Interactions between Purkinje neurones and Bergmann glia

Bellamy, Tomas C.

doi:10.1080/14734220600724569

Cited by 118 publications

(102 citation statements)

References 106 publications

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“…Moreover, cerebellar Purkinje cells are inhibitory neurons that do not express adenosine A1 receptors (1,23). It is, however, of interest that both studies concluded that glia Ca 2+ signaling triggers an increase in up states and may reflect that glia use different strategies to modulate neural circuits depending on their location in CNS.…”

Section: Discussionmentioning

confidence: 99%

Bergmann glia modulate cerebellar Purkinje cell bistability via Ca ²⁺ -dependent K ⁺ uptake

Wang

Xu²,

Wang³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

104

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Recent studies have shown that cerebellar Bergmann glia display coordinated Ca 2+ transients in live mice. However, the functional significance of Bergmann glial Ca 2+ signaling remains poorly understood. Using transgenic mice that allow selective stimulation of glial cells, we report here that cytosolic Ca 2+ regulates uptake of K + by Bergmann glia, thus providing a powerful mechanism for control of Purkinje cell-membrane potential. The decline in extracellular K + evoked by agonist-induced Ca 2+ in Bergmann glia transiently increased spike activity of Purkinje cells in cerebellar slices as well as in live anesthetized mice. Thus, Bergmann glia play a previously unappreciated role in controlling the membrane potential and thereby the activity of adjacent Purkinje cells.two-photon laser scanning microscopy | ion-sensitive microelectrode B ergmann glial cells in cerebellum are electrically nonexcitable cells that in many ways serve the same functions as protoplasmic astrocytes in forebrain. Bergmann glia are chiefly responsible for glutamate uptake and extracellular K + homeostasis (1). Their highly negative resting membrane potential of −80 to −85 mV combined with a large number of inwardly rectifying K + channels helps maintain a tight control of extracellular K + concentration (2). Bergmann glial cells also display Ca 2+ transients in response to glutamate or stimulation of climbing and parallel fibers in slices and to motor activity in vivo (3). However, although glial Ca 2+ signaling has been shown to regulate synaptic transmission in several brain regions, it is presently not established whether Bergmann glia can modulate the activity of Purkinje cells.Membrane potentials of almost all neurons in mammalian brain fluctuate between a hyperpolarized state (down state) and depolarized state (up state) during sleep/anesthesia and quiet wakefulness (4, 5). These fluctuations of the membrane potentials are synchronized between neighboring cells and detected as slow (∼0.5-1 Hz), large-amplitude delta waves (4). Even though the existence of bistability of Purkinje cells in awake mice has been questioned, it is generally agreed that bistability is a common phenomenon in both anesthetized and sleeping animals (5). The bistability of the resting membrane potential in Purkinje cells was first discovered by Llinás and Sugimori in cerebellar slices (6, 7). The current model predicts that bistability of Purkinje cells, similar to thalamic neurons, relies on the balance between noninactivating inward currents (persistent Na + currents and/or T-type Ca 2+ currents) (4, 8, 9) and an outward K + leak current (5-7, 10). However, Purkinje cell bistability is not simply an expression of intrinsic membrane properties because complex spikes generated by climbing fiber activation can toggle the membrane potential between up and down states in vivo (5). Recently, glutamate uncaging on distal dendrites of striate spiny neurons was shown to induce up states that lasted hundreds of milliseconds (11), and small hyperpolarization current...

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Section: Discussionmentioning

confidence: 99%

Bergmann glia modulate cerebellar Purkinje cell bistability via Ca ²⁺ -dependent K ⁺ uptake

Wang

Xu²,

Wang³

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

104

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“…The cerebellar PC is a unique neuron due to its huge soma and dendritic tree, its enormous number of synapses and its high vulnerability to pathologic conditions Sarna and Hawkes, 2003). So far, there is good evidence that glial cells influence the function of synaptic inputs to PCs (Bellamy, 2006;Bordey and Sontheimer, 2003;Brockhaus and Deitmer, 2002;Marcaggi et al, 2003;Takayasu et al, 2005), but it is unclear, whether they also contribute to their development. To address this issue, we established immunopanning protocols to enrich for PCs from postnatal mice and to culture them under glia-free conditions.…”

Section: Introductionmentioning

confidence: 99%

Glial cells promote dendrite formation and the reception of synaptic input in Purkinje cells from postnatal mice

Buard

Steinmetz

Claudepierre

et al. 2009

Glia

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Previous studies suggest that glial cells contribute to synaptogenesis in specific neurons from the postnatal CNS. Here, we studied whether this is true for Purkinje cells (PCs), which represent a unique neuronal cell type due to their large size, massive synaptic input, and high vulnerability. Using new glia-free cultures enriched in PCs from postnatal mice we show that these neurons survived and grew, but displayed only low levels of excitatory and inhibitory synaptic activity. Coculture with glial cells strongly enhanced the frequency and size of spontaneous and miniature excitatory synaptic currents as well as neurite growth and branching. Immunocytochemical staining for microtubule-associated protein 2- (MAP2-) positive neurites revealed impaired dendrite formation in PCs under glia-free conditions, which can explain the absence of synaptic activity. Glial signals strongly enhanced dendritogenesis in PCs and thus their ability to receive excitatory synaptic input from granule cells (GCs). The enhancement of dendrite formation was mimicked by glia-conditioned medium (GCM), whereas the increase in synaptic activity required physical presence of glia. This indicated that dendrite development is necessary but not sufficient for PCs to receive excitatory synaptic input and that synaptogenesis requires additional signals. The level of inhibitory synaptic activity was low even in cocultures due to a low incidence of inhibitory interneurons. Taken together, our results reinforce the idea that glial cells promote synaptogenesis in specific neuronal cell types.

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“…The Bergmann glial cell is a specialized astrocyte of the cerebellar cortex, which has a close anatomical and functional association with Purkinje and granule neurons throughout development (Bellamy, 2006;Muller and Kettenmann, 1995;Yamada and Watanabe, 2002). In the adult cerebellum, Bergmann glia display complex lateral processes, which sprout from the radial fibers first described by Bergmann, to form ''microdomains'' that enwrap the numerous synapses of the molecular layer (Grosche et al, 1999(Grosche et al, , 2002.…”

Section: Introductionmentioning

confidence: 99%

Depression of parallel and climbing fiber transmission to Bergmann glia is input specific and correlates with increased precision of synaptic transmission

Balakrishnan

Bellamy

2008

Glia

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In the cerebellar cortex, Bergmann glia enclose the synapses of both parallel and climbing fiber inputs to the Purkinje neuron. The glia express Ca(2+)-permeable AMPA receptors, and the GLAST and GLT-1 classes of glutamate transporter, which are activated by glutamate released during synaptic transmission. We have previously reported that parallel fiber to Bergmann glial transmission in rat cerebellar slices exhibits a form of frequency-dependent plasticity, namely long-term depression, following repetitive stimulation at 0.1-1 Hz. Here, we report that this form of plasticity is also present at the climbing fiber input, that climbing and parallel fibers can be depressed independently, that discrete parallel fiber inputs can also be depressed independently, and that depression is maintained when a distributed array of parallel fibers are stimulated (in contrast to several forms of synaptic plasticity at the Purkinje neuron). Depression of glutamate transporter currents does not correlate with a decrease in the stringency with which Purkinje neuron synapses are isolated. Rather, postsynaptic currents in Purkinje neurons decay more rapidly and perisynaptic metabotropic glutamate receptors are activated less effectively after stimulation at 0.2 and 1 Hz, suggesting that depression arises from a decrease in extrasynaptic glutamate concentration and not from impairment of glutamate clearance in and around the synapse. These results indicate that neuron-glial plasticity is activity dependent, input specific and does not require spillover between adjacent synapses to manifest. They also argue against a withdrawal of the glial sheath from synaptic regions as the putative mechanism of plasticity.

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Interactions between Purkinje neurones and Bergmann glia

Cited by 118 publications

References 106 publications

Bergmann glia modulate cerebellar Purkinje cell bistability via Ca ²⁺ -dependent K ⁺ uptake

Bergmann glia modulate cerebellar Purkinje cell bistability via Ca ²⁺ -dependent K ⁺ uptake

Glial cells promote dendrite formation and the reception of synaptic input in Purkinje cells from postnatal mice

Depression of parallel and climbing fiber transmission to Bergmann glia is input specific and correlates with increased precision of synaptic transmission

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Interactions between Purkinje neurones and Bergmann glia

Cited by 118 publications

References 106 publications

Bergmann glia modulate cerebellar Purkinje cell bistability via Ca 2+ -dependent K + uptake

Bergmann glia modulate cerebellar Purkinje cell bistability via Ca 2+ -dependent K + uptake

Glial cells promote dendrite formation and the reception of synaptic input in Purkinje cells from postnatal mice

Depression of parallel and climbing fiber transmission to Bergmann glia is input specific and correlates with increased precision of synaptic transmission

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Bergmann glia modulate cerebellar Purkinje cell bistability via Ca ²⁺ -dependent K ⁺ uptake

Bergmann glia modulate cerebellar Purkinje cell bistability via Ca ²⁺ -dependent K ⁺ uptake