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Determinants of functional coupling between astrocytes and respiratory neurons in the pre-Bötzinger complex.

Schnell C, Fresemann J, Hülsmann S - PLoS ONE (2011)

Bottom Line: In astrocytes that exhibited rhythmic potassium fluxes and glutamate transporter currents, we did not find a translation of respiratory neuronal activity into phase-locked astroglial calcium signals.We conclude that astrocytes do not exhibit respiratory-rhythmic calcium fluctuations when they are able to prevent synaptic glutamate accumulation.Calcium signaling is, however, observed when glutamate transport processes in astrocytes are suppressed or neuronal discharge activity is excessive.

View Article: PubMed Central - PubMed

Affiliation: Abt. Neuro- und Sinnesphysiologie, Zentrum Physiologie und Pathophysiologie, Georg-August-Universität, Göttingen, Germany.

ABSTRACT
Respiratory neuronal network activity is thought to require efficient functioning of astrocytes. Here, we analyzed neuron-astrocyte communication in the pre-Bötzinger Complex (preBötC) of rhythmic slice preparations from neonatal mice. In astrocytes that exhibited rhythmic potassium fluxes and glutamate transporter currents, we did not find a translation of respiratory neuronal activity into phase-locked astroglial calcium signals. In up to 20% of astrocytes, 2-photon calcium imaging revealed spontaneous calcium fluctuations, although with no correlation to neuronal activity. Calcium signals could be elicited in preBötC astrocytes by metabotropic glutamate receptor activation or after inhibition of glial glutamate uptake. In the latter case, astrocyte calcium elevation preceded a surge of respiratory neuron discharge activity followed by network failure. We conclude that astrocytes do not exhibit respiratory-rhythmic calcium fluctuations when they are able to prevent synaptic glutamate accumulation. Calcium signaling is, however, observed when glutamate transport processes in astrocytes are suppressed or neuronal discharge activity is excessive.

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Lack of respiratory-rhythmic calcium signals in astrocytes of the pre-Bötzinger Complex.The figure shows an example of 2-photon calcium imaging from identified astrocytes in the pre-Bötzinger Complex in the presence of bicuculline (20 µM) and strychnine (10 µM). EGFP astrocytes (A) were labeled with Oregon Green BAPTA-1 AM (OGB-1 AM, B). (C) Cross correlation (CC) maps of OGB-1 AM fluorescence were calculated for each image series between each pixel and a respiratory neuron (cell 7). In panel (D) the OGB-1 AM fluorescence signals from three astrocytes (1–3) and four respiratory neurons (4–7) are depicted with the integrated network output (preBötC ∫). Astrocytes show spontaneous calcium oscillations that were not phase-locked to the neuronal activity. Additionally, as shown in panel (E) the cycle-averaged data of these recording did not reveal any respiratory-rhythmic calcium signal in the astrocytes.
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pone-0026309-g005: Lack of respiratory-rhythmic calcium signals in astrocytes of the pre-Bötzinger Complex.The figure shows an example of 2-photon calcium imaging from identified astrocytes in the pre-Bötzinger Complex in the presence of bicuculline (20 µM) and strychnine (10 µM). EGFP astrocytes (A) were labeled with Oregon Green BAPTA-1 AM (OGB-1 AM, B). (C) Cross correlation (CC) maps of OGB-1 AM fluorescence were calculated for each image series between each pixel and a respiratory neuron (cell 7). In panel (D) the OGB-1 AM fluorescence signals from three astrocytes (1–3) and four respiratory neurons (4–7) are depicted with the integrated network output (preBötC ∫). Astrocytes show spontaneous calcium oscillations that were not phase-locked to the neuronal activity. Additionally, as shown in panel (E) the cycle-averaged data of these recording did not reveal any respiratory-rhythmic calcium signal in the astrocytes.

Mentions: Two–photon imaging of cells loaded with Oregon Green BAPTA-1 AM (OGB-1 AM) was also carried out to detect Ca2+ signals simultaneously in preBötC astrocytes and neurons on the surface and deeper in the slice. Calcium signals were measured in 14 slices from 300 fluorescent-protein labeled astrocytes and from 103 respiratory neurons that were located within 50 µm of the labeled astrocytes (figure 5). Thirty-eight astrocytes (12.7%) exhibited spontaneous fluctuating calcium signals. The calcium signals, however, were not correlated with and entrained by preBötC neuron discharges.


Determinants of functional coupling between astrocytes and respiratory neurons in the pre-Bötzinger complex.

Schnell C, Fresemann J, Hülsmann S - PLoS ONE (2011)

Lack of respiratory-rhythmic calcium signals in astrocytes of the pre-Bötzinger Complex.The figure shows an example of 2-photon calcium imaging from identified astrocytes in the pre-Bötzinger Complex in the presence of bicuculline (20 µM) and strychnine (10 µM). EGFP astrocytes (A) were labeled with Oregon Green BAPTA-1 AM (OGB-1 AM, B). (C) Cross correlation (CC) maps of OGB-1 AM fluorescence were calculated for each image series between each pixel and a respiratory neuron (cell 7). In panel (D) the OGB-1 AM fluorescence signals from three astrocytes (1–3) and four respiratory neurons (4–7) are depicted with the integrated network output (preBötC ∫). Astrocytes show spontaneous calcium oscillations that were not phase-locked to the neuronal activity. Additionally, as shown in panel (E) the cycle-averaged data of these recording did not reveal any respiratory-rhythmic calcium signal in the astrocytes.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3198395&req=5

pone-0026309-g005: Lack of respiratory-rhythmic calcium signals in astrocytes of the pre-Bötzinger Complex.The figure shows an example of 2-photon calcium imaging from identified astrocytes in the pre-Bötzinger Complex in the presence of bicuculline (20 µM) and strychnine (10 µM). EGFP astrocytes (A) were labeled with Oregon Green BAPTA-1 AM (OGB-1 AM, B). (C) Cross correlation (CC) maps of OGB-1 AM fluorescence were calculated for each image series between each pixel and a respiratory neuron (cell 7). In panel (D) the OGB-1 AM fluorescence signals from three astrocytes (1–3) and four respiratory neurons (4–7) are depicted with the integrated network output (preBötC ∫). Astrocytes show spontaneous calcium oscillations that were not phase-locked to the neuronal activity. Additionally, as shown in panel (E) the cycle-averaged data of these recording did not reveal any respiratory-rhythmic calcium signal in the astrocytes.
Mentions: Two–photon imaging of cells loaded with Oregon Green BAPTA-1 AM (OGB-1 AM) was also carried out to detect Ca2+ signals simultaneously in preBötC astrocytes and neurons on the surface and deeper in the slice. Calcium signals were measured in 14 slices from 300 fluorescent-protein labeled astrocytes and from 103 respiratory neurons that were located within 50 µm of the labeled astrocytes (figure 5). Thirty-eight astrocytes (12.7%) exhibited spontaneous fluctuating calcium signals. The calcium signals, however, were not correlated with and entrained by preBötC neuron discharges.

Bottom Line: In astrocytes that exhibited rhythmic potassium fluxes and glutamate transporter currents, we did not find a translation of respiratory neuronal activity into phase-locked astroglial calcium signals.We conclude that astrocytes do not exhibit respiratory-rhythmic calcium fluctuations when they are able to prevent synaptic glutamate accumulation.Calcium signaling is, however, observed when glutamate transport processes in astrocytes are suppressed or neuronal discharge activity is excessive.

View Article: PubMed Central - PubMed

Affiliation: Abt. Neuro- und Sinnesphysiologie, Zentrum Physiologie und Pathophysiologie, Georg-August-Universität, Göttingen, Germany.

ABSTRACT
Respiratory neuronal network activity is thought to require efficient functioning of astrocytes. Here, we analyzed neuron-astrocyte communication in the pre-Bötzinger Complex (preBötC) of rhythmic slice preparations from neonatal mice. In astrocytes that exhibited rhythmic potassium fluxes and glutamate transporter currents, we did not find a translation of respiratory neuronal activity into phase-locked astroglial calcium signals. In up to 20% of astrocytes, 2-photon calcium imaging revealed spontaneous calcium fluctuations, although with no correlation to neuronal activity. Calcium signals could be elicited in preBötC astrocytes by metabotropic glutamate receptor activation or after inhibition of glial glutamate uptake. In the latter case, astrocyte calcium elevation preceded a surge of respiratory neuron discharge activity followed by network failure. We conclude that astrocytes do not exhibit respiratory-rhythmic calcium fluctuations when they are able to prevent synaptic glutamate accumulation. Calcium signaling is, however, observed when glutamate transport processes in astrocytes are suppressed or neuronal discharge activity is excessive.

Show MeSH
Related in: MedlinePlus