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NEUROSCIENCE |
1 Department of Neurophysiology, University of Tokyo Graduate School of Medicine, Tokyo 113-0033, Japan
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(Received 19 January 2007;
accepted after revision 28 February 2007;
first published online 1 March 2007)
Corresponding author T. Takahashi: Department of Neurophysiology, University of Tokyo Graduate School of Medicine, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan. Email: ttakahas{at}mail.doshisha.ac.jp
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Introduction |
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An important factor determining the maximal frequency of synaptic transmission is the presynaptic action potential duration, which becomes shorter during the second postnatal week (Taschenberger & von Gersdorff, 2000; Fedchyshyn & Wang, 2005). Developmental changes in presynaptic Na+ currents (Leão et al. 2005) can contribute to shortening of presynaptic action potential duration. However, presynaptic K+ currents (IpK) might also undergo developmental change and contribute to the action potential shortening. Developmental changes in K+ currents have been reported in postsynaptic neurons (Harris et al. 1988; O'Dowd et al. 1988; Gurantz et al. 1996; Gurantz et al. 2000; Riazanski et al. 2001; Hattori et al. 2003). However, little is known about developmental changes in K+ currents at the nerve terminal. In the present study, we addressed this issue by directly recording K+ currents from the calyx of Held presynaptic terminals of developing rats.
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Methods |
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All experiments were performed in accordance with the guideline of the Physiological Society of Japan. Brainstem slices were prepared from P7–21 Wistar rats as previously described (Forsythe & Barnes-Davies, 1993). Briefly, the rat was decapitated under halothane anaesthesia and the brain was quickly removed. Transverse slices (150–200 µm thick) containing MNTB were cut using a tissue slicer (ZERO-1; Dosaka, Kyoto, Japan). Slices were maintained in artificial cerebrospinal fluid (aCSF) at 37°C for 30–45 min and subsequently maintained at room temperature. MNTB principal cells and calyces were visually identified using a 60x water immersion objective lens (Olympus, Tokyo, Japan) attached to an upright microscope (Axioskop; Zeiss, Oberkochen, Germany).
The standard aCSF contained (mM): 125 NaCl, 2.5 KCl, 26 NaHCO3, 1.25 NaH2PO4, 2 CaCl2, 1 MgCl2, 10 glucose, 3 myo-inositol, 2 sodium pyruvate and 0.5 ascorbic acid, pH 7.4 when bubbled with 95% O2 and 5% CO2. For recording K+ currents, the aCSF contained tetrodotoxin (TTX; 1 µM) (Wako, Osaka, Japan), and the pipette solution contained (mM): 97.5 potassium gluconate, 32.5 KCl, 10 Hepes, 5 EGTA, 1 MgCl2, 12 Na2 phosphocreatine, 2 ATP-Mg and 0.5 GTP-Na (295–305 mosmol l–1, pH 7.3 adjusted with KOH; final K+ concentration, 143.5 mM). Presynaptic current-clamp recordings were made using the same pipette solution. In the majority of whole-cell K+ current recordings (Figs 2, 3, 4 and 5), to reduce driving force of K+, we replaced potassium gluconate (97.5 mM) in the pipette solution by equimolar N-methyl-D-glucamine gluconate (pH adjusted to 7.3 with gluconate; final internal K+ concentration, 32.5 mM); otherwise the amplitude of IpK often exceeded the range of amplifier (±20 nA) when a command potential above +20 mV was given. In this low-K+ pipette solution, the reversal potential of K+ currents was –66 mV. For recording BK currents (Fig. 3) and action potentials (Fig. 7), EGTA concentration in the pipette solution was reduced to 0.2 mM. Presynaptic Na+ currents (IpNa; Supplemental Fig. 1) were recorded with a low-Na+ aCSF containing (mM): 20 NaCl, 110 N-methyl-D-glucamine Cl, 20 tetraethylammonium (TEA) Cl, 2.5 KCl, 10 Hepes, 10 glucose, 2 BaCl2, 0.1 CdCl2 (pH 7.3 adjusted with HCl) and with a pipette solution containing (mM): 110 CsCl, 20 TEA, 10 Hepes, 10 EGTA, 1 MgCl2, 5 tris-pohsphocreatine, 2 ATP-Mg, 0.5 GTP-Na (295–305 mosmol l–1, pH adjusted to 7.3 with CsOH). The liquid junction potentials between the pipette solutions and aCSF were +10 mV for potassium gluconate solution, +7 mV for N-methyl-D-glucamine gluconate solution and –3 mV for CsCl solution, which were not corrected for unless otherwise noted. Drugs were applied to aCSF perfusing slices at the rate of 1.0–1.5 ml min–1. TEA and 4-aminopyridine (4-AP) were purchased from Tokyo Kasei Kogyo (Tokyo, Japan) and Wako, respectively. The synthetic peptides margatoxin (MgTX) and iberiotoxin (IbTX) were from Peptide Institute (Osaka, Japan). All other chemicals and salts were from Nacalai (Kyoto, Japan), Sigma or Wako.
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Whole-cell patch-clamp recordings were made from presynaptic calyceal terminals. The pipette resistance was 4.5–7.0 M
. Immediately after making a whole-cell patch, the access resistance was 6–15 M, which was routinely compensated by 80%. We monitored access resistance throughout the recording and excluded the data from analysis if measured access resistance changed by ±20%. Voltage-clamp recordings were made using a patch-clamp amplifier (Axopatch-1D or -200B; Axon Instruments, Union City, CA, USA). Presynaptic currents were elicited by depolarizing command pulses in a stepwise manner from a holding potential of –80 mV. Leak currents in whole-cell recordings were subtracted by the scaled pulse (P/8) protocol. The current amplitude was measured at 10 ms after the command pulse onset for IpK, and at the peak value for IpNa. To estimate the IpK density (Figs 2B and 4), the IpK amplitude was corrected for the error caused by the series resistance remaining after compensation, by scaling a factor
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) voltage follower. Presynaptic action potentials were evoked by a depolarizing current injection via recording pipettes or afferent fibre stimulation using a monopolar glass pipette. Records were low-pass-filtered at 5 kHz and digitized at 20–50 kHz using an analog to digital converter (Digidata 1320A) with pCLAMP8.2/9.1 software (Axon Instruments). All experiments were carried out at room temperature (25–27°C).
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Results |
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Figure 1A illustrates action potentials evoked in calyceal presynaptic terminals by afferent fibre stimulation at different postnatal periods. During postnatal development from P7 to P14 the action potential duration became markedly shorter as previously reported (Taschenberger & von Gersdorff, 2000; Fedchyshyn & Wang, 2005). However, no further change was observed from P14 to P21. The mean action potential half-width was 487 ± 29 µs at P7–8 (n = 9), 244 ± 6 µs at P13–15 (n = 9) and 279 ± 9 µs at P19–21 (n = 5). During postnatal development from P7 to P21, neither the action potential amplitude nor resting membrane potential significantly changed.
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Because of large current amplitudes, the IpK amplitude often exceeded the amplifier range (±20 nA) when a command potential above +20 mV was given, particularly in more mature calyces. To improve voltage-clamp performance, we reduced IpK amplitudes by reducing K+ concentration in recording pipette solutions by 75% (see Methods). In this low [K+]i (32.5 mM) solution, IpK could be recorded, for depolarizing command pulses of up to +40 mV. At +40 mV the IpK amplitude was 3.7 ± 0.5 nA at P7–8 (n = 8) and 14.1 ± 1.0 nA at P13–15 (n = 9) (Fig. 2A), which were corrected for series resistance (see Methods) to be 4.2 ± 0.7 nA at P7–8 and 24.7 ± 3.9 nA at P13–15. During development the membrane capacitance of calyceal terminal increased from 9.9 ± 1.4 pF (n = 8) to 16.7 ± 1.5 pF (n = 9) (Fig. 2B) because of an increase in the surface membrane area (Wimmer et al. 2006). The K+ current densities, estimated from the corrected IpK amplitude at +40 mV divided by nerve terminal capacitance, were 0.46 ± 0.08 nA pF–1 at P7–8 and 1.51 ± 0.02 nA pF–1 at P13–15, indicating a 3.3-fold increase during the second postnatal week.
Developmental changes in individual K+ current components
We next asked which K+ current component is responsible for this developmental increase in IpK, as K+ currents in the calyx nerve terminal are composed of multiple components (Ishikawa et al. 2003). The main component is sensitive to 4-aminopyridine (4-AP), and comprises the high-voltage-activated (HVA) and tetraethylammonium (TEA)-sensitive Kv3 currents, and the low-voltage-activated (LVA) and margatoxin (MgTX)-sensitive Kv1 currents. The 4-AP-insensitive minor component comprises Ca2+-induced large-conductance K+ (BK) currents, and as yet unidentified slowly activating K+ currents.
4-AP (5 mM) blocked a large proportion of IpK at P7–8 as at P13–15 (Fig. 3A). After 4-AP application, the high-voltage-activated Ca2+ currents appeared as inward currents, which had been masked by larger outward K+ currents (Ishikawa et al. 2003). The amplitude of Ca2+ currents remained similar during the second postnatal week (data not shown; see also Fedchyshyn & Wang, 2005). Thus the developmental increase in IpK was caused predominantly by an increase in the 4-AP-sensitive component. The BK channel-specific blocker iberiotoxin (IbTX; 100 nM) attenuated outward currents remaining in the presence of 4-AP (Fig. 3B). The density of BK currents at +20 mV, estimated from the IbTX-sensitive difference currents, was 48 ± 12 pA pF–1 at P7–8 (n = 5) and 40 ± 12 pA pF–1 at P13–15 (n = 5) (Fig. 3C). Thus BK current density remained similar during the second postnatal week. The rise time (10–90%) of BK currents at P13–15 (1.5 ± 0.2 ms, n = 5) was not significantly different from that at P7–8 (1.8 ± 0.1 ms, n = 5, P = 0.20).
Parallel developmental changes in Kv3 and Kv1 currents in the nerve terminal
After blocking Ca2+ currents and BK currents with Cd2+ (100 µM), K+ currents were pharmacologically dissected. Bath-application of TEA (1 mM) attenuated K+ currents (Fig. 4A), and additional application of the scorpion peptide MgTX (10 nM) further attenuated the K+ currents. Currents remaining after applications of Cd2+ (100 µM), TEA (1 mM) and MgTX (10 nM) showed delayed rectifying properties (Fig. 4Ac) and were blocked by 10 mM TEA (Ishikawa et al. 2003), suggesting that they were K+ currents. Because of a lack of type-specific K+ channel blocker, we could not identify these currents. From these experiments the 1 mM TEA-sensitive Kv3 and MgTX-sensitive Kv1 components were isolated as difference currents. In this protocol, changing the order of blocker applications has no effect on the amplitude of difference currents, excluding an overlap in their blocking effects (Ishikawa et al. 2003). It also argues against possible errors arising from current subtraction, such as time-dependent change in series resistance or current amplitude-dependent change in the voltage-clamp condition. The TEA-sensitive Kv3 component underwent a 3-fold increase in density from P7–8 to P13–15 (Table 1). Similarly the MgTX-sensitive Kv1 component underwent a 3.1-fold increase, and the remaining currents underwent a 2.2-fold increase in densities from P7–8 to P13–15. Consequently, the proportion of Kv3 and Kv1 conductance relative to total K+ conductance remained essentially the same during the second postnatal week (Fig. 4B). When compared at the maximal conductance given by the sigmoid fits, the Kv3 proportion was 58 ± 2% of total K+ conductance (Gtotal) at P7–8 (n = 8) and 55 ± 5% at P14–15 (n = 6), whereas the Kv1 proportion was 24 ± 2% at P7–8 and 28 ± 4% at P14–15. The activation curves of Kv3 also remained essentially the same during development. Although the half-activation voltage of Kv1 currents slightly shifted toward positive potential, this difference was statistically insignificant (Table 1).
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K+ currents in outside-out patch membrane excised from calyces
Further to attain optimal voltage-clamp performance we recorded K+ currents in outside-out patches excised from calyx nerve terminals at P7–8 and P13–15 (Fig. 6A). K+ currents were observed in all patches examined. The K+ current amplitude in excised patches was 248 ± 59 pA at P7–8 (n = 13) and 610 ± 166 pA at P13–15 (n = 10), indicating a 2.5-fold increase during development, which is comparable to the developmental increase in the K+ current density in whole-cell recordings (Fig. 2B). Consistent with whole-cell recordings, the activation kinetics of K+ currents in excised patches became faster during the second postnatal week, with the rise time (10–90%) at 0 mV being 4.6 ± 0.4 ms at P7–8 (n = 9) and 2.8 ± 0.4 ms at P13–15 (n = 8) (P < 0.01) (Fig. 6B). In excised patches, despite better voltage-clamp conditions, the rise time of K+ currents was slower than that of whole-terminal IpK in both age groups (paired Student's t test, P < 0.03). Similar phenomena have been reported for K+ currents (Scannevin & Trimmer, 1997; Maguire et al. 1998) and Na+ currents (Shcherbatko et al. 1999; Leão et al. 2005), and are thought to arise from a cytoskeletal deformation by patch excision (Scannevin & Trimmer, 1997; Maguire et al. 1998; Shcherbatko et al. 1999).
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Functional outcome of the developmental increase in Kv1 and Kv3 currents
We next investigated the functional outcome of the developmental changes in presynaptic Kv3 and Kv1 currents. Action potentials were evoked by a train of fibre stimulations at room temperature. At P7–8, presynaptic action potentials followed inputs up to 200 Hz (30 stimuli), but started to show failures at 300 Hz (Fig. 7). At P13–15, however, presynaptic spikes followed afferent inputs up to 400 Hz with no failure. Although TEA (1 mM) blocks both Kv3 and BK channels (Coetzee et al. 1999), the BK channel-specific blocker IbTX (100 nM) had no effect on the spiking fidelity either at P7–8 or P13–15. Furthermore, raising EGTA concentration in recording pipettes to 5 mM had no effect on the spiking fidelity. Irrespective of whether IbTX was present, TEA (1 mM) markedly increased failures at 400 Hz at P13–15 (n = 5, P < 0.01). However, this effect of TEA was less significant at P7–8 (Fig. 7B and C). In the presence of TEA spiking fidelity at P7–8 calyces was similar to that at P13–15 calyces (Fig. 7C), suggesting that developmental changes in Kv3 currents contribute to the establishment of high-fidelity presynaptic spiking in response to high-frequency inputs. We next investigated whether the developmental changes in Kv1 currents contribute to action potential generation in calyceal nerve terminals. A strong sustained presynaptic depolarization (100 ms) by a current injection (up to 240 pA) evoked only several action potentials at the beginning of the depolarization at P13–15 calyces (3.7 ± 1.1, n = 5) (Fig. 8A), in all calyces examined as previously reported (Ishikawa et al. 2003). In contrast, at P7–8 calyces, action potentials occurred in a burst (21.8 ± 2.5, n = 6) throughout the depolarization (Fig. 8A). The threshold current for action potential generation increased from 73 ± 10 pA at P7–8 (n = 6) to 123 ± 12 pA at P13–15 (n = 6, P < 0.01) (Fig. 8B). After blocking Kv1 channels with MgTX, these age differences disappeared. In the presence of MgTX (10 nM), a sustained depolarization gave rise to a burst of action potentials in P13–15 calyces (Fig. 8A, see also Ishikawa et al. 2003). The number of spikes generated by a given current was similar to that in P7–8 calyces (Fig. 8B). Furthermore, the firing threshold for calyces was similar between P7–8 and P13–15. These results suggest that a developmental increase in Kv1 currents raises firing threshold and converts the spiking behaviour of the nerve terminal from tonic to phasic.
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Discussion |
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Developmental changes in presynaptic K+ currents
During embryonic and postnatal development, Kv3 channels transcripts are upregulated in various CNS regions in rats (Perney et al. 1992; Gurantz et al. 2000), as well as in Xenopus (Gurantz et al. 2000). Expression of Kv1 channels also increases during development in culture (Gurantz et al. 1996; Grosse et al. 2000). In line with these reports, at the calyx of Held nerve terminal, both Kv3 and Kv1 whole-terminal currents underwent a 3-fold increase in density during the second postnatal week. Consistently, K+ currents recorded from patches excised from calyceal terminals underwent a 2.5-fold increase in density during the second postnatal week. In contrast, BK currents, which play little role in synaptic transmission at the calyx of Held (Ishikawa et al. 2003), did not undergo developmental change at this nerve terminal, unlike in cerebral (Kang et al. 1996) and cerebellar (Kang et al. 1996; Muller et al. 1998) neuronal somata. In agreement with our observations, the number of Kv3.1 immunogold particles, which are predominantly located on the non-synaptic side of calyceal terminals, undergoes 4-fold increase from P9 to P16 (Elezgarai et al. 2003).
The rise time of K+ currents became markedly faster during development at the calyx of Held, as in cultured Xenopus spinal neurons (Harris et al. 1988; O'Dowd et al. 1988). Although both Kv1 and Kv3 currents underwent developmental acceleration in activation kinetics, Kv3 currents have much faster rise time and higher density than Kv1 currents at +40 mV, to which action potentials normally reach. Therefore Kv3 currents are likely to determine the rise time of total IpK. The developmental acceleration in Kv3 currents was not secondary to changes in their voltage dependence (Fig. 5), unlike the modulatory effect of casein kinase on the voltage dependence of Kv3 channel kinetics (Macica & Kaczmarek, 2001). Kv3 channels are classified into four subtypes having different activation kinetics (Rudy et al. 1999). Developmental reorganization of Kv3 channel subtypes toward faster activation kinetics might underlie acceleration in Kv3 current rise time. Recombinant channels of Kv3.1a and Kv3.1b mRNA splicing variants have similar kinetics (Yokoyama et al. 1989; Kanemasa et al. 1995), whereas Kv3.3 and Kv3.4 channels have relatively fast activation kinetics among Kv3 families (Rudy et al. 1999). It remains to be seen whether Kv3.3 or Kv3.4 channels increase their expression during development at the calyceal terminals.
Contribution of presynaptic K+ currents to action potential duration
Presynaptic action potentials at the calyx of Held become shorter in duration during the second postnatal week (Taschenberger & von Gersdorff, 2000; Fedchyshyn & Wang, 2005). Our results indicate that this developmental change reaches a steady level at around P14 (Fig. 1A). During the second postnatal week, IpK increased in density and became faster in activation kinetics. Concomitantly, presynaptic Na+ currents became faster in inactivation kinetics (Supplemental Fig. 1; Leão et al. 2005). All these changes are likely to contribute to the developmental shortening of action potential duration. Blocking Kv3 channels by TEA (1 mM) prolongs action potential duration (Wang & Kaczmarek, 1998), whereas blocking Kv1 channels by MgTX (Ishikawa et al. 2003) or dendrotoxin (Dodson et al. 2003) has no such effect. Although both Kv3 and Kv1 currents undergo developmental changes, Kv3 currents have higher density (Fig. 4 and Table 1) and faster rise time kinetics (Fig. 5) compared with Kv1 currents. Taken together, these results suggest that developmental changes of Kv3 channels, rather than Kv1 channels, contribute to developmental shortening of action potential duration.
It has been reported that Kv1 immunoreactivity is predominantly located in the transition zone between the axon and calyceal terminal in P9 rats (Dodson et al. 2003). Consistently excised patches from P7–8 calyces showed no MgTX-sensitive Kv1 current. However, at P13–15 calyces, 5 out of 13 patches showed Kv1 current components (Fig. 6C). These results suggest that Kv1 channels undergo redistribution from the axon to the nerve terminal during postnatal development. This developmental redistribution of Kv1 channels, together with its increase in current density (Fig. 4), may contribute to stabilizing mature nerve terminals. Regarding the stabilizing role of Kv1 channels, it has been postulated that the firing behaviour during sustained depolarization depends upon axonal length (Dodson et al. 2003). However, at P13–15 calyces, in the absence of MgTX, we did not see tonic firing during sustained depolarization, as previously reported (Ishikawa et al. 2003), whereas tonic firing was consistently observed at P7–8 calyces.
Besides developmental changes in K+ currents and Na+ currents, morphological reformation of the nerve terminal (Kandler & Friauf, 1993) and redistribution of ion channels might affect presynaptic action potential duration. Morphological reformation of calyces from a spoon-shaped to a finger-like structure can accelerate extracellular K+ clearance, thereby potentially shortening action potential waveform (Clay, 2005), particularly during high-frequency spiking.
Physiological implications for the developmental changes in presynaptic K+ currents
The duration of the presynaptic action potential is directly correlated with the magnitude of Ca2+ influx, which triggers transmitter release (Katz & Miledi, 1969; Augustine, 1990; Borst & Sakmann, 1999). Therefore, the developmental shortening of the action potential can contribute to the developmental decrease in transmitter release probability observed at the rat calyx of Held during the second postnatal week (Iwasaki & Takahashi, 2001; Taschenberger et al. 2002). Developmental shortening of presynaptic action potential duration may also synchronize quantal release, shorten synaptic latency, and reduce its jitter (Borst & Sakmann, 1999; Fedchyshyn & Wang, 2005), thereby contributing to establishment of precisely timed synaptic transmission.
Reliable high-frequency synaptic transmission at the calyx of Held is essential for sound localization (Oertel, 1997). Mature calyceal synapses follow inputs of several hundred Hertz at room temperature (Fig. 7B, see also Wu & Kelly, 1993; Taschenberger & von Gersdorff, 2000), whereas transmission in response to high-frequency inputs is unreliable in immature calyces (Futai et al. 2001). During postnatal development, high-fidelity transmission at high frequency is acquired through developmental changes in both presynaptic and postsynaptic elements. Postsynaptically, developmental downregulation of NMDA receptors, which depends upon auditory activity, contributes to acquisition of high-fidelity transmission up to 100 Hz (Futai et al. 2001). Developmental shortening in the decay time of EPSCs (Taschenberger & von Gersdorff, 2000; Futai et al. 2001; Joshi & Wang, 2002; Yamashita et al. 2003; Koike-Tani et al. 2005), caused by speeding of deactivation and desensitization kinetics of AMPA receptor channels (Koike-Tani et al. 2005), may further contribute to high-fidelity transmission above 100 Hz (Joshi et al. 2004).
Presynaptically, developmental changes in Kv3 channels contribute to shortening of action potential duration. Furthermore, developmental stabilization of nerve terminals by the Kv1 channel upregulation and redistribution, suppresses aberrant firings. These changes, together with a developmental decrease in the recovery time of Na+ channels from inactivation (Leão et al. 2005), would enable calyceal terminals to fire reliably in response to high-frequency inputs, thereby contributing to the establishment of high-fidelity synaptic transmission.
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Footnotes |
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) and P13–15 (
). B, developmental increase in K+ current density. Left, membrane capacitance of calyceal terminals at P7–8 (filled bar) and P13–15 (open bar). *Significant difference (P < 0.05). Right, current density–voltage relationships at P7–8 and P13–15. The current density was calculated from the scaled IpK amplitude divided by the membrane capacitance (left). The liquid junction potential was corrected for this I–V relationship.
), TEA + IbTX (
)/k}], where V
). C, developmental acceleration in the rise time of IpK. Left, sample traces at 0 mV showing the rising phase of IpK at different ages (superimposed after peak amplitude normalization). Right, voltage dependence of the 10–90% rise time at P7–8, P13–15 and P19–21. *Significant difference among data from three age groups (two-way ANOVA, P < 0.01).
