Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Science 30 September 1994:
Vol. 265. no. 5181, pp. 2098 - 2101
DOI: 10.1126/science.7916485
Prev | Table of Contents | Next

Articles

Science, Vol 265, Issue 5181, 2098-2101
Copyright © 1994 by American Association for the Advancement of Science

articles

Release of adenosine by activation of NMDA receptors in the hippocampus

OJ Manzoni, T Manabe, and RA Nicoll

Department of Pharmacology, University of California at San Francisco 94143.

Adenosine is present in the mammalian brain in large amounts and has potent effects on neuronal activity, but its role in neural signaling is poorly understood. The glutamate receptor agonist N-methyl-D-aspartate (NMDA) caused a presynaptic depression of excitatory synaptic transmission in the CA1 region of guinea pig hippocampal slices. This depression was blocked by an adenosine A1 receptor antagonist, which suggests that activation of the NMDA subtype of glutamate receptor raises the concentration of extracellular adenosine, which acts on presynaptic inhibitory A1 receptors. Strong tetanic stimulation caused a heterosynaptic inhibition that was blocked by both NMDA and A1 receptor antagonists. Enkephalin, which selectively inhibits interneurons, antagonized the heterosynaptic inhibition. These findings suggest that synaptically released glutamate activates NMDA receptors, which in turn releases adenosine, at least in part from interneurons, that acts at a distance to inhibit presynaptically the release of glutamate from excitatory synapses. Thus, interneurons may mediate a widespread purinergic presynaptic inhibition.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
The GABAB1a Isoform Mediates Heterosynaptic Depression at Hippocampal Mossy Fiber Synapses.
N. Guetg, R. Seddik, R. Vigot, R. Turecek, M. Gassmann, K. E. Vogt, H. Brauner-Osborne, R. Shigemoto, O. Kretz, M. Frotscher, et al. (2009)
J. Neurosci. 29, 1414-1423
   Abstract »    Full Text »    PDF »
The Hemo-Neural Hypothesis: On The Role of Blood Flow in Information Processing.
C. I. Moore and R. Cao (2008)
J Neurophysiol 99, 2035-2047
   Abstract »    Full Text »    PDF »
Astrocytes play a critical role in transient heterosynaptic depression in the rat hippocampal CA1 region.
M. Andersson, F. Blomstrand, and E. Hanse (2007)
J. Physiol. 585, 843-852
   Abstract »    Full Text »    PDF »
Coincident Glutamatergic and Cholinergic Inputs Transiently Depress Glutamate Release at Rat Schaffer Collateral Synapses.
K. E. Gipson and M. F. Yeckel (2007)
J Neurophysiol 97, 4108-4119
   Abstract »    Full Text »    PDF »
Activity-Dependent Depression of Local Excitatory Connections in the CA1 Region of Mouse Hippocampus.
A. E. Fink, J. Sarinana, E. E. Gray, and T. J. O'Dell (2007)
J Neurophysiol 97, 3926-3936
   Abstract »    Full Text »    PDF »
The Neuropeptide Nociceptin Is a Synaptically Released Endogenous Inhibitor of Hippocampal Long-Term Potentiation.
S. Bongsebandhu-phubhakdi and T. Manabe (2007)
J. Neurosci. 27, 4850-4858
   Abstract »    Full Text »    PDF »
GABAergic Interneurons Facilitate Mossy Fiber Excitability in the Developing Hippocampus.
M. Nakamura, Y. Sekino, and T. Manabe (2007)
J. Neurosci. 27, 1365-1373
   Abstract »    Full Text »    PDF »
Adenosine Inhibits Activity of Hypocretin/Orexin Neurons by the A1 Receptor in the Lateral Hypothalamus: A Possible Sleep-Promoting Effect.
Z.-W. Liu and X.-B. Gao (2007)
J Neurophysiol 97, 837-848
   Abstract »    Full Text »    PDF »
Astrocyte control of synaptic transmission and neurovascular coupling..
P. G. Haydon and G. Carmignoto (2006)
Physiol Rev 86, 1009-1031
   Abstract »    Full Text »    PDF »
Astrocytes Coordinate Synaptic Networks: Balanced Excitation and Inhibition.
T. Fellin, O. Pascual, and P. G. Haydon (2006)
Physiology 21, 208-215
   Abstract »    Full Text »    PDF »
ERK-Dependent Modulation of Cerebellar Synaptic Plasticity after Chronic {Delta}9-Tetrahydrocannabinol Exposure.
R. Tonini, S. Ciardo, M. Cerovic, T. Rubino, D. Parolaro, M. Mazzanti, and R. Zippel (2006)
J. Neurosci. 26, 5810-5818
   Abstract »    Full Text »    PDF »
GABAergic network activation of glial cells underlies hippocampal heterosynaptic depression..
A. Serrano, N. Haddjeri, J.-C. Lacaille, and R. Robitaille (2006)
J. Neurosci. 26, 5370-5382
   Abstract »    Full Text »    PDF »
Epileptogenesis Is Associated With Enhanced Glutamatergic Transmission in the Perforant Path.
A. Scimemi, S. Schorge, D. M. Kullmann, and M. C. Walker (2006)
J Neurophysiol 95, 1213-1220
   Abstract »    Full Text »    PDF »
Astrocytic Purinergic Signaling Coordinates Synaptic Networks.
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 (2005)
Science 310, 113-116
   Abstract »    Full Text »    PDF »
Targeting Prefrontal Cortical Dopamine D1 and N-Methyl-D-Aspartate Receptor Interactions in Schizophrenia Treatment.
C. R. Yang and L. Chen (2005)
Neuroscientist 11, 452-470
   Abstract »    PDF »
A2B receptor activation promotes glycogen synthesis in astrocytes through modulation of gene expression.
I. Allaman, S. Lengacher, P. J. Magistretti, and L. Pellerin (2003)
Am J Physiol Cell Physiol 284, C696-C704
   Abstract »    Full Text »    PDF »
Activity-Dependent Release of Adenosine Contributes to Short-Term Depression at CA3-CA1 Synapses in Rat Hippocampus.
D. H. Brager and S. M. Thompson (2003)
J Neurophysiol 89, 22-26
   Abstract »    Full Text »    PDF »
International Union of Pharmacology. XXV. Nomenclature and Classification of Adenosine Receptors.
B. B. Fredholm, A. P. IJzerman, K. A. Jacobson, K.-N. Klotz, and J. Linden (2001)
Pharmacol. Rev. 53, 527-552
   Abstract »    Full Text »    PDF »
Effects of adenosine receptors on the synaptic and EPSP-spike components of long-term potentiation and depotentiation in the guinea-pig hippocampus.
S. Fujii, Y. Kuroda, K.-i. Ito, K. Kaneko, and H. Kato (1999)
J. Physiol. 521, 451-466
   Abstract »    Full Text »    PDF »
Adenosine-induced presynaptic inhibition of IPSCs and EPSCs in rat hypothalamic supraoptic nucleus neurones.
S. H R Oliet and D. A Poulain (1999)
J. Physiol. 520, 815-825
   Abstract »    Full Text »    PDF »
Adenosine: a Mediator of Interleukin-1beta -Induced Hippocampal Synaptic Inhibition.
W. P. Luk, Y. Zhang, T. D. White, F. A. Lue, C. Wu, C.-G. Jiang, L. Zhang, and H. Moldofsky (1999)
J. Neurosci. 19, 4238-4244
   Abstract »    Full Text »    PDF »
Temperature-Dependent Modulation of Excitatory Transmission in Hippocampal Slices Is Mediated by Extracellular Adenosine.
S. A. Masino and T. V. Dunwiddie (1999)
J. Neurosci. 19, 1932-1939
   Abstract »    Full Text »    PDF »
Decreased Presynaptic Sensitivity to Adenosine after Cocaine Withdrawal.
O. Manzoni, D. Pujalte, J. Williams, and J. Bockaert (1998)
J. Neurosci. 18, 7996-8002
   Abstract »    Full Text »    PDF »
Predictive Reward Signal of Dopamine Neurons.
W. Schultz (1998)
J Neurophysiol 80, 1-27
   Abstract »    Full Text »    PDF »
Kainate receptor-mediated inhibition of presynaptic Ca2+ influx and EPSP in area CA1 of the rat hippocampus.
H. Kamiya and S. Ozawa (1998)
J. Physiol. 509, 833-845
   Abstract »    Full Text »    PDF »
Levels of Endogenous Adenosine in Rat Striatum. I. Regulation by Ionotropic Glutamate Receptors, Nitric Oxide and Free Radicals.
S. M. Delaney, P. N. Shepel, and J. D. Geiger (1998)
J. Pharmacol. Exp. Ther. 285, 561-567
   Abstract »    Full Text »
Effect of Protein Kinase C Activation on N-Methyl-D-Aspartate-Evoked Release of Adenosine and [3H]Norepinephrine from Rat Cortical Slices.
Y. Wang and T. D. White (1998)
J. Pharmacol. Exp. Ther. 285, 105-109
   Abstract »    Full Text »
Differential Presynaptic Localization of Metabotropic Glutamate Receptor Subtypes in the Rat Hippocampus.
R. Shigemoto, A. Kinoshita, E. Wada, S. Nomura, H. Ohishi, M. Takada, P. J. Flor, A. Neki, T. Abe, S. Nakanishi, et al. (1997)
J. Neurosci. 17, 7503-7522
   Abstract »    Full Text »    PDF »
A Postsynaptic Interaction between Dopamine D1 and NMDA Receptors Promotes Presynaptic Inhibition in the Rat Nucleus Accumbens via Adenosine Release.
J. Harvey and M. G. Lacey (1997)
J. Neurosci. 17, 5271-5280
   Abstract »    Full Text »    PDF »
Adenosine Modulation of Calcium Currents and Presynaptic Inhibition of GABA Release in Suprachiasmatic and Arcuate Nucleus Neurons.
G. Chen and A. N. van den Pol (1997)
J Neurophysiol 77, 3035-3047
   Abstract »    Full Text »    PDF »
Distinct forms of short-term plasticity at excitatory synapses of hippocampus and neocortex.
M. A. Castro-Alamancos and B. W. Connors (1997)
PNAS 94, 4161-4166
   Abstract »    Full Text »    PDF »
Modulation of Excitatory Synaptic Transmission by Adenosine Released from Single Hippocampal Pyramidal Neurons.
J. M. Brundege and T. V. Dunwiddie (1996)
J. Neurosci. 16, 5603-5612
   Abstract »    Full Text »    PDF »
Presynaptic N-methyl-D-aspartate receptors at the parallel fiber-Purkinje cell synapse.
M. Casado, S. Dieudonne, and P. Ascher (2000)
PNAS 97, 11593-11597
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)