Home LiteratureArticle Details
PMID: 18372288 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Locus coeruleus alpha-adrenergic-mediated activation of cortical astrocytes in vivo.

Cerebral cortex (New York, N.Y. : 1991) ·Vol. 18 ·No. 12 ·2008-12-00 ·Pages 2789-95

Bekar LK, He W, Nedergaard M

Abstract

The locus coeruleus (LC) provides the sole source of norepinephrine (NE) to the cortex for modulation of cortical synaptic activity in response to salient sensory information. NE has been shown to improve signal-to-noise ratios, sharpen receptive fields and function in learning, memory, and cognitive performance. Although LC-mediated effects on neurons have been addressed, involvement of astrocytes has thus far not been demonstrated in these neuromodulatory functions. Here we show for the 1st time in live mice, that astrocytes exhibit rapid Ca(2+) increases in response to electrical stimulation of the LC. Additionally, robust peripheral stimulation known to result in phasic LC activity leads to Ca(2+) responses in astrocytes throughout sensory cortex that are independent of sensory-driven glutamate-dependent pathways. Furthermore, the astrocytic Ca(2+) transients are competitively modulated by alpha(2)-specific agonist/antagonist combinations known to impact LC output, are sensitive to the LC-specific neurotoxin N-(2-chloroethyl)-N-ethyl-2-bromobenzylamine, and are inhibited locally by an alpha-adrenergic antagonist. Future investigations of LC function must therefore consider the possibility that LC neuromodulatory effects are in part derived from activation of astrocytes.

MeSH Terms
Animals Astrocytes/physiology Calcium/physiology Cerebral Cortex/physiology Electric Stimulation Isoflurane Locus Coeruleus/physiology Male Mice Mice, Inbred Strains Neurons/physiology Receptors, Adrenergic, alpha/physiology Receptors, Metabotropic Glutamate/physiology Sensory Receptor Cells/physiology Sensory Thresholds/physiology Somatosensory Cortex/physiology
Chemicals
Receptors, Adrenergic, alpha Receptors, Metabotropic Glutamate Isoflurane Calcium
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Bekar Lane K
Division of Glial Disease and Therapeutics, Department of Neurosurgery, University of Rochester, Rochester, NY 14642, USA.
He Wei
Nedergaard Maiken
References (44)
44 references, click to expand
  1. Neurone-to-astrocyte signalling in the brain represents a distinct multifunctional unit.
    J Physiol. 2004 Aug 15;559(Pt 1):3-15 PMID: 15218071
  2. Role of thalamocortical sensory suppression during arousal: focusing sensory inputs in neocortex.
    J Neurosci. 2002 Nov 15;22(22):9651-5 PMID: 12427819
  3. Sulforhodamine 101 as a specific marker of astroglia in the neocortex in vivo.
    Nat Methods. 2004 Oct;1(1):31-7 PMID: 15782150
  4. Glycogen is a preferred glutamate precursor during learning in 1-day-old chick: biochemical and behavioral evidence.
    J Neurosci Res. 2007 Nov 15;85(15):3326-33 PMID: 17455305
  5. Norepinephrine exhibits two distinct profiles of action on sensory cortical neuron responses to excitatory synaptic stimuli.
    Synapse. 2000 Sep 15;37(4):273-82 PMID: 10891864
  6. Astrocytic purinergic signaling coordinates synaptic networks.
    Science. 2005 Oct 7;310(5745):113-6 PMID: 16210541
  7. Noradrenergic innervation of the developing and mature visual and motor cortex of the rat brain: a light and electron microscopic immunocytochemical analysis.
    J Comp Neurol. 2002 Apr 1;445(2):145-58 PMID: 11891659
  8. Norepinephrine triggers release of glial ATP to increase postsynaptic efficacy.
    Nat Neurosci. 2005 Aug;8(8):1078-86 PMID: 15995701
  9. Noradrenaline neuron innervation of the neocortex in the rat.
    Brain Res. 1978 Jan 13;139(2):219-31 PMID: 624057
  10. Noradrenergic activation amplifies bottom-up and top-down signal-to-noise ratios in sensory thalamus.
    J Neurosci. 2006 Apr 19;26(16):4426-36 PMID: 16624962
  11. Role of pertussis toxin-sensitive G-proteins in the analgesic and anesthetic actions of alpha 2-adrenergic agonists in the rat.
    Anesthesiology. 1995 Oct;83(4):816-22 PMID: 7574062
  12. Adrenergic calcium signaling in astrocyte networks within the hippocampal slice.
    J Neurosci. 1995 Aug;15(8):5535-50 PMID: 7643199
  13. Electrical stimulation of locus coeruleus strengthens the surround inhibition in layer V barrel cortex in rat.
    Neurosci Lett. 2006 Jul 3;401(3):280-4 PMID: 16600499
  14. Neuronal activity triggers calcium waves in hippocampal astrocyte networks.
    Neuron. 1992 Mar;8(3):429-40 PMID: 1347996
  15. GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression.
    J Neurosci. 2006 May 17;26(20):5370-82 PMID: 16707789
  16. The interaction of the beta-haloethyl benzylamines, xylamine, and DSP-4 with catecholaminergic neurons.
    Annu Rev Pharmacol Toxicol. 1990;30:387-403 PMID: 2188573
  17. Astrocyte-mediated potentiation of inhibitory synaptic transmission.
    Nat Neurosci. 1998 Dec;1(8):683-92 PMID: 10196584
  18. Inhibition of glycogenolysis in astrocytes interrupts memory consolidation in young chickens.
    Glia. 2006 Aug 15;54(3):214-22 PMID: 16819764
  19. Calcium dynamics of cortical astrocytic networks in vivo.
    PLoS Biol. 2004 Apr;2(4):E96 PMID: 15094801
  20. Astrocytes, from brain glue to communication elements: the revolution continues.
    Nat Rev Neurosci. 2005 Aug;6(8):626-40 PMID: 16025096
  21. Muscarinic acetylcholine receptor knockout mice show distinct synaptic plasticity impairments in the visual cortex.
    J Physiol. 2006 Dec 15;577(Pt 3):829-40 PMID: 17023506
  22. Heterosynaptic facilitation of in vivo thalamocortical long-term potentiation in the adult rat visual cortex by acetylcholine.
    Cereb Cortex. 2007 Apr;17(4):839-48 PMID: 16707735
  23. The locus coeruleus-noradrenergic system: modulation of behavioral state and state-dependent cognitive processes.
    Brain Res Brain Res Rev. 2003 Apr;42(1):33-84 PMID: 12668290
  24. Dexmedetomidine injection into the locus ceruleus produces antinociception.
    Anesthesiology. 1996 Apr;84(4):873-81 PMID: 8638842
  25. Properties of synaptically evoked astrocyte calcium signal reveal synaptic information processing by astrocytes.
    J Neurosci. 2005 Mar 2;25(9):2192-203 PMID: 15745945
  26. Glia-derived D-serine controls NMDA receptor activity and synaptic memory.
    Cell. 2006 May 19;125(4):775-84 PMID: 16713567
  27. Modulation of long-term synaptic depression in visual cortex by acetylcholine and norepinephrine.
    J Neurosci. 1999 Mar 1;19(5):1599-609 PMID: 10024347
  28. Are glial cells targets of the central noradrenergic system? A review of the evidence.
    Brain Res Brain Res Rev. 1989 Oct-Dec;14(4):297-309 PMID: 2560410
  29. A novel long-latency response of locus coeruleus neurons to noxious stimuli: mediation by peripheral C-fibers.
    J Neurophysiol. 1994 May;71(5):1752-61 PMID: 8064346
  30. Astrocytic adrenoceptors: a major drug target in neurological and psychiatric disorders?
    Curr Drug Targets CNS Neurol Disord. 2004 Jun;3(3):239-67 PMID: 15180484
  31. Decision making, the P3, and the locus coeruleus-norepinephrine system.
    Psychol Bull. 2005 Jul;131(4):510-32 PMID: 16060800
  32. High-frequency stimulation together with adrenoceptor activation facilitates the maintenance of long-term potentiation at visual cortical inhibitory synapses.
    Cereb Cortex. 2006 Sep;16(9):1239-48 PMID: 16251503
  33. Connexins regulate calcium signaling by controlling ATP release.
    Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15735-40 PMID: 9861039
  34. Astrocytic Ca2+ signaling evoked by sensory stimulation in vivo.
    Nat Neurosci. 2006 Jun;9(6):816-23 PMID: 16699507
  35. Cellular and subcellular sites for noradrenergic action in the monkey dorsolateral prefrontal cortex as revealed by the immunocytochemical localization of noradrenergic receptors and axons.
    Cereb Cortex. 1998 Apr-May;8(3):269-77 PMID: 9617922
  36. New roles for astrocytes: redefining the functional architecture of the brain.
    Trends Neurosci. 2003 Oct;26(10):523-30 PMID: 14522144
  37. Unilateral hindpaw inflammation induces bilateral activation of the locus coeruleus and the nucleus subcoeruleus in the rat.
    Brain Res Bull. 2003 Jul 15;61(2):117-23 PMID: 12831996
  38. Ultrastructural relationships between noradrenergic nerve fibers and non-neuronal elements in the rat cerebral cortex.
    Glia. 1996 Jun;17(2):133-46 PMID: 8776580
  39. Neuron-to-astrocyte signaling is central to the dynamic control of brain microcirculation.
    Nat Neurosci. 2003 Jan;6(1):43-50 PMID: 12469126
  40. GLIA: listening and talking to the synapse.
    Nat Rev Neurosci. 2001 Mar;2(3):185-93 PMID: 11256079
  41. An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance.
    Annu Rev Neurosci. 2005;28:403-50 PMID: 16022602
  42. Beta-adrenergic receptors: astrocytic localization in the adult visual cortex and their relation to catecholamine axon terminals as revealed by electron microscopic immunocytochemistry.
    J Neurosci. 1992 Mar;12(3):781-92 PMID: 1347560
  43. Intercellular calcium signaling mediated by point-source burst release of ATP.
    Proc Natl Acad Sci U S A. 2002 Jul 23;99(15):9840-5 PMID: 12097649
  44. Astroglial and vascular interactions of noradrenaline terminals in the rat cerebral cortex.
    J Cereb Blood Flow Metab. 1997 Aug;17(8):894-904 PMID: 9290587
Article Info
Journal
Cerebral cortex (New York, N.Y. : 1991)
Abbr.
Cereb Cortex
ISSN
1460-2199
Published
2008-12-00
Epub
2008-00-27
Pages
2789-95
Language
English
Region
United States
NLM ID
9110718
PMCID
PMC2583159
Subset
IM
Grants
NINDS NIH HHS · NS30007 · United States
NINDS NIH HHS · NS38073 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com