Rapid astrocyte calcium signals correlate with neuronal activity and onset of the hemodynamic response in vivo
Open accessAbstract
Elevation of intracellular Ca2+ in astrocytes can influence cerebral microcirculation and modulate synaptic transmission. Recently, in vivo imaging studies identified delayed, sensory-driven Ca2+ oscillations in cortical astrocytes; however, the long latencies of these Ca2+ signals raises questions in regards to their suitability for a role in short-latency modulation of cerebral microcirculation or rapid astrocyte-to-neuron communication. Here, using in vivo two-photon Ca2+ imaging, we demonstrate that approximately 5% of sulforhodamine 101-labeled astrocytes in the hindlimb area of the mouse primary somatosensory cortex exhibit short-latency (peak amplitude approximately 0.5 s after stimulus onset), contralateral hindlimb-selective sensory-evoked Ca2+ signals that operate on a time scale similar to neuronal activity and correlate with the onset of the hemodynamic response as measured by intrinsic signal imaging. The kinetics of astrocyte Ca2+ transients were similar in rise and decay times to postsynaptic neuronal transients, but decayed more slowly than neuropil Ca2+ transients that presumably reflect presynaptic transients. These in vivo findings suggest that astrocytes can respond to sensory activity in a selective manner and process information on a subsecond time scale, enabling them to potentially form an active partnership with neurons for rapid regulation of microvascular tone and neuron-astrocyte network properties.
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TL;DR
In urethane-anesthetized mice, a small subset (~5%) of SR101-labeled astrocytes in hindlimb somatosensory cortex showed contralateral hindlimb-selective sensory-evoked Ca²⁺ signals peaking ~0.5 s after stimulus onset. These rapid astrocyte signals matched neuronal timescales and correlated with the onset of the hemodynamic response, suggesting astrocytes can respond on subsecond timescales relevant to neurovascular coupling.
Key findings
- Of 355 astrocytes (7 mice), 18 (5.07%; 5.08 ± 1.28% per mouse) showed above-threshold Ca²⁺ elevation after contralateral hindlimb stimulation; no other limbs induced significant responses. Astrocyte peak amplitude was 19.1 ± 1.7% ΔF/F₀.
- Time-to-peak did not differ significantly among astrocytes (0.41 ± 0.11 s), neurons (0.56 ± 0.09 s), and neuropil (0.43 ± 0.09 s; F(2,18) = 0.67; p = 0.52). Decay tau was shorter in neuropil (0.55 ± 0.04 s) than astrocytes (1.07 ± 0.17 s; p = 0.011) and neurons (1.21 ± 0.18 s; p = 0.005).
- The IOS hemodynamic response began ~600–800 ms after stimulus onset, while astrocyte Ca²⁺ peaked ~0.5 s after onset. Endfoot transients occurred in 12.7% of endfeet (n = 102; 4 mice), with peak 18.8 ± 5.4%, time-to-peak 0.73 ± 0.19 s, and decay tau 0.93 ± 0.10 s.
- Astrocyte responses were unlikely to be neuropil contamination: mean absolute OGB-1 fluorescence increase was 44.4 ± 5.1 gray levels in astrocytes vs 13.3 ± 1.4 in neuropil ROIs (t test, p << 0.001).
Methods
- Urethane-anesthetized C57B6 mice (male and female, 2–4 months). Intrinsic optical signal imaging mapped hindlimb/forelimb cortex during mechanical limb stimulation; two-photon Ca²⁺ imaging used OGB-1 and SR101 in layers I–III of hindlimb somatosensory cortex.
- 355 astrocytes across 7 mice; stimuli were 0.5–1.0 s at 3, 10, or 100 Hz. Responses were thresholded as ΔF/F₀ >1 SD over baseline for ≥0.5 s; ANOVA with post hoc t tests and Bonferroni correction was used, and G/R ratio controlled for movement artifact in high-resolution endfoot imaging.
Limitations
- The paper does not present a formal limitations section; it notes significant intertrial variability in endfoot Ca²⁺ responses.
- Evident from the text: only a small subset of astrocytes responded (~5%; 18 responsive astrocytes), imaging was limited to anesthetized mice and layers I–III of hindlimb cortex, and the study reports correlations with hemodynamic onset rather than causal manipulation of astrocyte Ca²⁺ or blood flow.
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- Findingown data
Astrocyte Ca2+ transients had decay taus significantly longer than neuropil Ca2+ transients (1.07 ± 0.17 s vs 0.55 ± 0.04 s).
“Post hoc t tests using the Bonferroni correction revealed significantly shorter decay taus in neuropil ROIs (0.55 Ϯ 0.04 s) compared with astrocytes (1.07 Ϯ 0.17 s; p ϭ 0.011) and neurons (1.21 Ϯ 0.18 s; p ϭ 0.005).”
Quote in the paperNot a substantial claim - Findingcitation
The hemodynamic response (increased light reflectance/decreased absorbance) starts approximately 600-800 ms after stimulus onset.
“After the initial dip, increased blood flow (functional hyperemia) is associated with increased oxyhemoglobin concentration and blood volume, manifested in the IOS by increased light reflectance/decreased absorbance starting ϳ600 -800 ms after stimulus onset (Fig. 1 B) (Devor et al., 2003).”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Devor et al., 2003
Not checked in the free run.
- Findingown data
Astrocyte Ca2+ responses to brief contralateral hindlimb stimulation reached peak amplitude approximately 0.5 s after stimulus onset (mean time-to-peak 0.41 ± 0.11 s).
“peak amplitude ϳ0.5 s after stimulus onset”
- Also stated in: § Results · plain
“Whereas time-to-peak (from stimulus onset) means did not differ significantly between astrocytes (0.41 Ϯ 0.11 s), neurons (0.56 Ϯ 0.09 s), and neuropil (0.43 Ϯ 0.09 s; F (2,18) ϭ 0.67; p ϭ 0.52)”
Quote in the paperSubstantial claim - Also stated in: § Results · plain
- Findingown data
Eighteen of 355 astrocytes (5.07%) in layers I-III of hindlimb-activated somatosensory cortex showed an above-threshold stimulus-driven Ca2+ elevation after contralateral hindlimb stimulation.
“Eighteen astrocytes (5.07% of total astrocytes; an average of 5.08 Ϯ 1.28% per mouse) showed an above-threshold stimulus-driven Ca 2ϩ elevation after cHL stimulation.”
Quote in the paperSubstantial claim - Findingown data
The mean increase in absolute OGB-1 fluorescence in astrocytes during the 1.5 s after stimulation (44.4 ± 5.1 gray levels) was significantly greater than in neuropil ROIs (13.3 ± 1.4 gray levels).
“The mean increases in absolute OGB-1 fluorescence (peak Ϫ F o ) in astrocytes (44.4 Ϯ 5.1 gray levels) during the 1.5 s after stimulation was significantly greater than the mean increase in fluorescence in neuropil ROIs (13.3 Ϯ 1.4 gray levels) in the same images (t test, p Ͻ Ͻ 0.001).”
Quote in the paperSubstantial claim
- Findingown data
No limb other than the contralateral hindlimb induced a significant astrocyte Ca2+ response.
“No other limbs induced a significant Ca 2ϩ response.”
Quote in the paperNot a substantial claim - Study design and conductown data
The threshold criteria (change in Ca2+-induced fluorescence greater than one SD over baseline for at least 0.5 s) were effective for separating responsive cells from noise.
“Thresholds were set to identify cells where the change in Ca 2ϩ -induced fluorescence relative to baseline fluorescence was greater than one SD over baseline and remained above this criterion for at least 0.5 s (or three times the frame rate for frame rates Ͼ170 ms/frame).These criteria were found effective for separating responsive cells from noise.”
Quote in the paperSubstantial claim - Premisecitation
Different subpopulations of protoplasmic astrocytes possess varying glutamate-receptor complements.
“Furthermore, different subpopulations of protoplasmic astrocytes possess varying glutamate-receptor complements, and the shortand long-latency responses may reflect the activation of different glutamate receptors (Matthias et al., 2003;Wallraff et al., 2004;Jabs et al., 2005)”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites Matthias et al., 2003
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- cites Wallraff et al., 2004
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- cites Jabs et al., 2005
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- Premisecitation
Elevation of intracellular Ca2+ in astrocyte endfeet is sufficient to trigger rapid changes in vascular tone.
“Astrocytes also form a close physical and functional partnership with brain arterioles, because elevation of intracellular Ca 2ϩ in astrocyte endfeet is sufficient to trigger rapid changes in vascular tone (Zonta et al., 2003;Mulligan and MacVicar, 2004;Takano et al., 2006).”
Quote in the paperSubstantial claim0 of 3 sources checked- cites Zonta et al., 2003
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- cites Mulligan and MacVicar, 2004
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- cites Takano et al., 2006
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- Study design and conductown data
The G/R ratio confirms that the astrocyte and endfoot Ca2+ transient is selective to the Ca2+ indicator and cannot be explained by movement artifact.
“G/R ratios confirm that this transient is selective to the Ca 2ϩ indicator and cannot be explained by movement artifact, which would affect both OGB-1 and SR101 channels.”
Quote in the paperSubstantial claim - Premisecitation
Different subtypes of glutamate receptor are activated at different intensities of neuronal stimulation.
“Astrocyte Ca 2ϩ signals are graded according to the degree of neuronal activation, rather than all-or-none, and different subtypes of glutamate receptor are activated at different intensities of neuronal stimulation (Porter and McCarthy, 1996;Pasti et al., 1997;Latour et al., 2001;Lalo et al., 2006;Wang et al., 2006).”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites Porter and McCarthy, 1996
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- cites Pasti et al., 1997
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- cites Latour et al., 2001
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- Premisecitation
Recent in vivo work indicates that both short- and long-latency astrocyte Ca2+ signals can be observed in response to intracortical electrical stimulation.
“Consistent with these proposals, recent in vivo work indicates that both short-and long-latency astrocyte Ca 2ϩ signals can be observed in response to intracortical electrical stimulation (Gobel et al., 2007)”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Gobel et al., 2007
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- Interpretationown data
Astrocyte Ca2+ signals correlate with the onset of the hemodynamic response as measured by intrinsic signal imaging.
“correlate with the onset of the hemodynamic response as measured by intrinsic signal imaging.”
Quote in the paperSubstantial claim - Premisecitation
Astrocyte Ca2+ signals are graded according to the degree of neuronal activation, rather than all-or-none.
“Astrocyte Ca 2ϩ signals are graded according to the degree of neuronal activation, rather than all-or-none, and different subtypes of glutamate receptor are activated at different intensities of neuronal stimulation (Porter and McCarthy, 1996;Pasti et al., 1997;Latour et al., 2001;Lalo et al., 2006;Wang et al., 2006).”
Quote in the paperNot a substantial claim0 of 3 sources checked- cites Porter and McCarthy, 1996
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- cites Pasti et al., 1997
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- cites Latour et al., 2001
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- Interpretationown data
Astrocyte Ca2+ transients decayed more slowly than neuropil Ca2+ transients that presumably reflect presynaptic transients.
“The kinetics of astrocyte Ca 2ϩ transients were similar in rise and decay times to postsynaptic neuronal transients, but decayed more slowly than neuropil Ca 2ϩ transients that presumably reflect presynaptic transients.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Kerr et al., 2005
Not checked in the free run.
- Interpretationown data
Astrocyte responses were not caused by contamination from neuropil responses.
“These findings are inconsistent with the astrocyte responses being caused by contamination from neuropil responses.”
Quote in the paperSubstantial claim - Interpretationreasoning
A possible limitation of the previous study is that it uses an astrocyte-specific labeling method that uses prolonged incubation in high DMSO and pluronic detergent without the protection of the overlying dura.
“A possible limitation of the previous study is that it uses an astrocyte-specific labeling method that uses prolonged incubation in high DMSO and pluronic detergent without the protection of the overlying dura.”
Quote in the paperSubstantial claim - Interpretationreasoning
Astrocytes are potentially able to form an active partnership with neurons for rapid regulation of microvascular tone and neuron-astrocyte network properties.
“enabling them to potentially form an active partnership with neurons for rapid regulation of microvascular tone and neuron-astrocyte network properties.”
Quote in the paperSubstantial claim - Interpretationown data
Astrocyte Ca2+ transients had rise and decay times similar to postsynaptic neuronal transients.
“The kinetics of astrocyte Ca 2ϩ transients were similar in rise and decay times to postsynaptic neuronal transients, but decayed more slowly than neuropil Ca 2ϩ transients that presumably reflect presynaptic transients.”
Quote in the paperSubstantial claim - Interpretationown data
Sensory-driven astrocyte Ca2+ oscillations can occur at short latencies necessary to facilitate hyperemia to the active cortex.
“Our data demonstrates that sensory-driven astrocyte Ca 2ϩ oscillations, which have been proposed to modulate microvascular tone (Zonta et al., 2003;Mulligan and MacVicar, 2004;Takano et al., 2006), can occur at short latencies necessary to facilitate hyperemia to the active cortex.”
Quote in the paperSubstantial claim
- The quote only partly states this claim. 1
- May combine two claims. 4
- Classified as probably not a substantial claim. 4
The quote only partly states this claim.
Findingown dataAstrocyte and neuron Ca2+ transients did not differ significantly in decay tau (1.07 ± 0.17 s vs 1.21 ± 0.18 s, p = 0.59).
“The mean decay taus of astrocytes and neurons were not significantly different ( p ϭ 0.59).”
Quote in the paperNot a substantial claimMay combine two claims.
Findingown dataApproximately 20-30% of neurons and most neuropil ROIs in the same image planes showed Ca2+ responses above threshold criteria.
“Approximately 20 -30% of neurons and most neuropil ROIs in the same image planes showed Ca 2ϩ responses above threshold criteria.”
Quote in the paperNot a substantial claimProbably not a substantial claim: may not pass S3 (load-bearing).
PremisecitationMetabotropic glutamate receptors and glutamate uptake transporters on astrocytes have been implicated in the hemodynamic response to neuronal activity.
“and metabotropic glutamate receptors and glutamate uptake transporters on astrocytes have been implicated in the hemodynamic response to neuronal activity (Gurden et al., 2006;Takano et al., 2006).”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites Gurden et al., 2006
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- cites Takano et al., 2006
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May combine two claims.
Interpretationown dataAstrocytes can respond to sensory activity in a selective manner and process information on a subsecond time scale.
“These in vivo findings suggest that astrocytes can respond to sensory activity in a selective manner and process information on a subsecond time scale”
Quote in the paperSubstantial claimProbably not a substantial claim: may not pass S1 (asserted).
PremisecitationNeuron-to-astrocyte communication may be a key mediator of functional hyperemia.
“It has been suggested that neuron-to-astrocyte communication may be a key mediator of this functional hyperemia (Zonta et al., 2003;Takano et al., 2006)”
Quote in the paperNot a substantial claim0 of 2 sources checked- cites Zonta et al., 2003
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- cites Takano et al., 2006
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PremisecitationHyperemia begins ~600 ms after sensory stimulus onset and would require a rapid response from astrocytes.
“Previous evidence indicates that hyperemia begins ϳ600 ms after sensory stimulus onset and, thus, would require a rapid response from astrocytes (Kleinfeld et al., 1998;Devor et al., 2003).”
Quote in the paperSubstantial claim0 of 2 sources checked- cites Kleinfeld et al., 1998
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- cites Devor et al., 2003
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Classified as probably not a substantial claim. May combine two claims.
PremisecitationAstrocytes can communicate with neurons on a rapid subsecond time scale, and in vitro and in situ studies have shown that astrocyte Ca2+ transients and synaptic-like currents can be triggered by neuronal activity.
“The presence of ionotropic glutamate receptors and rapid transporter-mediated currents suggest that astrocytes can communicate with neurons on a rapid subsecond time scale, and in vitro and in situ studies have shown that astrocyte Ca 2ϩ transients and synaptic-like currents can be triggered by neuronal activity (Dani et al., 1992;Murphy et al., 1993;Porter andMcCarthy, 1995a,b, 1996;Bergles and”
Quote in the paperSubstantial claim0 of 3 sources checked- cites Dani et al., 1992
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- cites Murphy et al., 1993
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- cites Porter andMcCarthy, 1995a,b
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InterpretationcitationCareful examination of Gobel et al. data suggests that smaller, short-latency Ca2+ transients were also triggered by electrical stimulation in some astrocytes.
“although the authors note the large amplitude, long-lasting Ca 2ϩ oscillations that propagate throughout the glial network, careful examination of the data presented suggests that smaller, short-latency Ca 2ϩ transients were also triggered by electrical stimulation in some astrocytes.”
Quote in the paperNot a substantial claim0 of 1 sources checked- cites Gobel et al., 2007
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Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Astrocytes are sensitive to changes in neural activity and respond with increases in intracellular calcium levels.
“In vivo imaging studies of astrocytes have shown that astrocytes are sensitive to changes in neural activity and respond with increases in intracellular calcium levels (Wang et al., 2006; Winship et al., 2007).”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Winship et al., 2007
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- Authors
- Winship, I. R., Plaa, N., & Murphy, T. H.
- Affiliations
- University of British Columbia (CA)
- Venue
- Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2007-06-06
- Volume
- 27
- Issue
- 23
- Pages
- 6268-6272
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6672142
- OpenAlex
- W2054459050
- Semantic Scholar
- 9c442e4e61461e8b7b1b77e7f83d93c39f83a302
- Cited by
- 221
- References
- 32
- Citations by year
- 2025: 7 · 2024: 4 · 2023: 12 · 2022: 9 · 2021: 11 · 2020: 9 · 2019: 5 · 2018: 8 · 2017: 9 · 2016: 16 · 2015: 17 · 2014: 14 · 2013: 21 · 2012: 19
- FWCI
- 6.34
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Heart and Stroke Foundation of Canada
- Canadian Stroke Network
- Michael Smith Health Research BC
- Canadian Institutes of Health Research
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Keywords
- calcium oscillations, sensory evoked potentials, primary somatosensory cortex, hemodynamic response, astrocyte-neuron communication, cerebral microcirculation, sulforhodamine 101, intrinsic signal imaging, microvascular tone, neuronal activity
- MeSH terms
- Action Potentials, Animals, Astrocytes, Female, Hindlimb, Male, Mice, Inbred C57BL, Microcirculation, Neurons, Somatosensory Cortex, Time Factors, Calcium Signaling, Mice
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