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Departments of 1Geriatric Medicine, 2Cardiovascular Medicine, and 3Integrative Brain Science, Kyoto University Graduate School of Medicine, Kyoto 606-8501, Japan
Submitted 30 October 2003; accepted in final form 17 December 2003
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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; Lynch et al. 1983), long-term depression (Rose and Konnerth 2001; Sakurai 1990), electroencephalographic (EEG) rhythm generation (McCormick and Contreras 2001), and neural cell death (Choi 1995) are all dependent on intracellular Ca2+ increase. Yet, once intracellular Ca2+ is increased, one of such Ca2+-dependent events, but not the others, is specifically triggered. How can the versatility and specificity co-exist in the neural Ca2+ signaling? An emerging view related to this question is that Ca2+ channels and Ca2+-activated channels form functional complexes, and each complex may be dedicated to one particular function. It is classically known that a channel coupling composed of voltage-dependent Ca2+ channels (VDCCs) and small-conductance Ca2+-dependent K+ channels (SK channels) is responsible for spike-frequency adaptation, a Ca2+-dependent negative feedback regulation of membrane excitability (Sah 1996). A specific linkage of N-methyl-D-aspartate receptors (NMDARs) and large-conductance Ca2+-dependent K+ channels (big-K; BK channels) enables a synaptically triggered, extra-synaptic inhibition (Isaacson and Murphy 2001). Ca2+ inflow from NMDARs is known as a particularly suitable activator of ryanodine receptors (RyRs) in hippocampus pyramidal cell spines, suggesting a functional coupling between NMDARs and RyRs (Emptage et al. 1999). An intimate link is proposed between VDCCs and Ca2+-dependent cationic channels, which contributes to generation of spike afterdepolarization (Partridge and Valenzuela 1999). The Ca2+-activated Ca2+-release channels RyRs and IP3Rs appear to play unique roles in organizing such channel complex because these channels can be targets and donors of Ca2+ at the same time. Hence, the Ca2+ release from these channels may in turn activate a second target, thereby forming a functional triad instead of a coupling.
An interesting feature of such a functional triad involving inosiol-1,4,5-trisphosphate receptors (IP3Rs) would be that the intermediate member of the triad, the IP3R, is dependent not just on Ca2+ but also on IP3-mobilizing neurotransmitters. Recently, cooperative regulation of IP3Rs by Ca2+ and IP3 (Bezprozvanny et al. 1991; Finch et al. 1991; Iino 1990) has been increasingly recognized in neurons (Nakamura et al. 1999, 2000; Wang et al. 2000; Yamamoto et al. 2000, 2002a,b; Yang et al. 2002). Typically, a Ca2+-induced Ca2+ release (CICR) from IP3Rs has been described in hippocampus (Nakamura et al. 1999; Power and Sah 2002) and visual cortex pyramidal cells (Yamamoto et al. 2000) in which IP3Rs are activated beforehand by IP3 until their opening is finally triggered by action potential-induced Ca2+ inflow through VDCCs. We have proposed that a functional significance of this mode of IP3-assisted CICR may reside in its role in enhancement of spike-frequency adaptation (Yamamoto et al. 2002a). Because the target of this distinct type of CICR is not known, a functional triad consisting of VDCCs, IP3Rs, and the yet-unknown target has not been undoubtedly established to date. We have now identified SK channels as the target. This functional triad was switched on by IP3-mobilizing neurotransmitters and indeed enhanced spike-frequency adaptation in visual cortex pyramidal cells.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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All experiments were performed in accordance with the guiding principle of the Physiological Society of Japan and with the approval of the Animal Care Committee of Kyoto University Graduate School of Medicine. Slices (300 µm thick) of the visual cortex were prepared from Wistar rats (16–18 days old) with a microslicer DTK-1000 (Dosaka, Kyoto, Japan). Slices were kept at room temperature for 
60 min before experiments in normal medium composed (in mM) of 124 NaCl, 3.0 KCl, 2.5 CaCl2, 2.5 MgSO4, 1.3 NaH2PO4, 26 NaHCO3, and 10 glucose bubbled with a mixture of 95% O2-5% CO2. In some experiments, CNQX (10 µM) and bicuculline (10 µM) were added. The slices were placed in a recording chamber on the stage of an upright microscope (BX50WI, Olympus, Tokyo, Japan) with a x60 water-immersion objective. The chamber was continuously perfused with medium at room temperature (
25°C) bubbled with a mixture of 95% O2-5% CO2.
Electrophysiology
Whole cell recordings were made from the soma of visually identified pyramidal neurons located in layer 2/3 of the visual cortex. Recordings were continued only in cells that had the resting membrane potential below -55 mV. Patch pipettes (5–8 M
) were filled with an internal solution containing (in mM) 7 KCl, 144 K-gluconate, 10 HEPES, 2 MgATP, and 0.2 Na2GTP, pH adjusted to 7.3 with KOH. Capacitance was compensated almost fully. Series resistance was always 15–50 M and left uncompensated. The EPC-9 patch-clamp amplifier and program package PULSE-PULSEFIT (HEKA Electronics, Lambrecht, Germany) were used for data acquisition. For voltage-clamp recording (held at -55 mV), a short depolarization command to +10 mV for 5 ms was applied to evoke tail currents (IAHP), which would generate afterhyperpolarization (AHP) under current clamp (IAHP). IAHPs were recorded every 40–60 s and digitized at 5–10 kHz. We integrated IAHP from 20 to 200–500 ms after the step depolarization to calculate the charge transfer representing the medium AHP (mAHP). This charge transfer was adopted as the index for evaluating the magnitude of mAHPs. For current-clamp recording, a single action potential was evoked by a 3-ms depolarization current pulse (800 pA), and mAHP following the action potential was recorded. Trains of action potentials were evoked by injecting depolarizing currents (100–250 pA for 500 ms). Carbachol application depolarized recorded neurons by at most 5–10 mV, and we set the membrane potential back exactly to the resting level by passing hyperpolarizing currents. The current-clamp recording started 5 min after the application.
Drugs used
Depending on the purpose of experiments, we bath-applied one or more of the following drugs: apamin (100 nM; Alomone), carbachol (Cch; 10 µM), atropine (1 µM), thapsigargin (1 µM; Alomone), (RS)-3,5-dihydroxyphenylglycine (DHPG; 10 µM; Tocris), CNQX (10 µM; Tocris) and bicuculline (10 µM; Tocris), linopirdine (50 µM; Sigma), iberiotoxin (50 nM; Alomone). Heparin (low molecular weight, 4 mg/ml; Calbiochem) and ruthenium red (100 µM) were contained in the internal solution of patch pipettes and thereby injected intracellularly. For thapsigargin application, the recorded cells were preincubated for 20–60 min in medium containing thapsigargin. For Ca2+ imaging, the Ca2+ indicator Oregon Green 488 BAPTA-1 (50 µM; Molecular Probe) was injected intracellularly. Ni2+ (500 µM) was applied extracellularly. At this concentration, Ni2+ blocks all subtypes of VDCCs (Randall 1998). All the drugs were purchased from Nacalai (Kyoto, Japan) unless otherwise noted.
Ca2+ imaging
For Ca2+ imaging, neurons were filled with Oregon green 488 BAPTA-1 (50 µM), a Ca2+ indicator, through the patch pipette. Fluorescence images were acquired by a high-speed confocal laser-scanning microscope (Oz, Noran). Based on the fluorescence image, the time course of fluorescence intensity was calculated in several regions of interest (ROIs), which were selected over the nucleus (N), extranuclear soma (S), and the proximal dendrite (D). To examine Ca2+ transients in response to the depolarization command, 150 or 200 frames of image were collected at 120 Hz, and the increase in fluorescence intensity was averaged over each ROI within images. The fluorescence signals were subjected to background correction and were expressed as relative increases in fluorescence (
F/F) in comparison with the prestimulus fluorescence level (F). Recorded cells were held at -55 mV, and a depolarization step to +10 mV for 5 ms was given for each recording session.
Date analysis
Recorded data were analyzed with StatView. Data are expressed as means ± SE. Paired or unpaired t-test was used for statistics with the significance level set at P < 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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Under voltage clamp, the current that would produce AHP under current clamp (IAHP) was elicited in pyramidal neurons by a depolarization pulse. IAHP was integrated from 20 to 200 or 500 ms after the pulse termination to calculate the charge transfer carried by the middle part of IAHP that corresponds to the medium AHP (mAHP) (Sah 1996). IAHP had a single peak followed by a single exponential decay, which lasted 200 ms. IAHP was completely abolished by the selective SK channel antagonist apamin (Fig. 1A), thus reflecting mostly mAHP. The charge transfer was reduced to 7.1 ± 3.8% (n = 8, P < 0.0001) by apamin, confirming that IAHP was attributable largely to SK channels. After application of the muscarinic agonist Cch, a second slow component of IAHP emerged after the same fast component as observed without Cch, thereby enhancing the total charge transfer to 297 ± 21% (n = 40, P < 0.0001; Figs. 1B and 2). By co-application of apamin along with Cch, both the fast and slow components of IAHP were completely abolished (- 44.2 ± 7.7%, n = 15, P < 0.0001). In the presence of Cch and apamin, but not with apamin alone, a small, sustained inward current was observed after the depolarization pulse (Figs. 1B and 2). Co-application of the muscarinic receptor (mAchR) antagonist atropine with Cch completely prevented the Cch-induced emergence of the slow component, which is evidenced by reduction of the slow IAHP enhancement to 98.9 ± 1.1% (n = 7, Figs. 1C and 2) as compared with 297 ± 21% in the presence of Cch alone (P < 0.001).
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What role does the Ca2+ influx through VDCCs play in the dual activation of IAHP? Removal of the extracellular Ca2+ almost completely abolished both the fast and slow activations (Figs. 1D and 2). The charge transfer by IAHP was reduced to 15.9 ± 9.3% (n = 9, P < 0.0001) of control. IAHP was also sensitive to VDCC blockade by 500 µM Ni2+ with the charge transfer reduced to 5.0 ± 8.1% (n = 10, P < 0.0001, Fig. 2). These results indicate that Ca2+ influx through VDCCs is essential for generating both the fast and the Cch-induced, slow components of IAHP.
How did the slow IAHP component emerge with Cch application? Because mAchR activation by Cch will produce IP3, Ca2+ released through IP3R may keep SK channels activated for a longer period. To test this possibility, the IP3R blocker heparin was included in the patch solution. Heparin prevented the slow enhancement of IAHP in all the cells tested (67.3 ± 4.9%, n = 9, P < 0.0001; Fig. 3, A and D). Thapsigargin, a Ca2+ store depleter, also prevented this slow enhancement (67.3 ± 4.9%, n = 9, P < 0.0001; Fig. 3, B and D). Because Ca2+ influx might activate RyRs as well, we tested the effect of ruthenium red, a blocker of RyRs. But, the enhancement of IAHP due to Cch was 280 ± 44% with ruthenium red (n = 4, P < 0.0001; Fig. 3, C and D), which was not significantly different from the 297 ± 21% increase with Cch alone. These results indicate that Ca2+ release from IP3Rs, but not RyRs, is essential for emergence of the slow enhancement of IAHP. IP3 is produced by activation of type I metabotropic glutamate receptors (mGluRs) as well. The potent type-I-mGluR agonist DHPG indeed enhanced IAHP (to 356 ± 40%, n = 8, P < 0.0001; Fig. 3E), indicating that increase in IP3 is essential and sufficient for the slow activation of SK channels.
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By Ca2+ imaging, Ca2+ mobilization underlying the dual SK channel activation was investigated (Fig. 4). Prior to Cch application, [Ca2+]i elevation occurred immediately after the depolarization command and decreased gradually both in soma and proximal dendrite, thus consisting of just one phase of increase (Fig. 4C, black lines). This was observed in all the three ROIs (N, S, D in Fig. 4, A and C). After Cch application, by contrast, a delayed phase of [Ca2+]i increase emerged and overrode the initial phase in all the ROIs (Fig. 4C, red lines). The green lines in Fig. 4C indicate the subtractions between [Ca2+]i elevations with and without Cch, thus representing the newly emerged phase of [Ca2+]i increase after Cch application. Ca2+ increases at the peak of elevation, as expressed by percent of the prepulse level (F/F), were 44.3 ± 7.1% (N), 93.3 ± 10.4% (S), and 167.4 ± 14.9% (D) after Cch application, and significantly greater than before Cch application (N, 17.7 ± 1.1%, P < 0.005; S, 57.0 ± 8.1%, P < 0.0005; D, 124.2 ± 15.0%, P < 0.005; n = 12).
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), activates apamin-sensitive SK channels.
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As shown thus far, IP3R activation added a second slow phase of depolarization-induced SK currents to the first phase, which was evoked already without IP3R activation. The entire time course of SK currents was thereby prolonged, and the total outward charge transfer increased. We then tested whether such prolongation of SK currents really decreases membrane excitability after spike discharge. Under current clamp, Cch deepened and prolonged mAHP induced by a single action potential (Fig. 6A). The amplitude of mAHP was 4.46 ± 0.55 mV without Cch and became significantly larger with Cch (6.16 ± 0.52 mV; n = 5, P < 0.05; Fig. 6C). The time to peak of mAHP was also significantly longer with Cch (228 ± 15 ms) than without Cch (149 ± 10 ms, n = 5, P < 0.01). Intracellular injection of heparin curtailed this effect of Cch. With heparin intracellularly injected, the mAHP amplitude (2.18 ± 0.24 mV before Cch application) was not enlarged by Cch application (0.92 ± 0.3 mV, n = 5; Fig. 6B). Rather the mAHP amplitude was reduced, and a presumed spike afterdepolarization was overridden. Spike-induced calcium release from IP3Rs (IP3-assisted CICR) was thus suggested to play a critical part in the Cch-induced enlargement of mAHP.
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F/F), was significantly greater (74.2 ± 13.7%) than before Cch application (41.2 ± 4.1%, P < 0.05; n = 4). Thus spike-induced calcium release from IP3Rs was suggested to contribute to Cch-induced enhancement of mAHP during a single spike.
We then examined effects of Cch on repetitive spike firing. Depolarizing currents of longer duration (500 ms) were injected. On injection, all the neurons fired in the regular spiking fashion (McCormick et al. 1985). The current intensity was adjusted to evoke 8–10 action potentials for 500 ms. Cch application enhanced spike-frequency adaptation as previously reported (Yamamoto et al. 2002a) and diminished the number of action potentials by 1.6 ± 0.3 (n = 9, P < 0.01; Fig. 7A and B). Then by using the SK channel blocker apamin, it was studied whether this Cch-induced enhancement of spike-frequency adaptation depends on SK channels. Currents of the same intensity evoked a larger number of spikes (9.7 ± 0.62) in apamin-containing medium than in control medium (7.7 ± 0.62, P < 0.03, n = 10). Therefore the current intensity under apamin application was so reduced that much the same numbers of spikes could be evoked as in normal medium. To confirm the dependence of Cch-induced effects on SK channels, we first recorded spike firing under blockade of SK channels by apamin, and then Cch was further applied. Under SK channel blockade by apamin, Cch application failed to enhance spike-frequency adaptation, confirming our conclusion that Cch-induced enhancement of spike-frequency adaptation depends on SK channels. Cch application rather increased the number of action potentials by 1.8 ± 0.5 (n = 10, P < 0.001). This excitability increase is due likely to blockade of M channels by Cch (Marrion 1997) because the M channel blocker linopirdine slightly exaggerated the Cch-induced enhancement of spike-frequency adaptation (n = 8, data not shown). The BK channel blocker iberiotoxin failed to affect Cch-induced enhancement of spike-frequency adaptation (n = 7, data not shown), again supporting the conclusion that SK channels are the target of depolarization-induced calcium release enabled by mAchR activation.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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Spike-frequency adaptation is a typical example of Ca2+-mediated regulation of membrane excitability in which a class of Ca2+-activated K+ channels, SK channels, are activated by spike-induced increases in intracellular Ca2+, thereby stabilizing membrane excitability in a negative feedback fashion (Sah 1996). SK channels, activated voltage-independently and inactivated with a slow time course (Hirschberg et al. 1998), play the principle role in spike-frequency adaptation by evoking mAHP (Sah 1996). Because spike firing opens VDCCs and generate mAHP, it is naturally understood that Ca2+ entry through VDCCs will attenuate spike firing in a feedback manner (Sah and Davies 2000). The gain of this minimal feedback may not necessarily depend on the firing rate because the per spike Ca2+ increase here has been shown constant (Yamamoto et al. 2002a). As a second source of Ca2+ increase, IP3-induced Ca2+ released from IP3Rs (IICR) is also reported to open Ca2+-activated K+ channels including SK channels in midbrain (Fiorillo and Williams 1998, 2000; Morikawa et al. 2000) and neocortex neurons (Stutzmann et al. 2003). However, because IICR occurs depending on release of neurotransmitters that lead to IP3 synthesis but not on spike firing, a direct activation of SK channels by IICR cannot constitute a feedback regulation of spike firing. Also, an upregulation of SK channels by IICR would not slow down the time course of Ca2+ entry and therefore would not explain the associated emergence of the slow components of both Ca2+ increase and IAHP shown in the present experiments. As a third possibility, spike-triggered Ca2+ influx persuades RyRs to release Ca2+ [the conventional CICR (Llano et al. 1994; Verkratsky and Shmigol 1996)], which was documented to open Ca2+-activated K+ channels, including SK channels, in sympathetic neurons (Akita and Kuba 2000; Davies et al. 1996; Jobling et al. 1993). This conventional CICR could therefore boost the ability of spike-triggered Ca2+ influx to open SK channels activity-dependently. Some intracellular signals, such as cADP ribose or FK binding protein, are known to modulate RyRs in neurons (Berridge 1998; Higashida et al. 2001). However, these signals are not unequivocally shown to be mobilized by extracellular signals like neurotransmitters. Thus so far, a synaptic control cannot be held possible on spike firing regulation based on the conventional CICR.
Yet another form of CICR has been described in hippocampus (Nakamura et al. 1999; Power and Sah 2002) and neocortex pyramidal cells (Larkum et al. 2003; Yamamoto et al. 2000). Here, IP3Rs are initially primed by IP3 increase, and then a subsequent spike-induced inflow of Ca2+ triggers Ca2+ release from IP3Rs. This is a CICR by definition. But, Ca2+ is released from IP3Rs instead of RyRs. Also, this mode of CICR, called IP3-assisted CICR in Yamamoto et al. (2000, 2002a), is different from IICR that is triggered by increase in IP3 alone. The functional significance of IP3-assisted CICR seems to originate from the supra-linearity of the per spike Ca2+ increase during its occurrence (Yamamoto et al. 2002a). The present findings have shown that Ca2+ recruited by IP3-assisted CICR aimed at SK channels in pyramidal cells. A functional triad is thus established that consists of VDCCs, IP3Rs, and SK channels. With this triad, because of an activity-dependent Ca2+ release, the per spike Ca2+ increase may grow supra-linearly with the firing rate increased, resulting in a supra-linear increase in SK channel open probability. Thus the gain of spike-frequency adaptation will be modified activity-dependently. Such gain modifiability may enable a finer tuning of spike firing. More remarkably, this gain control is regulated synaptically by neurotransmitters leading to IP3 synthesis.
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ACKNOWLEDGMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGMENTSREFERENCES |
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GRANTS
This work was supported by Grants-in-Aid for Scientific Research and Center of Excellence Grant 12CE2006 from the Ministry of Education, Culture, Sports, Science and Technology of Japan.
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FOOTNOTES |
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Address for reprint requests and other correspondence: N. Kato, Dept. of Integrative Brain Science, Graduate School of Medicine, Kyoto University, 606-8501 Kyoto, Japan (E-mail: f50207{at}sakura.kudpc.kyoto-u.ac.jp).
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A. T. Gulledge and G. J. Stuart Cholinergic Inhibition of Neocortical Pyramidal Neurons J. Neurosci., November 2, 2005; 25(44): 10308 - 10320. [Abstract] [Full Text] [PDF]
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I. Ismailov, D. Kalikulov, T. Inoue, and M. J. Friedlander The Kinetic Profile of Intracellular Calcium Predicts Long-Term Potentiation and Long-Term Depression J. Neurosci., November 3, 2004; 24(44): 9847 - 9861. [Abstract] [Full Text] [PDF]
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