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Cited by 155Neuroscience and Neuropharmacology ResearchIon channel regulation and functionIon Channels and Receptors

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Parvalbumin Is a Mobile Presynaptic Ca2+Buffer in the Calyx of Held that Accelerates the Decay of Ca2+and Short-Term Facilitation

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Müller, Martin, Felmy, Felix, Schwaller, Beat, Schneggenburger, Ralf·2007·The Journal of Neuroscience
DOI 10.1523/jneurosci.5582-06.2007PMC PMC6673482
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Abstract

Presynaptic Ca 2+signaling plays a crucial role in short-term plasticity of synaptic transmission. Here, we studied the role of mobile endogenous presynaptic Ca 2+buffer(s) in modulating paired-pulse facilitation at a large excitatory nerve terminal in the auditory brainstem, the calyx of Held. To do so, we assessed the effect of presynaptic whole-cell recording, which should lead to the diffusional loss of endogenous mobile Ca 2+buffers, on paired-pulse facilitation and on intracellular Ca 2+concentration ([Ca 2+]i) transients evoked by action potentials. In unperturbed calyces briefly preloaded with the Ca 2+indicator fura-6F, the [Ca 2+]i transient decayed surprisingly fast (τ fast, ∼30 ms). Presynaptic whole-cell recordings made without additional Ca 2+buffers slowed the decay kinetics of [Ca 2+]i and paired-pulse facilitation (twofold to threefold), but the amplitude of the [Ca 2+]i transient was changed only marginally. The fast [Ca 2+]i decay was restored by adding the slow Ca 2+buffer EGTA (50–100 μ m) or parvalbumin (100 μ m), a Ca 2+-binding protein with slow Ca 2+-binding kinetics, to the presynaptic pipette solution. In contrast, the fast Ca 2+buffer fura-2 strongly reduced the amplitude of the [Ca 2+]i transient and slowed its decay, suggesting that the mobile endogenous buffer in calyces of Held has slow, rather than fast, binding kinetics. In parvalbumin knock-out mice, the decay of [Ca 2+]i and facilitation was slowed approximately twofold compared with wild-type mice, similar to what is observed during whole-cell recordings in rat calyces of Held. Thus, in young calyces of Held, a mobile Ca 2+buffer with slow binding kinetics, primarily represented by parvalbumin, accelerates the decay of spatially averaged [Ca 2+]i and paired-pulse facilitation.

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Figure1 Rapid decay of AP-induced [Ca 2 + ] i transients in unperturbed calyces of Held. A , Fluorescence image showing a calyx of Held that was preloaded with 80 -100 𝛍 M fura-6F during a brief ( ∼ 30 s) whole-cell recording (left image taken at 1 × 1 pixel binning; right image taken at 8 × 15 binning). Scale bar, 10 𝛍 m. B , Fluorescence signals (top gray traces) of the six superpixels marked in A (black dots in right image) and the resulting average fluorescence signal (superimposed black trace) during a single 100 Hz train of 10 stimuli. The bottom black trace represents the background-corrected average fluorescence signal. The F 355 values (gray circles) measured before and after the stimulation were linearly interpolated (black dotted line) and used to calculate the fluorescence ratio (see Materials and Methods). C , Average [Ca 2 + ] i transients elicited by single APs (average of n = 32traces; C1 ) or by 10 APs at 100 Hz (average of n = 4; C2 ) in a calyx preloaded with fura-6F. The decays of both [Ca 2 + ] i transients were fitted with double exponentials (red traces). D , Average [Ca 2 + ] i transients evoked by single APs ( D1 ) and by 10 APs at 100 Hz ( D2 ), as assessed during a continuous whole-cell recording with 100 𝛍 Mfura-6F of the same terminal as shown in A-C . For comparison, the corresponding [Ca 2 + ] i transients obtained after preloading ( C ) are shown as dotted traces. The insets depict presynaptic APs measured in response to single stimuli and 100 Hz trains. Data in A-D are from the same cell. E , Fast decay time constants ( 𝛕 fast ; left) and mean amplitudes (right) of single AP-evoked [Ca 2 + ] i transients recorded in n = 5rat calyces after preloading (open bar) andafterrepatching(graybar).Notethesignificant slowing after repatching ( p = 0.009). F , Fast decay time constants ( 𝛕 fast ; left) and amplitudes ([Ca 2 + ] i ; right) of [Ca 2 + ] i transients in response to the 100 Hz trains.
Figure1 Rapid decay of AP-induced [Ca 2 + ] i transients in unperturbed calyces of Held. A , Fluorescence image showing a calyx of Held that was preloaded with 80 -100 𝛍 M fura-6F during a brief ( ∼ 30 s) whole-cell recording (left image taken at 1 × 1 pixel binning; right image taken at 8 × 15 binning). Scale bar, 10 𝛍 m. B , Fluorescence signals (top gray traces) of the six superpixels marked in A (black dots in right image) and the resulting average fluorescence signal (superimposed black trace) during a single 100 Hz train of 10 stimuli. The bottom black trace represents the background-corrected average fluorescence signal. The F 355 values (gray circles) measured before and after the stimulation were linearly interpolated (black dotted line) and used to calculate the fluorescence ratio (see Materials and Methods). C , Average [Ca 2 + ] i transients elicited by single APs (average of n = 32traces; C1 ) or by 10 APs at 100 Hz (average of n = 4; C2 ) in a calyx preloaded with fura-6F. The decays of both [Ca 2 + ] i transients were fitted with double exponentials (red traces). D , Average [Ca 2 + ] i transients evoked by single APs ( D1 ) and by 10 APs at 100 Hz ( D2 ), as assessed during a continuous whole-cell recording with 100 𝛍 Mfura-6F of the same terminal as shown in A-C . For comparison, the corresponding [Ca 2 + ] i transients obtained after preloading ( C ) are shown as dotted traces. The insets depict presynaptic APs measured in response to single stimuli and 100 Hz trains. Data in A-D are from the same cell. E , Fast decay time constants ( 𝛕 fast ; left) and mean amplitudes (right) of single AP-evoked [Ca 2 + ] i transients recorded in n = 5rat calyces after preloading (open bar) andafterrepatching(graybar).Notethesignificant slowing after repatching ( p = 0.009). F , Fast decay time constants ( 𝛕 fast ; left) and amplitudes ([Ca 2 + ] i ; right) of [Ca 2 + ] i transients in response to the 100 Hz trains.CC-BY-NC-SA · From the PDF
Figure 2 TheslowCa 2 + buffers EGTA and parvalbumin restore the fast decay of AP-evoked [Ca 2 + ] i transients. A , AP-evoked [Ca 2 + ] i transient (average of n = 21sweeps)during presynaptic whole-cell recording of a calyx of Held with 100 𝛍 M fura-6F in the pipette solution. B , A [Ca 2 + ] i transient (average of n = 32) from another calyx, recorded with 100 𝛍 M fura-6F and 100 𝛍 M EGTA in the pipette solution. C , Example of a [Ca 2 + ] i transient (average of n = 18) measuredinaratcalyxwith100 𝛍 Mfura-6F and 100 𝛍 Mparvalbuminaddedtothepresynaptic pipette solution. Note that the [Ca 2 + ] i transients decay more rapidly in the presence of EGTA ( B ) and parvalbumin ( C ) compared with the no-added buffer condition ( A ). D , Example of a [Ca 2 + ] i transient (average of n = 10 sweeps) recorded with 50 𝛍 M fura-2. Note the small amplitude and the slow decay of [Ca 2 + ] i . In A-D , red lines are double-exponential ( A-C ) or single-exponential ( D ) fits of the [Ca 2 + ] i decay. E , Average fast decay time constants ( 𝛕 fast ) of AP-evoked [Ca 2 + ] i transients of calyces of Held recorded with 100 𝛍 Mfura-6F (open bars; n = 4 cells), 100 𝛍 M fura-6F and 100 𝛍 M EGTA (gray bars; n = 4 cells), 100 𝛍 M fura-6F and 50 𝛍 M parvalbumin (open red bar; n = 3 cells), 100 𝛍 M fura-6F and 100 𝛍 M parvalbumin (filled red bar; n = 4), or 50 𝛍 M fura-2 (blue bar; n = 5). The fura-2 data, which have an order of magnitude slower [Ca 2 + ] i decay, are plotted on the right y -axis. Note that 100 𝛍 M parvalbumin restored the rapid [Ca 2 + ] i decay observed in unperturbed calyces of Held (Fig. 1 E ) ( p = 0.4). F , Mean [Ca 2 + ] i amplitudes measured under the various Ca 2 + buffer conditions. The black and gray dotted lines in E and F represent the average ± SD of the corresponding values obtained in measurements of unperturbed calyces of Held (Fig. 1 E ).
Figure 2 TheslowCa 2 + buffers EGTA and parvalbumin restore the fast decay of AP-evoked [Ca 2 + ] i transients. A , AP-evoked [Ca 2 + ] i transient (average of n = 21sweeps)during presynaptic whole-cell recording of a calyx of Held with 100 𝛍 M fura-6F in the pipette solution. B , A [Ca 2 + ] i transient (average of n = 32) from another calyx, recorded with 100 𝛍 M fura-6F and 100 𝛍 M EGTA in the pipette solution. C , Example of a [Ca 2 + ] i transient (average of n = 18) measuredinaratcalyxwith100 𝛍 Mfura-6F and 100 𝛍 Mparvalbuminaddedtothepresynaptic pipette solution. Note that the [Ca 2 + ] i transients decay more rapidly in the presence of EGTA ( B ) and parvalbumin ( C ) compared with the no-added buffer condition ( A ). D , Example of a [Ca 2 + ] i transient (average of n = 10 sweeps) recorded with 50 𝛍 M fura-2. Note the small amplitude and the slow decay of [Ca 2 + ] i . In A-D , red lines are double-exponential ( A-C ) or single-exponential ( D ) fits of the [Ca 2 + ] i decay. E , Average fast decay time constants ( 𝛕 fast ) of AP-evoked [Ca 2 + ] i transients of calyces of Held recorded with 100 𝛍 Mfura-6F (open bars; n = 4 cells), 100 𝛍 M fura-6F and 100 𝛍 M EGTA (gray bars; n = 4 cells), 100 𝛍 M fura-6F and 50 𝛍 M parvalbumin (open red bar; n = 3 cells), 100 𝛍 M fura-6F and 100 𝛍 M parvalbumin (filled red bar; n = 4), or 50 𝛍 M fura-2 (blue bar; n = 5). The fura-2 data, which have an order of magnitude slower [Ca 2 + ] i decay, are plotted on the right y -axis. Note that 100 𝛍 M parvalbumin restored the rapid [Ca 2 + ] i decay observed in unperturbed calyces of Held (Fig. 1 E ) ( p = 0.4). F , Mean [Ca 2 + ] i amplitudes measured under the various Ca 2 + buffer conditions. The black and gray dotted lines in E and F represent the average ± SD of the corresponding values obtained in measurements of unperturbed calyces of Held (Fig. 1 E ).CC-BY-NC-SA · From the PDF
Image 3
CC-BY-NC-SA · From the PDF
Figure 4 Theinfluence of presynaptically added Ca 2 + buffers on paired-pulse facilitation and presynaptic [Ca 2 + ] i transients. A1 , Examples of presynaptic whole-cell calcium currents ( I Ca ) and EPSCs in response to paired voltage-clamp pulses of three different interstimulus intervals ( 𝚫 t ). A2 , Paired-pulse facilitation (mean ± SEM) of the recording shown in A1 . The data were fitted with an exponential function, with time constant 𝛕 = 93 ms. B , Paired-pulse facilitation in another cell pair, in which 100 𝛍 M EGTA was added to the presynaptic intracellular solution. Note the accelerated decay of facilitation. C , Mean facilitation (top) and presynaptic [Ca 2 + ] i (bottom) measured with 100 𝛍 M fura-6F added to the presynaptic pipette solution. D , Facilitation and presynaptic [Ca 2 + ] i transient in a cell pair recorded with 100 𝛍 M fura-6F and 75 𝛍 M EGTA in the presynaptic pipette solution. E , Facilitation and presynaptic [Ca 2 + ] i of a cell pair recorded with 50 𝛍 Mfura-2inthepresynapticpipettesolution. In A2-E , red lines are single- or double-exponential fits, with the time constants ( 𝛕 ) or fast time constants in the case of double-exponential fits ( 𝛕 fast ) as indicated. F , Average decay time constants of facilitation recorded under the various conditions of presynaptically added Ca 2 + buffer. Note the significant speeding of the decay of facilitation to ∼ 30 ms induced by 100 𝛍 M EGTA ( p = 0.029) or by 75 𝛍 M EGTA and 100 𝛍 M fura-6F ( p = 0.005). G , Average fast decay time constants of [Ca 2 + ] i transients recorded with 100 𝛍 M fura-6F without addedbuffer(redopenbar; n = 4cells) and with 75 𝛍 MEGTA( n = 9; red bar). The blue bar (right ordinate) shows the average decay time constant of [Ca 2 + ] i (monoexponential fit) measured with 50 𝛍 M fura-2 ( n = 3). EGTA (75 𝛍 M) significantly ( p = 0.0005) accelerated the decay of [Ca 2 + ] i compared with the no-added buffer condition (arrowhead). H , Amplitude of facilitation under the different conditions of presynaptically added Ca 2 + buffers. Note the significant decrease in facilitation in the presynaptic presence of 50 𝛍 M fura-2 (blue bar).
Figure 4 Theinfluence of presynaptically added Ca 2 + buffers on paired-pulse facilitation and presynaptic [Ca 2 + ] i transients. A1 , Examples of presynaptic whole-cell calcium currents ( I Ca ) and EPSCs in response to paired voltage-clamp pulses of three different interstimulus intervals ( 𝚫 t ). A2 , Paired-pulse facilitation (mean ± SEM) of the recording shown in A1 . The data were fitted with an exponential function, with time constant 𝛕 = 93 ms. B , Paired-pulse facilitation in another cell pair, in which 100 𝛍 M EGTA was added to the presynaptic intracellular solution. Note the accelerated decay of facilitation. C , Mean facilitation (top) and presynaptic [Ca 2 + ] i (bottom) measured with 100 𝛍 M fura-6F added to the presynaptic pipette solution. D , Facilitation and presynaptic [Ca 2 + ] i transient in a cell pair recorded with 100 𝛍 M fura-6F and 75 𝛍 M EGTA in the presynaptic pipette solution. E , Facilitation and presynaptic [Ca 2 + ] i of a cell pair recorded with 50 𝛍 Mfura-2inthepresynapticpipettesolution. In A2-E , red lines are single- or double-exponential fits, with the time constants ( 𝛕 ) or fast time constants in the case of double-exponential fits ( 𝛕 fast ) as indicated. F , Average decay time constants of facilitation recorded under the various conditions of presynaptically added Ca 2 + buffer. Note the significant speeding of the decay of facilitation to ∼ 30 ms induced by 100 𝛍 M EGTA ( p = 0.029) or by 75 𝛍 M EGTA and 100 𝛍 M fura-6F ( p = 0.005). G , Average fast decay time constants of [Ca 2 + ] i transients recorded with 100 𝛍 M fura-6F without addedbuffer(redopenbar; n = 4cells) and with 75 𝛍 MEGTA( n = 9; red bar). The blue bar (right ordinate) shows the average decay time constant of [Ca 2 + ] i (monoexponential fit) measured with 50 𝛍 M fura-2 ( n = 3). EGTA (75 𝛍 M) significantly ( p = 0.0005) accelerated the decay of [Ca 2 + ] i compared with the no-added buffer condition (arrowhead). H , Amplitude of facilitation under the different conditions of presynaptically added Ca 2 + buffers. Note the significant decrease in facilitation in the presynaptic presence of 50 𝛍 M fura-2 (blue bar).CC-BY-NC-SA · From the PDF
Figure 5 AP-induced presynaptic [Ca 2 + ] i transients decay slowly in parvalbumin knockout mice. A , B , Example of [Ca 2 + ] i transients in a calyx of Held from a PV -/ -mouse ( A ) and from a wild-type (wt) mouse ( B ). The decay of the [Ca 2 + ] i transients were fitted with doubleexponential functions (gray traces). C , D , Average fast decay time constants ( 𝛕 fast ; C ) and average amplitudes ([Ca 2 + ] i ; D ) of [Ca 2 + ] i transients elicited by single APs in PV -/ -(gray bars; n = 11cells) and in wild-type (white bars; n = 7cells) cells. Note the significant slowing ( p = 0.0005) of the [Ca 2 + ] i transients in PV -/ -mice, whereas the [Ca 2 + ] i amplitudes were not significantly different ( p = 0.42).
Figure 5 AP-induced presynaptic [Ca 2 + ] i transients decay slowly in parvalbumin knockout mice. A , B , Example of [Ca 2 + ] i transients in a calyx of Held from a PV -/ -mouse ( A ) and from a wild-type (wt) mouse ( B ). The decay of the [Ca 2 + ] i transients were fitted with doubleexponential functions (gray traces). C , D , Average fast decay time constants ( 𝛕 fast ; C ) and average amplitudes ([Ca 2 + ] i ; D ) of [Ca 2 + ] i transients elicited by single APs in PV -/ -(gray bars; n = 11cells) and in wild-type (white bars; n = 7cells) cells. Note the significant slowing ( p = 0.0005) of the [Ca 2 + ] i transients in PV -/ -mice, whereas the [Ca 2 + ] i amplitudes were not significantly different ( p = 0.42).CC-BY-NC-SA · From the PDF
Figure 6 Paired-pulse facilitation decays slowly at the calyx of Held of parvalbumin knock-out mice. A1 , Representative EPSCs in response to pulse pairs at three different interstimulus intervals ( 𝚫 t ) in a PV -/ -cell, recorded at 0.6 mM extracellular [Ca 2 + ]. A2 , Mean facilitation as a function of the interstimulus interval of the PV -/ -cell shown in A1 ( n = 15 repetitions). The data were fitted by an exponential function, with a time constant of 77 ms. B , Paired-pulse facilitation in a cell from a wild-type (wt) mouse ( n = 17 repetitions). Note the fast decay of paired-pulse facilitation, with a time constant of 17 ms in this cell. C , Average decay time constants of paired-pulse facilitation obtained in n = 8 cells from PV -/ -mice (gray bar), and in n = 7 cells from wild-type mice (white bar). Note the significantly ( p = 0.039) slower decay of paired-pulse facilitation in PV -/ -mice. D , The amplitude of paired-pulse facilitation was unchanged between wild-type mice (open bar; n = 7 cells) and PV -/ -mice (gray bar; n = 8 cells; p = 0.96).
Figure 6 Paired-pulse facilitation decays slowly at the calyx of Held of parvalbumin knock-out mice. A1 , Representative EPSCs in response to pulse pairs at three different interstimulus intervals ( 𝚫 t ) in a PV -/ -cell, recorded at 0.6 mM extracellular [Ca 2 + ]. A2 , Mean facilitation as a function of the interstimulus interval of the PV -/ -cell shown in A1 ( n = 15 repetitions). The data were fitted by an exponential function, with a time constant of 77 ms. B , Paired-pulse facilitation in a cell from a wild-type (wt) mouse ( n = 17 repetitions). Note the fast decay of paired-pulse facilitation, with a time constant of 17 ms in this cell. C , Average decay time constants of paired-pulse facilitation obtained in n = 8 cells from PV -/ -mice (gray bar), and in n = 7 cells from wild-type mice (white bar). Note the significantly ( p = 0.039) slower decay of paired-pulse facilitation in PV -/ -mice. D , The amplitude of paired-pulse facilitation was unchanged between wild-type mice (open bar; n = 7 cells) and PV -/ -mice (gray bar; n = 8 cells; p = 0.96).CC-BY-NC-SA · From the PDF
Figure 7 Amodified single-compartment model of Ca 2 + signaling at the calyx of Held. An AP-evoked, spatially averaged [Ca 2 + ] i transient was simulated either in the absence of a slow Ca 2 + buffer (gray trace) or in the presence of 50 𝛍 M parvalbumin (PV). See Materials and Methods for the parameters used in the simulation. The inset shows the simulated [Ca 2 + ] i traces at increased time resolution. The simulated [Ca 2 + ] i transient in the absence of parvalbumin(graytraces)waswellfittedbyasingle-exponentialfunction,withtimeconstant 𝛕 = 78 ms.Inthepresenceof50 𝛍 Mparvalbumin, the initial decay of [Ca 2 + ] i wasaccelerated, and the decay of [Ca 2 + ] i was now best fit by a double-exponential function, with fast and slow time constants of 31 and 1310 ms, respectively. Note that the combination of a low endogenous Ca 2 + buffer capacity ( 𝛋 s = 40), a fast Ca 2 + extrusion rate ( 𝛄 = 500 s -1 ), and the presence of a Ca 2 + buffer with slow binding kinetics result in an extremely fast initial decay of spatially averaged [Ca 2 + ] i .
Figure 7 Amodified single-compartment model of Ca 2 + signaling at the calyx of Held. An AP-evoked, spatially averaged [Ca 2 + ] i transient was simulated either in the absence of a slow Ca 2 + buffer (gray trace) or in the presence of 50 𝛍 M parvalbumin (PV). See Materials and Methods for the parameters used in the simulation. The inset shows the simulated [Ca 2 + ] i traces at increased time resolution. The simulated [Ca 2 + ] i transient in the absence of parvalbumin(graytraces)waswellfittedbyasingle-exponentialfunction,withtimeconstant 𝛕 = 78 ms.Inthepresenceof50 𝛍 Mparvalbumin, the initial decay of [Ca 2 + ] i wasaccelerated, and the decay of [Ca 2 + ] i was now best fit by a double-exponential function, with fast and slow time constants of 31 and 1310 ms, respectively. Note that the combination of a low endogenous Ca 2 + buffer capacity ( 𝛋 s = 40), a fast Ca 2 + extrusion rate ( 𝛄 = 500 s -1 ), and the presence of a Ca 2 + buffer with slow binding kinetics result in an extremely fast initial decay of spatially averaged [Ca 2 + ] i .CC-BY-NC-SA · From the PDF

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Metadata

Authors
Müller, M., Felmy, F., Schwaller, B., & Schneggenburger, R.
Affiliations
  • École Polytechnique Fédérale de Lausanne (CH)
  • Ludwig-Maximilians-Universität München (DE)
  • University of Fribourg (CH)
ORCID
Venue
The Journal of Neuroscience
Publisher
Society for Neuroscience
Published
2007-02-28
Volume
27
Issue
9
Pages
2261-2271
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
DOI
10.1523/jneurosci.5582-06.2007
PMC
PMC6673482
OpenAlex
W1975952480
Cited by
155
References
46
Citations by year
2026: 4 · 2025: 4 · 2024: 3 · 2023: 7 · 2022: 4 · 2021: 7 · 2020: 4 · 2019: 5 · 2018: 7 · 2017: 1 · 2016: 8 · 2015: 9 · 2014: 11 · 2013: 10 · 2012: 8
FWCI
5.97
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
  • Zurich Open Repository and Archive (University of Zurich)
Funders
  • National Science Foundation
  • Deutsche Forschungsgemeinschaft (TP B1)
  • Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung (100400, 3100A0)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
  • Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
Keywords
parvalbumin, calyx of Held, paired-pulse facilitation, short-term plasticity, calcium transients, fura-2, EGTA, auditory brainstem, excitatory synapses
MeSH terms
Animals, Brain Stem, Calcium, Calcium-Binding Proteins, Mice, Inbred C57BL, Synaptic Transmission, Neuronal Plasticity, Parvalbumins, Rats, Wistar, Receptors, Presynaptic, Mice, Knockout, Patch-Clamp Techniques, Mice, Rats, In Vitro Techniques

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