QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

HOME  |   SEARCH  |   ARCHIVE  |   SUBSCRIBE  |   CONTACT  |   HELP

This Article Full Text Full Text (PDF) Submit an eLetter Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (58) Citing Articles via Google Scholar Google Scholar Articles by McKhann, G. M. Articles by Janigro, D. Search for Related Content PubMed PubMed Citation Articles by McKhann, G. M., II Articles by Janigro, D.

 Previous Article  |  Next Article 

Volume 17, Number 18, Issue of September 15, 1997 pp. 6850-6863
Copyright ©1997 Society for Neuroscience

Heterogeneity of Astrocyte Resting Membrane Potentials and Intercellular Coupling Revealed by Whole-Cell and Gramicidin-Perforated Patch Recordings from Cultured Neocortical and Hippocampal Slice Astrocytes

Received May 15, 1997; revised June 23, 1997; accepted June 26, 1997.

Guy M. McKhann II¹, Raimondo D'Ambrosio¹, and Damir Janigro^{1, 2}

¹ Departments of Neurological Surgery and ² Environmental Health, University of Washington School of Medicine, Seattle, Washington 98104

Astrocytes are thought to regulate the extracellular potassium concentration by mechanisms involving both voltage-dependent and transport-mediated ion fluxes combined with intercellular communication via gap junctions. Mechanisms regulating resting membrane potential (RMP) play a fundamental role in determining glial contribution to buffering of extracellular potassium and uptake of potentially toxic neurotransmitters. We have investigated the passive electrophysiological properties of cultured neocortical astrocytes and astrocytes recorded in hippocampal slices from 18-25 d postnatal rats. These experiments revealed a wide range of astrocyte RMPs that were independent of developmental factors, length of culturing, cellular morphology, the electrophysiological techniques used (whole-cell vs perforated recording), cell-specific expression of Na⁺/2HCO₃ co-transporters, or voltage-dependent Na⁺ channels. Exposure of cultured astrocytes to differentiation-inducing factors (such as cAMP) or inhibition of proliferation (by serum deprivation) did not significantly influence RMP. Expression of ATP-sensitive potassium channels was absent in these glia; thus, K_(ATP)-related mechanisms did not contribute to cell resting potential. In both cultured and slice astrocytes, spontaneous electrophysiological changes were commonly observed. These reversible events, which resulted in differential sensitivity to potassium channel blockers (cesium and barium) and sudden current-voltage profile changes, were attributable to dynamic changes in cell-to-cell coupling, as confirmed by recordings from isolated pairs of cells. We conclude that the heterogeneity of astrocytic RMP and intercellular coupling both in culture and in situ are intrinsic properties of glia that may contribute to transcellular transport of potassium. We propose a model in which spatial buffering may be facilitated by heterogeneous mechanisms controlling glial RMP in combination with dynamic changes in intercellular coupling.

Key words: spatial buffering; ion channel; excitability; inward rectifier; glia/neuronal interactions; resting membrane potential

This article has been cited by other articles:

				L. Krizanac-Bengez, M. Hossain, V. Fazio, M. Mayberg, and D. Janigro Loss of flow induces leukocyte-mediated MMP/TIMP imbalance in dynamic in vitro blood-brain barrier model: role of pro-inflammatory cytokines Am J Physiol Cell Physiol, October 1, 2006; 291(4): C740 - C749. [Abstract] [Full Text] [PDF]

				D. B. Kintner, A. Look, G. E. Shull, and D. Sun Stimulation of astrocyte Na+/H+ exchange activity in response to in vitro ischemia depends in part on activation of ERK1/2 Am J Physiol Cell Physiol, October 1, 2005; 289(4): C934 - C945. [Abstract] [Full Text] [PDF]

				B. Lenart, D. B. Kintner, G. E. Shull, and D. Sun Na-K-Cl Cotransporter-Mediated Intracellular Na+ Accumulation Affects Ca2+ Signaling in Astrocytes in an In Vitro Ischemic Model J. Neurosci., October 27, 2004; 24(43): 9585 - 9597. [Abstract] [Full Text] [PDF]

				S. Fukuda, F. Kato, Y. Tozuka, M. Yamaguchi, Y. Miyamoto, and T. Hisatsune Two Distinct Subpopulations of Nestin-Positive Cells in Adult Mouse Dentate Gyrus J. Neurosci., October 15, 2003; 23(28): 9357 - 9366. [Abstract] [Full Text] [PDF]

				F. Amzica, M. Massimini, and A. Manfridi Spatial Buffering during Slow and Paroxysmal Sleep Oscillations in Cortical Networks of Glial Cells In Vivo J. Neurosci., February 1, 2002; 22(3): 1042 - 1053. [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. H. De Pina-Benabou, M. Srinivas, D. C. Spray, and E. Scemes Calmodulin Kinase Pathway Mediates the K+-Induced Increase in Gap Junctional Communication between Mouse Spinal Cord Astrocytes J. Neurosci., September 1, 2001; 21(17): 6635 - 6643. [Abstract] [Full Text] [PDF]

				K. Higashi, A. Fujita, A. Inanobe, M. Tanemoto, K. Doi, T. Kubo, and Y. Kurachi An inwardly rectifying K+ channel, Kir4.1, expressed in astrocytes surrounds synapses and blood vessels in brain Am J Physiol Cell Physiol, September 1, 2001; 281(3): C922 - C931. [Abstract] [Full Text] [PDF]

				M. Zhou and H. K. Kimelberg Freshly Isolated Astrocytes From Rat Hippocampus Show Two Distinct Current Patterns and Different [K+]o Uptake Capabilities J Neurophysiol, December 1, 2000; 84(6): 2746 - 2757. [Abstract] [Full Text] [PDF]

				F. Amzica and M. Steriade Neuronal and Glial Membrane Potentials during Sleep and Paroxysmal Oscillations in the Neocortex J. Neurosci., September 1, 2000; 20(17): 6648 - 6665. [Abstract] [Full Text] [PDF]

				N. Rouach, J. Glowinski, and C. Giaume Activity-dependent Neuronal Control of Gap-junctional Communication in Astrocytes J. Cell Biol., June 26, 2000; 149(7): 1513 - 1526. [Abstract] [Full Text] [PDF]

				Z.-Q. Xiong and J. L. Stringer Extracellular pH Responses in CA1 and the Dentate Gyrus During Electrical Stimulation, Seizure Discharges, and Spreading Depression J Neurophysiol, June 1, 2000; 83(6): 3519 - 3524. [Abstract] [Full Text] [PDF]

				A. Emmi, H. J. Wenzel, P. A. Schwartzkroin, M. Taglialatela, P. Castaldo, L. Bianchi, J. Nerbonne, G. A. Robertson, and D. Janigro Do Glia Have Heart? Expression and Functional Role for Ether-A-Go-Go Currents in Hippocampal Astrocytes J. Neurosci., May 15, 2000; 20(10): 3915 - 3925. [Abstract] [Full Text] [PDF]

				F. Amzica and D. Neckelmann Membrane Capacitance of Cortical Neurons and Glia During Sleep Oscillations and Spike-Wave Seizures J Neurophysiol, November 1, 1999; 82(5): 2731 - 2746. [Abstract] [Full Text] [PDF]

				R. D'Ambrosio, D. O. Maris, M. S. Grady, H. R. Winn, and D. Janigro Impaired K+ Homeostasis and Altered Electrophysiological Properties of Post-Traumatic Hippocampal Glia J. Neurosci., September 15, 1999; 19(18): 8152 - 8162. [Abstract] [Full Text] [PDF]

				S. Kojima, T. Nakamura, T. Nidaira, K. Nakamura, N. Ooashi, E. Ito, K. Watase, K. Tanaka, K. Wada, Y. Kudo, et al. Optical Detection of Synaptically Induced Glutamate Transport in Hippocampal Slices J. Neurosci., April 1, 1999; 19(7): 2580 - 2588. [Abstract] [Full Text] [PDF]

				R. D'Ambrosio, J. Wenzel, P. A. Schwartzkroin, G. M. McKhann II, and D. Janigro Functional Specialization and Topographic Segregation of Hippocampal Astrocytes J. Neurosci., June 15, 1998; 18(12): 4425 - 4438. [Abstract] [Full Text] [PDF]

				G. Carmignoto, L. Pasti, and T. Pozzan On the Role of Voltage-Dependent Calcium Channels in Calcium Signaling of Astrocytes In Situ J. Neurosci., June 15, 1998; 18(12): 4637 - 4645. [Abstract] [Full Text] [PDF]

Home  |   Search  |   Archive  |   Subscribe  |   Contact  |   Help