 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
Previous Article | Next Article
Volume 16, Number 16, Issue of August 15, 1996 pp. 5073-5081
Copyright ©1996 Society for NeuroscienceHippocampal Astrocytes In Situ Respond to Glutamate Released from Synaptic Terminals
Received Feb. 22, 1996; revised May 20, 1996; accepted May 30, 1996.
James T. Porter and Ken D. McCarthy Department of Pharmacology, University of North Carolina School of Medicine, Chapel Hill, North Carolina 27599
A long-standing question in neurobiology is whether astrocytes respond to the neuronal release of neurotransmitters in vivo. To address this question, acutely isolated hippocampal slices were loaded with the calcium-sensitive dye Calcium Green-1 and the responses of the astrocytes to electrical stimulation of the Schaffer collaterals were monitored by confocal microscopy. To confirm that the responsive cells were astrocytes, the slices were immunostained for the astrocytic marker glial fibrillary acidic protein. Stimulation of the Schaffer collaterals (50 Hz, 2 sec) resulted in increases in the concentration of intracellular calcium ([Ca2+]i) in the astrocytes located in the stratum radiatum of CA1. The astrocytic responses were blocked by the sodium channel blocker tetrodotoxin, the voltage-dependent calcium channel blocker
-conotoxin-MVIIC, and the selective metabotropic glutamate receptor antagonist
-methyl-4-carboxyphenylglycine (MCPG). These results suggest that the astrocytic responses were induced by stimulation of metabotropic glutamate receptors on the astrocytes by neuronally released glutamate. The astrocytic responses to neuronal stimulation were enhanced in the presence of the K+ channel antagonist 4-aminopyridine (4-AP). Inhibition of the astrocytic responses in the presence of 4-AP required the presence of both MCPG and the ionotropic glutamate receptor antagonist kynurenic acid. These results suggest that higher levels of neuronal activity result in stimulation of both metabotropic and ionotropic glutamate receptors on the astrocytes. Overall, the results indicate that hippocampal astrocytes in situ are able to respond to the neuronal release of the neurotransmitter glutamate with increases in [Ca2+]i.
Key words: hippocampus; astrocytes; in situ; intracellular calcium; metabotropic glutamate receptors; ionotropic glutamate receptors; CA1; stratum radiatum; neural-glial interactions
This article has been cited by other articles:
M. Doengi, D. Hirnet, P. Coulon, H.-C. Pape, J. W. Deitmer, and C. Lohr
GABA uptake-dependent Ca2+ signaling in developing olfactory bulb astrocytes
PNAS, October 13, 2009; 106(41): 17570 - 17575.
[Abstract] [Full Text] [PDF]
Z. L. Kurth-Nelson, A. Mishra, and E. A. Newman
Spontaneous Glial Calcium Waves in the Retina Develop over Early Adulthood
J. Neurosci., September 9, 2009; 29(36): 11339 - 11346.
[Abstract] [Full Text] [PDF]
A. Nimmerjahn
Astrocytes going live: advances and challenges
J. Physiol., April 15, 2009; 587(8): 1639 - 1647.
[Abstract] [Full Text] [PDF]
E. Shigetomi, D. N. Bowser, M. V. Sofroniew, and B. S. Khakh
Two Forms of Astrocyte Calcium Excitability Have Distinct Effects on NMDA Receptor-Mediated Slow Inward Currents in Pyramidal Neurons
J. Neurosci., June 25, 2008; 28(26): 6659 - 6663.
[Abstract] [Full Text] [PDF]
J. Schummers, H. Yu, and M. Sur
Tuned Responses of Astrocytes and Their Influence on Hemodynamic Signals in the Visual Cortex
Science, June 20, 2008; 320(5883): 1638 - 1643.
[Abstract] [Full Text] [PDF]
J. Petravicz, T. A. Fiacco, and K. D. McCarthy
Loss of IP3 Receptor-Dependent Ca2+ Increases in Hippocampal Astrocytes Does Not Affect Baseline CA1 Pyramidal Neuron Synaptic Activity
J. Neurosci., May 7, 2008; 28(19): 4967 - 4973.
[Abstract] [Full Text] [PDF]
M. Andersson, F. Blomstrand, and E. Hanse
Astrocytes play a critical role in transient heterosynaptic depression in the rat hippocampal CA1 region
J. Physiol., December 15, 2007; 585(3): 843 - 852.
[Abstract] [Full Text] [PDF]
K. K. Murai and D. J. Van Meyel
Neuron Glial Communication at Synapses: Insights From Vertebrates and Invertebrates
Neuroscientist, December 1, 2007; 13(6): 657 - 666.
[Abstract] [PDF]
W. S. C. Ho and A. N. van den Pol
Bystander Attenuation of Neuronal and Astrocyte Intercellular Communication by Murine Cytomegalovirus Infection of Glia
J. Virol., July 1, 2007; 81(13): 7286 - 7292.
[Abstract] [Full Text] [PDF]
I. R. Winship, N. Plaa, and T. H. Murphy
Rapid Astrocyte Calcium Signals Correlate with Neuronal Activity and Onset of the Hemodynamic Response In Vivo
J. Neurosci., June 6, 2007; 27(23): 6268 - 6272.
[Abstract] [Full Text] [PDF]
D. N. Bowser and B. S. Khakh
Vesicular ATP Is the Predominant Cause of Intercellular Calcium Waves in Astrocytes
J. Gen. Physiol., June 1, 2007; 129(6): 485 - 491.
[Abstract] [Full Text] [PDF]
R. Piet and C. E. Jahr
Glutamatergic and Purinergic Receptor-Mediated Calcium Transients in Bergmann Glial Cells
J. Neurosci., April 11, 2007; 27(15): 4027 - 4035.
[Abstract] [Full Text] [PDF]
G. Burnstock
Physiology and Pathophysiology of Purinergic Neurotransmission
Physiol Rev, April 1, 2007; 87(2): 659 - 797.
[Abstract] [Full Text] [PDF]
E. J. Sweger, K. B. Casper, K. Scearce-Levie, B. R. Conklin, and K. D. McCarthy
Development of Hydrocephalus in Mice Expressing the Gi-Coupled GPCR Ro1 RASSL Receptor in Astrocytes
J. Neurosci., February 28, 2007; 27(9): 2309 - 2317.
[Abstract] [Full Text] [PDF]
T. Fellin, M. Gomez-Gonzalo, S. Gobbo, G. Carmignoto, and P. G. Haydon
Astrocytic Glutamate Is Not Necessary for the Generation of Epileptiform Neuronal Activity in Hippocampal Slices
J. Neurosci., September 6, 2006; 26(36): 9312 - 9322.
[Abstract] [Full Text] [PDF]
P. G. Haydon and G. Carmignoto
Astrocyte control of synaptic transmission and neurovascular coupling.
Physiol Rev, July 1, 2006; 86(3): 1009 - 1031.
[Abstract] [Full Text] [PDF]
M. Beierlein and W. G. Regehr
Brief bursts of parallel fiber activity trigger calcium signals in bergmann glia.
J. Neurosci., June 28, 2006; 26(26): 6958 - 6967.
[Abstract] [Full Text] [PDF]
A. Serrano, N. Haddjeri, J.-C. Lacaille, and R. Robitaille
GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression.
J. Neurosci., May 17, 2006; 26(20): 5370 - 5382.
[Abstract] [Full Text] [PDF]
R. Zur Nieden and J. W. Deitmer
The Role of Metabotropic Glutamate Receptors for the Generation of Calcium Oscillations in Rat Hippocampal Astrocytes In Situ
Cereb Cortex, May 1, 2006; 16(5): 676 - 687.
[Abstract] [Full Text] [PDF]
D. Crippa, U. Schenk, M. Francolini, P. Rosa, C. Verderio, M. Zonta, T. Pozzan, M. Matteoli, and G. Carmignoto
Synaptobrevin2-expressing vesicles in rat astrocytes: insights into molecular characterization, dynamics and exocytosis
J. Physiol., February 1, 2006; 570(3): 567 - 582.
[Abstract] [Full Text] [PDF]
D. Rossi, L. Brambilla, C. F. Valori, A. Crugnola, G. Giaccone, R. Capobianco, M. Mangieri, A. E. Kingston, A. Bloc, P. Bezzi, et al.
Defective Tumor Necrosis Factor-{alpha}-dependent Control of Astrocyte Glutamate Release in a Transgenic Mouse Model of Alzheimer Disease
J. Biol. Chem., December 23, 2005; 280(51): 42088 - 42096.
[Abstract] [Full Text] [PDF]
O. Pascual, K. B. Casper, C. Kubera, J. Zhang, R. Revilla-Sanchez, J.-Y. Sul, H. Takano, S. J. Moss, K. McCarthy, and P. G. Haydon
Astrocytic Purinergic Signaling Coordinates Synaptic Networks
Science, October 7, 2005; 310(5745): 113 - 116.
[Abstract] [Full Text] [PDF]
K. Matsui, C. E. Jahr, and M. E. Rubio
High-Concentration Rapid Transients of Glutamate Mediate Neural-Glial Communication via Ectopic Release
J. Neurosci., August 17, 2005; 25(33): 7538 - 7547.
[Abstract] [Full Text] [PDF]
E. A. Newman
Calcium Increases in Retinal Glial Cells Evoked by Light-Induced Neuronal Activity
J. Neurosci., June 8, 2005; 25(23): 5502 - 5510.
[Abstract] [Full Text] [PDF]
G. Perea and A. Araque
Properties of Synaptically Evoked Astrocyte Calcium Signal Reveal Synaptic Information Processing by Astrocytes
J. Neurosci., March 2, 2005; 25(9): 2192 - 2203.
[Abstract] [Full Text] [PDF]
D. N. Bowser and B. S. Khakh
ATP Excites Interneurons and Astrocytes to Increase Synaptic Inhibition in Neuronal Networks
J. Neurosci., September 29, 2004; 24(39): 8606 - 8620.
[Abstract] [Full Text] [PDF]
T. Fellin and G. Carmignoto
Neurone-to-astrocyte signalling in the brain represents a distinct multifunctional unit
J. Physiol., August 15, 2004; 559(1): 3 - 15.
[Abstract] [Full Text] [PDF]
M. C. Angulo, A. S. Kozlov, S. Charpak, and E. Audinat
Glutamate Released from Glial Cells Synchronizes Neuronal Activity in the Hippocampus
J. Neurosci., August 4, 2004; 24(31): 6920 - 6927.
[Abstract] [Full Text] [PDF]
M. Frerking
When astrocytes signal, kainate receptors respond
PNAS, March 2, 2004; 101(9): 2649 - 2650.
[Full Text] [PDF]
Q.-s. Liu, Q. Xu, G. Arcuino, J. Kang, and M. Nedergaard
From The Cover: Astrocyte-mediated activation of neuronal kainate receptors
PNAS, March 2, 2004; 101(9): 3172 - 3177.
[Abstract] [Full Text] [PDF]
G. Seifert, K. Huttmann, J. Schramm, and C. Steinhauser
Enhanced Relative Expression of Glutamate Receptor 1 Flip AMPA Receptor Subunits in Hippocampal Astrocytes of Epilepsy Patients with Ammon's Horn Sclerosis
J. Neurosci., February 25, 2004; 24(8): 1996 - 2003.
[Abstract] [Full Text] [PDF]
K. J. Todd, C. A. B. Slatter, and D. W. Ali
Activation of Ionotropic Glutamate Receptors on Peripheral Axons of Primary Motoneurons Mediates Transmitter Release at the Zebrafish NMJ
J Neurophysiol, February 1, 2004; 91(2): 828 - 840.
[Abstract] [Full Text] [PDF]
M. Zonta, A. Sebelin, S. Gobbo, T. Fellin, T. Pozzan, and G. Carmignoto
Glutamate-mediated cytosolic calcium oscillations regulate a pulsatile prostaglandin release from cultured rat astrocytes
J. Physiol., December 1, 2003; 553(2): 407 - 414.
[Abstract] [Full Text] [PDF]
M. Morita, C. Higuchi, T. Moto, N. Kozuka, J. Susuki, R. Itofusa, J. Yamashita, and Y. Kudo
Dual Regulation of Calcium Oscillation in Astrocytes by Growth Factors and Pro-Inflammatory Cytokines via the Mitogen-Activated Protein Kinase Cascade
J. Neurosci., November 26, 2003; 23(34): 10944 - 10952.
[Abstract] [Full Text] [PDF]
N. Li, J.-Y. Sul, and P. G. Haydon
A Calcium-Induced Calcium Influx Factor, Nitric Oxide, Modulates the Refilling of Calcium Stores in Astrocytes
J. Neurosci., November 12, 2003; 23(32): 10302 - 10310.
[Abstract] [Full Text] [PDF]
C. Krebs, H. B. Fernandes, C. Sheldon, L. A. Raymond, and K. G. Baimbridge
Functional NMDA Receptor Subtype 2B Is Expressed in Astrocytes after Ischemia In Vivo and Anoxia In Vitro
J. Neurosci., April 15, 2003; 23(8): 3364 - 3372.
[Abstract] [Full Text] [PDF]
X. Hou, F. Gobeil Jr., A. M. Marrache, C. Quiniou, S. Brault, D. Checchin, S. G. Bernier, F. Sennlaub, J.-S. Joyal, D. Abran, et al.
Increased platelet-activating factor-induced periventricular brain microvascular constriction associated with immaturity
Am J Physiol Regulatory Integrative Comp Physiol, April 1, 2003; 284(4): R928 - R935.
[Abstract] [Full Text] [PDF]
E. HANSSON and L. RONNBACK
Glial neuronal signaling in the central nervous system
FASEB J, March 1, 2003; 17(3): 341 - 348.
[Abstract] [Full Text] [PDF]
E. A. Newman
Glial Cell Inhibition of Neurons by Release of ATP
J. Neurosci., March 1, 2003; 23(5): 1659 - 1666.
[Abstract] [Full Text] [PDF]
K. Matthias, F. Kirchhoff, G. Seifert, K. Huttmann, M. Matyash, H. Kettenmann, and C. Steinhauser
Segregated Expression of AMPA-Type Glutamate Receptors and Glutamate Transporters Defines Distinct Astrocyte Populations in the Mouse Hippocampus
J. Neurosci., March 1, 2003; 23(5): 1750 - 1758.
[Abstract] [Full Text] [PDF]
F. Aguado, J. F. Espinosa-Parrilla, M. A. Carmona, and E. Soriano
Neuronal Activity Regulates Correlated Network Properties of Spontaneous Calcium Transients in Astrocytes In Situ
J. Neurosci., November 1, 2002; 22(21): 9430 - 9444.
[Abstract] [Full Text] [PDF]
R. D. Fields and B. Stevens-Graham
NEUROSCIENCE: New Insights into Neuron-Glia Communication
Science, October 18, 2002; 298(5593): 556 - 562.
[Abstract] [Full Text] [PDF]
A. Araque, E. D. Martin, G. Perea, J. I. Arellano, and W. Buno
Synaptically Released Acetylcholine Evokes Ca2+ Elevations in Astrocytes in Hippocampal Slices
J. Neurosci., April 1, 2002; 22(7): 2443 - 2450.
[Abstract] [Full Text] [PDF]
H. Nishiyama, T. Knopfel, S. Endo, and S. Itohara
Glial protein S100B modulates long-term neuronal synaptic plasticity
PNAS, March 19, 2002; 99(6): 4037 - 4042.
[Abstract] [Full Text] [PDF]
W. J. Nett, S. H. Oloff, and K. D. McCarthy
Hippocampal Astrocytes In Situ Exhibit Calcium Oscillations That Occur Independent of Neuronal Activity
J Neurophysiol, January 1, 2002; 87(1): 528 - 537.
[Abstract] [Full Text] [PDF]
H. Muyderman, M. Angehagen, M. Sandberg, U. Bjorklund, T. Olsson, E. Hansson, and M. Nilsson
alpha 1-Adrenergic Modulation of Metabotropic Glutamate Receptor-induced Calcium Oscillations and Glutamate Release in Astrocytes
J. Biol. Chem., November 30, 2001; 276(49): 46504 - 46514.
[Abstract] [Full Text] [PDF]
M. Zhou and H. K. Kimelberg
Freshly Isolated Hippocampal CA1 Astrocytes Comprise Two Populations Differing in Glutamate Transporter and AMPA Receptor Expression
J. Neurosci., October 15, 2001; 21(20): 7901 - 7908.
[Abstract] [Full Text] [PDF]
M. Mazzanti, J.-Y. Sul, and P. G. Haydon
Book Review: Glutamate on Demand: Astrocytes as a Ready Source
Neuroscientist, October 1, 2001; 7(5): 396 - 405.
[Abstract] [PDF]
S. Vesce, P. Bezzi, and A. Volterra
Synaptic Transmission with the Glia
Physiology, August 1, 2001; 16(4): 178 - 184.
[Abstract] [Full Text] [PDF]
X. Hou, L. J. Roberts II, D. F. Taber, J. D. Morrow, K. Kanai, F. Gobeil Jr., M. H. Beauchamp, S. G. Bernier, G. Lepage, D. R. Varma, et al.
2,3-Dinor-5,6-dihydro-15-F2t-isoprostane: a bioactive prostanoid metabolite
Am J Physiol Regulatory Integrative Comp Physiol, August 1, 2001; 281(2): R391 - R400.
[Abstract] [Full Text] [PDF]
K. Nagler, D. H Mauch, and F. W Pfrieger
Glia-derived signals induce synapse formation in neurones of the rat central nervous system
J. Physiol., June 15, 2001; 533(3): 665 - 679.
[Abstract] [Full Text] [PDF]
D. Rochon, I. Rousse, and R. Robitaille
Synapse-Glia Interactions at the Mammalian Neuromuscular Junction
J. Neurosci., June 1, 2001; 21(11): 3819 - 3829.
[Abstract] [Full Text] [PDF]
Y. Li, L. A. Holtzclaw, and J. T. Russell
Muller Cell Ca2+ Waves Evoked by Purinergic Receptor Agonists in Slices of Rat Retina
J Neurophysiol, February 1, 2001; 85(2): 986 - 994.
[Abstract] [Full Text] [PDF]
L. Pasti, M. Zonta, T. Pozzan, S. Vicini, and G. Carmignoto
Cytosolic Calcium Oscillations in Astrocytes May Regulate Exocytotic Release of Glutamate
J. Neurosci., January 15, 2001; 21(2): 477 - 484.
[Abstract] [Full Text] [PDF]
O. Blondel, C. Collin, W. J. McCarran, S. Zhu, R. Zamostiano, I. Gozes, D. E. Brenneman, and R. D. G. McKay
A Glia-Derived Signal Regulating Neuronal Differentiation
J. Neurosci., November 1, 2000; 20(21): 8012 - 8020.
[Abstract] [Full Text] [PDF]
V. Parpura and P. G. Haydon
From the Cover: Physiological astrocytic calcium levels stimulate glutamate release to modulate adjacent neurons
PNAS, July 18, 2000; 97(15): 8629 - 8634.
[Abstract] [Full Text] [PDF]
N. J. Willmott, K. Wong, and A. J. Strong
A Fundamental Role for the Nitric Oxide-G-Kinase Signaling Pathway in Mediating Intercellular Ca2+ Waves in Glia
J. Neurosci., March 1, 2000; 20(5): 1767 - 1779.
[Abstract] [Full Text] [PDF]
B. Innocenti, V. Parpura, and P. G. Haydon
Imaging Extracellular Waves of Glutamate during Calcium Signaling in Cultured Astrocytes
J. Neurosci., March 1, 2000; 20(5): 1800 - 1808.
[Abstract] [Full Text] [PDF]
X. Hou, F. Gobeil Jr, K. Peri, G. Speranza, A. M. Marrache, P. Lachapelle, J. Roberts II, D. R. Varma, S. Chemtob, and E. F. Ellis
Augmented Vasoconstriction and Thromboxane Formation by 15-F2t-Isoprostane (8-Iso-Prostaglandin F2{alpha}) in Immature Pig Periventricular Brain Microvessels • Editorial Comment
Stroke, February 1, 2000; 31(2): 516 - 524.
[Abstract] [Full Text] [PDF]
A. Araque, N. Li, R. T. Doyle, and P. G. Haydon
SNARE Protein-Dependent Glutamate Release from Astrocytes
J. Neurosci., January 15, 2000; 20(2): 666 - 673.
[Abstract] [Full Text] [PDF]
A. Kulik, A. Haentzsch, M. Luckermann, W. Reichelt, and K. Ballanyi
Neuron-Glia Signaling via alpha 1 Adrenoceptor-Mediated Ca2+ Release in Bergmann Glial Cells In Situ
J. Neurosci., October 1, 1999; 19(19): 8401 - 8408.
[Abstract] [Full Text] [PDF]
C. M. Atkins and J. D. Sweatt
Reactive Oxygen Species Mediate Activity-Dependent Neuron-Glia Signaling in Output Fibers of the Hippocampus
J. Neurosci., September 1, 1999; 19(17): 7241 - 7248.
[Abstract] [Full Text] [PDF]
R. Ventura and K. M. Harris
Three-Dimensional Relationships between Hippocampal Synapses and Astrocytes
J. Neurosci., August 15, 1999; 19(16): 6897 - 6906.
[Abstract] [Full Text] [PDF]
A. Araque, R. P. Sanzgiri, V. Parpura, and P. G. Haydon
Calcium Elevation in Astrocytes Causes an NMDA Receptor-Dependent Increase in the Frequency of Miniature Synaptic Currents in Cultured Hippocampal Neurons
J. Neurosci., September 1, 1998; 18(17): 6822 - 6829.
[Abstract] [Full Text] [PDF]
V. P. Bindokas, C. C. Lee, W. F. Colmers, and R. J. Miller
Changes in Mitochondrial Function Resulting from Synaptic Activity in the Rat Hippocampal Slice
J. Neurosci., June 15, 1998; 18(12): 4570 - 4587.
[Abstract] [Full Text] [PDF]
A. Nadal, J.-Y. Sul, M. Valdeolmillos, and P. A McNaughton
Albumin elicits calcium signals from astrocytes in brain slices from neonatal rat cortex
J. Physiol., June 15, 1998; 509(3): 711 - 716.
[Abstract] [Full Text] [PDF]
E. A. Newman and K. R. Zahs
Modulation of Neuronal Activity by Glial Cells in the Retina
J. Neurosci., June 1, 1998; 18(11): 4022 - 4028.
[Abstract] [Full Text] [PDF]
M. L. Cotrina, J. Kang, J. H-C Lin, E. Bueno, T. W. Hansen, L. He, Y. Liu, and M. Nedergaard
Astrocytic Gap Junctions Remain Open during Ischemic Conditions
J. Neurosci., April 1, 1998; 18(7): 2520 - 2537.
[Abstract] [Full Text] [PDF]
M. E. Harris-White, S. A. Zanotti, S. A. Frautschy, and A. C. Charles
Spiral Intercellular Calcium Waves in Hippocampal Slice Cultures
J Neurophysiol, February 1, 1998; 79(2): 1045 - 1052.
[Abstract] [Full Text] [PDF]
A. VERKHRATSKY, R. K. ORKAND, and H. KETTENMANN
Glial Calcium: Homeostasis and Signaling Function
Physiol Rev, January 1, 1998; 78(1): 99 - 141.
[Abstract] [Full Text] [PDF]
D. R. Harder, N. J. Alkayed, A. R. Lange, D. Gebremedhin, and R. J. Roman
Functional Hyperemia in the Brain : Hypothesis for Astrocyte-Derived Vasodilator Metabolites
Stroke, January 1, 1998; 29(1): 229 - 234.
[Abstract] [Full Text] [PDF]
G. Seifert, M. Zhou, and C. Steinhauser
Analysis of AMPA Receptor Properties During Postnatal Development of Mouse Hippocampal Astrocytes
J Neurophysiol, December 1, 1997; 78(6): 2916 - 2923.
[Abstract] [Full Text] [PDF]
L. Pasti, A. Volterra, T. Pozzan, and G. Carmignoto
Intracellular Calcium Oscillations in Astrocytes: A Highly Plastic, Bidirectional Form of Communication between Neurons and Astrocytes In Situ
J. Neurosci., October 15, 1997; 17(20): 7817 - 7830.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|