‐Vaughan D. 2011 Involvement of the metabotropic glutamate receptor mGluR5 in NMDA receptor‐dependent, learning‐facilitated long‐term depression in CA1 synapses. Cereb Cortex 21: 501– 509. 20525770 PMC3041006
  74. Penley SC, Hinman JR, Long LL, Markus EJ, Escabí MA, Chrobak JJ. 2013 Novel space alters theta and gamma synchrony across the longitudinal axis of the hippocampus. Front Syst Neurosci 7: 20‐ 23805081 PMC3691506
  75. Rajkumar R, Suri S, Deng M, Dawe HGS. 2013 Nicotine and clozapine cross‐prime the locus coeruleus noradrenergic system to induce long‐lasting potentiation in the rat hippocampus. 23: 616– 624. 23520012
  76. Raman IM, Tong G, Jahr CE. 1996 Beta‐adrenergic regulation of synaptic NMDA receptors by cAMP‐dependent protein kinase. Neuron 16: 415– 21. 8789956
  77. Reid AT, Harley CW. 2010 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. 19644680
  78. Rolls ET. 2010 A computational theory of episodic memory formation in the hippocampus. Behav Brain Res 215: 180– 196. 20307583
  79. Sara SJ, Bouret S. 2012 Orienting and reorienting: The locus coeruleus mediates cognition through arousal. Neuron 76: 130– 141. 23040811
  80. Sara SJ, Vankov A, Hervé A. 1994 Locus coeruleus‐evoked responses in behaving rats: A clue to the role of noradrenaline in memory. Brain Res Bull 35: 457– 465. 7859103
  81. Segal SK, Stark SM, Kattan D, Stark CE, Yassa MA. 2012 Norepinephrine‐mediated emotional arousal facilitates subsequent pattern separation. Neurobiol Learn Mem 97: 465– 469. 22498686 PMC3517207
  82. Smith CC, Greene RW. 2012 CNS dopamine transmission mediated by noradrenergic innervation. J Neurosci 32: 6072‐60 80. 22553014 PMC3371362
  83. Stanton PK, Sarvey JM. 1985 Blockade of norepinephrine‐induced long‐lasting potentiation in the hippocampal dentate gyrus by an inhibitor of protein synthesis. Brain Res 361: 276– 283. 4084800
  84. Stanton PK, Mody I, Heinemann U. 1989 A role for N‐methyl‐d‐aspartate receptors in norepinephrine‐induced long‐lasting potentiation in the dentate gyrus. Exp Brain Res 77: 517– 530. 2572445
  85. Straube T, Frey JU. 2003 Involvement of beta‐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. 12770561
  86. Straube T, Korz V, Balschun D, Frey JU. 2003 Requirement of beta‐adrenergic receptor activation and protein synthesis for LTP‐reinforcement by novelty in rat dentate gyrus. J Physiol 552: 953– 960. 12937286 PMC2343450
  87. Tenorio G, Connor SA, Guévremont D, Abraham WC, Williams J, O'Dell TJ, Nguyen PV. 2010 “silent” priming of translation‐dependent LTP by ß‐adrenergic receptors involves phosphorylation and recruitment of AMPA receptors. Learn Mem 17: 627– 638. 21097606 PMC2998333
  88. Tully K, Bolshakov VY. 2010 Emotional enhancement of memory: How norepinephrine enables synaptic plasticity. Mol Brain 3: 15. 20465834 PMC2877027
  89. Uzakov S, Frey JU, Korz V. 2005 Reinforcement of rat hippocampal LTP by holeboard training. Learn Mem 12: 165– 171. 15774946 PMC1074335
  90. Vankov A, Hervé‐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. 7582091
  91. Vianna MR, Alonso M, Viola H, Quevedo J, de PF, Furman M, de Stein ML Medina JH, Izquierdo. 2000 Role of hippocampal signalling pathways in long‐term memory formation of a nonassociative learning task in the rat. Learn Mem 7: 333– 340. PMC311352 11040265
  92. 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 beta‐adrenergic‐ and protein synthesis‐dependent mammalian plasticity mechanism. J Neurosci 24: 598– 604. 14736844 PMC6729256
  93. 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. 15329388 PMC6729640
  94. Yavich L, Jäkälä P, Tanila H. 2005 Noradrenaline overflow in mouse dentate gyrus following locus coeruleus and natural stimulation: Real‐time monitoring by in vivo voltammetry. J Neurochem 95: 641– 650. 16248883

Authors
Hansen, N., & Manahan‐Vaughan, D.
Affiliations
Ruhr University Bochum (DE)
Corresponding author
Manahan‐Vaughan, Denise
ORCID
Venue
Hippocampus
Publisher
Wiley
Published
2015-04-02
Volume
25
Issue
11
Pages
1285-1298
ISSN
  • 1050-9631 (ISSN-L)
  • 1098-1063
DOI
10.1002/hipo.22436
PMC
PMC6680149
OpenAlex
W1487826806
Cited by
92
References
100
Citations by year
2026: 6 · 2025: 11 · 2024: 9 · 2023: 9 · 2022: 11 · 2021: 9 · 2020: 6 · 2019: 3 · 2018: 9 · 2017: 10 · 2016: 8 · 2015: 1
FWCI
4.35
Type
journal article
Language
en
Open access
Licence
Locations
  • Hippocampus (publishedVersion, cc-by-nc-nd)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
Funders
German Research Foundation (MA1843/6-1)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
Keywords
hippocampal long-term potentiation, beta-adrenergic receptors, locus coeruleus, norepinephrine, perforant path stimulation, spatial learning, long-term depression, depotentiation, synaptic plasticity, dentate gyrus, novelty detection, beta-adrenoceptor antagonism
MeSH terms
Adrenergic beta-Agonists, Adrenergic beta-Antagonists, Animals, Behavior, Animal, Evoked Potentials, Hippocampus, Isoproterenol, Locus Coeruleus, Male, Propranolol, Receptors, Adrenergic, beta, Rats, Wistar, Long-Term Potentiation, Perforant Pathway, Long-Term Synaptic Depression, Rats, Spatial Learning

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