Cooperative Astrocyte and Dendritic Spine Dynamics at Hippocampal Excitatory Synapses

Overview

Journal J Neurosci

Specialty Neurology

Date 2006 Sep 1

PMID 16943543

Citations 180

Authors

Michael Haber

Lei Zhou

Keith K Murai

Affiliations

Soon will be listed here.

Abstract

Accumulating evidence is redefining the importance of neuron-glial interactions at synapses in the CNS. Astrocytes form "tripartite" complexes with presynaptic and postsynaptic structures and regulate synaptic transmission and plasticity. Despite our understanding of the importance of neuron-glial relationships in physiological contexts, little is known about the structural interplay between astrocytes and synapses. In the past, this has been difficult to explore because studies have been hampered by the lack of a system that preserves complex neuron-glial relationships observed in the brain. Here we present a system that can be used to characterize the intricate relationship between astrocytic processes and synaptic structures in situ using organotypic hippocampal slices, a preparation that retains the three-dimensional architecture of astrocyte-synapse interactions. Using time-lapse confocal imaging, we demonstrate that astrocytes can rapidly extend and retract fine processes to engage and disengage from motile postsynaptic dendritic spines. Surprisingly, astrocytic motility is, on average, higher than its dendritic spine counterparts and likely relies on actin-based cytoskeletal reorganization. Changes in astrocytic processes are typically coordinated with changes in spines, and astrocyte-spine interactions are stabilized at larger spines. Our results suggest that dynamic structural changes in astrocytes help control the degree of neuron-glial communication at hippocampal synapses.

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References

McKinney R, Capogna M, Durr R, Gahwiler B, Thompson S . Miniature synaptic events maintain dendritic spines via AMPA receptor activation. Nat Neurosci. 1999; 2(1):44-9. DOI: 10.1038/4548. View

Grosche J, Matyash V, Moller T, Verkhratsky A, Reichenbach A, Kettenmann H . Microdomains for neuron-glia interaction: parallel fiber signaling to Bergmann glial cells. Nat Neurosci. 1999; 2(2):139-43. DOI: 10.1038/5692. View

Kim C, Lisman J . A role of actin filament in synaptic transmission and long-term potentiation. J Neurosci. 1999; 19(11):4314-24. PMC: 6782630. View

Soffie M, Hahn K, Terao E, Eclancher F . Behavioural and glial changes in old rats following environmental enrichment. Behav Brain Res. 1999; 101(1):37-49. DOI: 10.1016/s0166-4328(98)00139-9. View

Ehrengruber M, Lundstrom K, Schweitzer C, Heuss C, Schlesinger S, Gahwiler B . Recombinant Semliki Forest virus and Sindbis virus efficiently infect neurons in hippocampal slice cultures. Proc Natl Acad Sci U S A. 1999; 96(12):7041-6. PMC: 22049. DOI: 10.1073/pnas.96.12.7041. View

Volfovsky N, Parnas H, Segal M, Korkotian E . Geometry of dendritic spines affects calcium dynamics in hippocampal neurons: theory and experiments. J Neurophysiol. 1999; 82(1):450-62. DOI: 10.1152/jn.1999.82.1.450. View

Ventura R, Harris K . Three-dimensional relationships between hippocampal synapses and astrocytes. J Neurosci. 1999; 19(16):6897-906. PMC: 6782870. View

Dunaevsky A, Tashiro A, Majewska A, Mason C, Yuste R . Developmental regulation of spine motility in the mammalian central nervous system. Proc Natl Acad Sci U S A. 1999; 96(23):13438-43. PMC: 23966. DOI: 10.1073/pnas.96.23.13438. View

Fischer M, Kaech S, Wagner U, Brinkhaus H, MATUS A . Glutamate receptors regulate actin-based plasticity in dendritic spines. Nat Neurosci. 2000; 3(9):887-94. DOI: 10.1038/78791. View

10.

Gan W, Grutzendler J, Wong W, Wong R, Lichtman J . Multicolor "DiOlistic" labeling of the nervous system using lipophilic dye combinations. Neuron. 2000; 27(2):219-25. DOI: 10.1016/s0896-6273(00)00031-3. View

11.

Kaufmann W, Moser H . Dendritic anomalies in disorders associated with mental retardation. Cereb Cortex. 2000; 10(10):981-91. DOI: 10.1093/cercor/10.10.981. View

12.

MATUS A . Actin-based plasticity in dendritic spines. Science. 2000; 290(5492):754-8. DOI: 10.1126/science.290.5492.754. View

13.

Ullian E, Sapperstein S, Christopherson K, Barres B . Control of synapse number by glia. Science. 2001; 291(5504):657-61. DOI: 10.1126/science.291.5504.657. View

14.

Haydon P . GLIA: listening and talking to the synapse. Nat Rev Neurosci. 2001; 2(3):185-93. DOI: 10.1038/35058528. View

15.

Iino M, Goto K, Kakegawa W, Okado H, Sudo M, Ishiuchi S . Glia-synapse interaction through Ca2+-permeable AMPA receptors in Bergmann glia. Science. 2001; 292(5518):926-9. DOI: 10.1126/science.1058827. View

16.

Dunaevsky A, Blazeski R, Yuste R, Mason C . Spine motility with synaptic contact. Nat Neurosci. 2001; 4(7):685-6. DOI: 10.1038/89460. View

17.

Korkotian E, Segal M . Spike-associated fast contraction of dendritic spines in cultured hippocampal neurons. Neuron. 2001; 30(3):751-8. DOI: 10.1016/s0896-6273(01)00314-2. View

18.

Castonguay A, Levesque S, Robitaille R . Glial cells as active partners in synaptic functions. Prog Brain Res. 2001; 132:227-40. DOI: 10.1016/S0079-6123(01)32079-4. View

19.

Bushong E, Martone M, Jones Y, Ellisman M . Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains. J Neurosci. 2002; 22(1):183-92. PMC: 6757596. View

20.

Grosche J, Kettenmann H, Reichenbach A . Bergmann glial cells form distinct morphological structures to interact with cerebellar neurons. J Neurosci Res. 2002; 68(2):138-49. DOI: 10.1002/jnr.10197. View