Synaptically released glutamate does not overwhelm transporters on hippocampal astrocytes during high-frequency stimulation

Journal of Neurophysiology

Volumn 83, Issue 5, 2000, Pages 2835-2843

  Diamond, Jeffrey S ^a,b   Jahr, Craig E ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMATE TRANSPORTER; GLUTAMIC ACID;

ACTION POTENTIAL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; ELECTROPHYSIOLOGY; HIPPOCAMPUS; LONG TERM POTENTIATION; MEASUREMENT; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPTIC TRANSMISSION;

EID: 0034127640     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.2000.83.5.2835     Document Type: Article

References (58)

1. ANDERSEN, P., SUNDBERG, S. H., SVEEN, O., AND WIGSTROM, H. Specific long-lasting potentiation of synaptic transmission in hippocampal slices. Nature 266: 736-737, 1977.
2. ARRIZA, J. L., FAIRMAN, W. A., WADICHE, J. I., MURDOCH, G. H., KAVANAUGH, M. P., AND AMARA, S. G. Functional comparisons of three glutamate transporter subtypes cloned from human motor cortex. J. Neurosci. 14: 5559-5569, 1994.
3. ASZTELY, F., ERDEMLI, G., AND KULLMANN, D. M. Extrasynaptic glutamate spillover in the hippocampus: dependence on temperature and the role of active glutamate uptake. Neuron 18: 281-293, 1997.
4. BARBOUR, B., KELLER, B. U., LLANO, I., AND MARTY, A. Prolonged presence of glutamate during excitatory synaptic transmission to cerebellar Purkinje cells. Neuron 12: 1331-1343, 1994.
5. BASKYS, A. AND MALENKA, R. C. Agonists at metabotropic glutamate receptors presynaptically inhibit EPSCs in neonatal rat hippocampus. J. Physiol. (Lond.) 444: 687-701, 1991.
6. BERGLES, D. E. AND JAHR, C. E. Synaptic activation of glutamate transporters in hippocampal astrocytes. Neuron 19: 1297-1308, 1997.
7. BERGLES, D. E. AND JAHR, C. E. Glial contribution to glutamate uptake at Schaffer collateral-commissural synapses in the hippocampus. J. Neurosci. 18: 7709-7716, 1998.
8. BLISS, T. V. AND LOMO, T. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol. (Lond.) 232: 331-356, 1973.
9. BRUNDEGE, J. M. AND DUNWIDDIE, T. V. Role of adenosine as a modulator of synaptic activity in the central nervous system. Adv. Pharmacol. 39: 353-391, 1997.
10. CLEMENTS, J. D. A statistical test for demonstrating a presynaptic site of action for a modulator of synaptic amplitude. J. Neurosci. Methods 31: 75-88, 1990.
11. CLEMENTS, J. D. Transmitter timecourse in the synaptic cleft: its role in central synaptic function. Trends Neurosci. 19: 163-171, 1996.
12. CLEMENTS, J. D., LESTER, R. A., TONG, G., JAHR, C. E., AND WESTBROOK, G. L. The time course of glutamate in the synaptic cleft. Science 258: 1498-1501, 1992.
13. COGNAR, P., LEINEKUGEL, X., BEN-ARI, Y., AND CRÉPEL, V. A long-lasting calcium-activated nonselective cation current is generated by synaptic stimulation or exogenous activation of group I metabotropic glutamate receptors in CA1 pyramidal neurons. J. Neurosci. 17: 5366-5379, 1997.
14. DE BARRY, J., LANGLEY, O. K., VINCENDON, G., AND GUMBOS, G. L-Glutamate and L-glutamine uptake in adult rat cerebellum: an autoradiographic study. Neuroscience 7: 1289-1297, 1982.
15. DEL CASTILLO, J. AND KATZ, B. Quantal components of the end-plate potential. J. Physiol. (Lond.) 124: 560-573, 1954.
16. DIAMOND, J. S., BERGLES, D. E., AND JAHR, C. E. Glutamate release monitored with astrocyte transporter currents during LTP. Neuron 21: 425-433, 1998.
17. DIAMOND, J. S. AND JAHR, C. E. Asynchronous release of synaptic vesicles determines the time course of the AMPA receptor-mediated EPSC. Neuron 15: 1097-1107, 1995.
18. DIAMOND, J. S. AND JAHR, C. E. Transporters buffer synaptically released glutamate on a submillisecond time scale. J. Neurosci. 17: 4672-4687, 1997.
19. DIAO, L. H. AND DUNWIDDIE, T. V. The effect of temperature on adenosine receptor and adenosine transporter function in rat hippocampal slices. Soc. Neurosci. Abstr. 24: 1604, 1998.
20. FABER, D. S. AND KORN, H. Applicability of the coefficient of variation method for analysing synaptic plasticity. Biophys. J. 60: 1288-1294, 1991.
21. FAIRMAN, W. A., VANDENBERG, R. J., ARRIZA, J. L., KAVANAUGH, M. P., AND AMARA, S. G. An excitatory amino-acid transporter with properties of a ligand-gated chloride channel. Nature 375: 599-603, 1995.
22. FORSYTHE, I. D. AND CLEMENTS, J. D. Presynaptic glutamate receptors depress excitatory monosynaptic transmission between mouse hippocampal neurones. J. Physiol. (Lond.) 429: 1-16, 1990.
23. HARRIS, K. M. AND VENTURA, R. Small inter-PSD distances and variability in astroglial coverage suggests that glutamate spillover occurs at many but not all hippocampal CA1 synapses. Soc. Neurosci. Abstr. 24: 827, 1998.
24. HARTZELL, H. C., KUFFLER, S. W., AND YOSHIKAMI, D. Postsynaptic potentiation: interaction between quanta of acetylcholine at the skeletal neuromuscular synapse. J. Physiol. (Lond.) 251: 427-463, 1975.
25. HAUSSER, M. AND ROTH, A. Estimating the time course of the excitatory synaptic conductance in neocortical pyramidal cells using a novel voltage jump method. J. Neurosci. 17: 7606-7625, 1997.
26. HJELMSTAD, G. O., NICOLL, R. A., AND MALENKA, R. C. Synaptic refractory period provides a measure of probability of release in the hippocampus. Neuron 19: 1309-1318, 1997.
27. ISAAC, J. T., NICOLL, R. A., AND MALENKA, R. C. Evidence for silent synapses: implications for the expression of LTP. Neuron 15: 427-434, 1995.
28. JOHNSTON, G. A., KENNEDY, S. M., AND TWITCHIN, B. Action of the neurotoxin kainic acid on high affinity uptake of L-glutamic acid in rat brain slices. J. Neurochem. 32: 121-127, 1979.
29. KLOCKNER, U., STORCK, T., CONRADT, M., AND STOFFEL, W. Functional properties and substrate specificity of the cloned L-glutamate/L-aspartate transporter GLAST-1 from rat brain expressed in Xenopus oocytes. J. Neurosci. 14: 5759-5765, 1994.
30. KOJIMA, S., NAKAMURA, T., NIDAIRA, T., NAKAMURA, K., OOASHI, N., ITO, E., WATASE, K., TANAKA, K., WADA, K., KUDO, Y., AND MIYAKAWA, H. Optical detection of synaptically induced glutamate transport in hippocampal slices. J. Neurosci. 19: 2580-2588, 1999.
31. KULLMANN, D. M. Amplitude fluctuations of dual-component EPSCs in hippocampal pyramidal cells: implications for long-term potentiation. Neuron 12: 1111-1120, 1994.
32. KULLMANN, D. M. AND ASZTELY, F. Extrasynaptic glutamate spillover in the hippocampus: evidence and implications. Trends Neurosci. 21: 8-14, 1998.
33. KULLMANN, D. M., ERDEMLI, G., AND ASZTELY, F. LTP of AMPA and NMDA receptor-mediated signals: evidence for presynaptic expression and extrasynaptic glutamate spill-over. Neuron 17: 461-474, 1996.
34. LARSON, J., WONG, D., AND LYNCH, G. Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Res. 368: 347-350, 1986.
35. LEHRE, K. P. AND DANBOLT, N. C. The number of glutamate transporter subtype molecules at glutamatergic synapses: chemical and stereological quantification in young adult rat brain. J. Neurosci. 18: 8751-8757, 1998.
36. LIAO, D., HESSLER, N. A., AND MALINOW, R. Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375: 400-404, 1995.
37. LUSCHER, C., MALENKA, R. C., AND NICOLL, R. A. Monitoring glutamate release during LTP with glial transporter currents. Neuron 21: 435-441, 1998.
38. LYNCH, G. S., DUNWIDDIE, T., AND GRIBKOFF, V. Heterosynaptic depression: a postsynaptic correlate of long-term potentiation. Nature 266: 737-739, 1977.
39. MCLENNAN, H. The autoradiographic localization of L-[3h]glutamate in rat brain tissue. Brain Res. 115: 139-144, 1976.
40. MENNERICK, S. AND ZORUMSKI, C. F. Presynaptic influence on the time course of fast excitatory synaptic currents in cultured hippocampal cells. J. Neurosci. 15: 3178-3192, 1995.
41. MIN, M. Y., RUSAKOV, D. A., AND KULLMANN, D. M. Activation of AMPA, kainate, and metabotropic receptors at hippocampal mossy fiber synapses: role of glutamate diffusion. Neuron 21: 561-570, 1998.
42. OTIS, T. S., KAVANALIGH, M. P., AND JAHR, C. E. Postsynaptic glutamate transport at the climbing fiber-Purkinje cell synapse. Science 277: 1515-1518, 1997.
43. OTIS, T. S., WU, Y. C., AND TRUSSELL, L. O. Delayed clearance of transmitter and the role of glutamate transporters at synapses with multiple release sites. J. Neurosci. 16: 1634-1644, 1996.
44. PINES, G., DANBOLT, N. C., BJORAS, M., ZHANG, Y., BENBAHAN, A., EIDE, L., KOEPSELL, H., STORM-MATHISEN, J., SEEBERG, E., AND KANNER, B. I. Cloning and expression of a rat brain L-glutamate transporter. Nature 360: 464-467, 1992.
45. ROTHSTEIN, J. D., DYKES-HOBERG, M., PARDO, C. A., BRISTOL, L. A., JIN, L., KUNCL, R. W., KANAI, Y., HEDIGER, M. A., WANG, Y., SCHIELKE, J. P., AND WELTY, D. F. Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron 16: 675-686, 1996.
46. ROTHSTEIN, J. D., MARTIN, L., LEVEY, A. I., DYKES-HOBERG, M., JIN, L., WU, D., NASH, N., AND KUNCL, R. W. Localization of neuronal and glial glutamate transporters. Neuron 13: 713-725, 1994.
47. RUSAKOV, D. A. AND KULLMANN, D. M. Extrasynaptic glutamate diffusion in the hippocampus: ultrastructural constraints, uptake, and receptor activation. J. Neurosci. 18: 3158-3170, 1998.
48. SCANZIANI, M., SALIN, P. A., VOGT, K. E., MALENKA, R. C., AND NICOLL, R. A. Use-dependent increases in glutamate concentration activate presynaptic metabotropic glutamate receptors. Nature 385: 630-634, 1997.
49. SPRUSTON, N., JAFFE, D. B., WILLIAMS, S. H., AND JOHNSTON, D. Voltage- and space-clamp errors associated with the measurement of electrotonically remote synaptic events. J. Neurophysiol. 70: 781-802, 1993.
50. STEVENS, C. F. AND WANG, Y. Facilitation and depression at single central synapses. Neuron 14: 795-802, 1995.
51. TAKAHASHI, M., KOVALCHUK, Y., AND ATTWELL, D. Pre- and postsynaptic determinants of EPSC waveform at cerebellar climbing fiber and parallel fiber to Purkinje cell synapses. J. Neurosci. 15: 5693-5702, 1995.
52. TANAKA, K., WATASE, K., MANABE, T., YAMADA, K., WATANABE, M., TAKAHASHI, K., IWAMA, H., NISHIKAWA, T., ICHIHARA, N., KIKUCHI, T., OKUYAMA, S., KAWASHIMA, N., HORI, S., TAKIMOTO, M., AND WADA, K. Epilepsy and exacerbation of brain injury in mice lacking the glutamate transporter GLT-1. Science 276: 1699-1702, 1997.
53. TONG, G. AND JAHR, C. E. Block of glutamate transporters potentiates postsynaptic excitation. Neuron 13: 1195-1203, 1994.
54. VON GERSDORFF, H., SCHNEGGENRURGER, R., WEIS, S., AND NEHER, E. Presynaptic depression at a calyx synapse: the small contribution of metabotropic glutamate receptors. J. Neurosci. 17: 8137-8146, 1997.
55. WADICHE, J. I., AMARA, S. G., AND KAVANAUGH, M. P. Ion fluxes associated with excitatory amino acid transport. Neuron 15: 721-728, 1995.
56. WADICHE, J. I. AND KAVANAUGH, M. P. Macroscopic and microscopic properties of a cloned glutamate transporter/chloride channel. J. Neurosci. 18: 7650-7661, 1998.
57. WAHL, L. M., POUZAT, C., AND STRATFORD, K. J. Monte Carlo simulation of fast excitatory synaptic transmission at a hippocampal synapse. J. Neurophysiol. 75: 597-608, 1996.
58. WILKIN, G. P., GARTHWAITE, J., AND BALAZS, R. Putative acidic amino acid transmitters in the cerebellum. II. Electron microscopic localization of transport sites. Brain Res. 244: 69-80, 1982.