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CELLULAR |
1 Department of Physiology, New York Medical College, Valhalla, NY 10595, USA
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(Received 25 May 2006;
accepted after revision 26 June 2006;
first published online 29 June 2006)
Corresponding author W. Ross: Department of Physiology, New York Medical College, Valhalla, NY 10595, USA. Email: ross{at}nymc.edu
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Introduction |
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The sites of Ca2+ release from stores may be particularly interesting because the large amplitude (several micromolar) and duration (0.5–1.5 s) of the [Ca2+]i increases from this source suggest that they could be effective in activating a number of downstream signalling mechanisms. Some inhibitory neurons target the apical dendrite close to the cell body and the IPSPs they evoke are known to be modulated by large postsynaptic Ca2+ signals (e.g. Wilson & Nicoll, 2001; Alger, 2002). In addition, several papers (Spacek & Harris, 1997; Berridge, 1998; Oertner & Svoboda, 2002; Nakamura et al. 2002) have suggested that synaptically activated waves could propagate through this region to the soma where large [Ca2+]i changes could affect protein synthesis, gene expression (Ghosh & Greenberg, 1995; Hardingham et al. 2001) and long-term synaptic plasticity (e.g. Yeckel et al. 1999).
Examination of previous results indicates that there is variability in the reported extent of Ca2+ wave propagation in the dendrites and soma of pyramidal neurons. Jaffe & Brown (1994) induced waves in these cells with ionophoretic glutamate pulses. While they did not systematically analyse these waves, examples in their paper show propagation through the soma. Similarly, Power & Sah (2002) evoked Ca2+ waves that entered the soma and passed through the nucleus following acute application of muscarine or carbachol (CCh). They also found that synaptic activation of cholinergic fibres enhanced spike-evoked Ca2+ signals in the soma, although the effect was small. In contrast, in our anecdotal experience (Nakamura et al. 1999, 2002; Zhou & Ross, 2002) most synaptically activated Ca2+ waves appeared to be confined to the dendritic region and rarely entered the soma. Therefore, we decided to examine more systematically the extent of wave propagation and to investigate conditions that modulate the spatial properties of Ca2+ release, in particular those mechanisms that could extend propagation into and through the cell body.
We found that focal stimulation in the SR evoked waves of variable extent that almost never propagated through the cell body; most waves stopped at the soma–dendrite border. Associative stimulation with a secondary electrode near the soma, pairing synaptic stimulation with backpropagating action potentials, or priming of stores with action potential-evoked Ca2+ entry also failed to extend the waves into the soma. However, bath application of low concentrations of carbachol under appropriate conditions or the direct injection of IP3 into the cell body consistently allowed synaptically activated waves to propagate through the soma. These waves, and the few waves that propagated through the soma without modulators, had high amplitude in the centre of the cell, in contrast to spike-evoked [Ca2+]i increases, which were largest just under the membrane. Some of these results have been published previously in abstract form (Hong et al. 2005).
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Methods |
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Experiments were performed on transverse hippocampal slices (300 µm thick) prepared from 2- to 4-week-old Sprague-Dawley rats (Nakamura et al. 1999, 2002). Animals were anaesthetized with isoflurane and decapitated using procedures approved by the Institutional Animal Care and Use Committee of New York Medical College. Slices were cut in an ice-cold solution consisting of (mM): 120 choline-Cl, 3 KCl, 8 MgCl2, 1.25 NaH2PO4, 26 NaHCO3, and 10–20 glucose. They were incubated for at least 1 h in normal artificial cerebrospinal fluid (ACSF) composed of (mM): 124 NaCl, 2.5 KCl, 2 CaCl2, 2 MgCl2, 1.25 NaH2PO4, 26 NaHCO3 and 10 or 20 glucose, bubbled with a mixture of 95% O2–5% CO2, making the final pH 7.4. The same solution was used for recording.
Submerged and superfused slices were placed in a chamber mounted on a stage rigidly bolted to an air table and were viewed with a 40x or 60x water-immersion lens in an Olympus BX50WI microscope mounted on an X–Y translation stage. Somatic whole-cell recordings were made using patch pipettes pulled from 1.5 mm outer diameter thick-walled glass tubing (1511-M, Friedrich and Dimmock, Millville, NJ, USA). Tight seals on CA1 pyramidal cell somata were made with the ‘blow and seal’ technique using video-enhanced DIC optics to visualize the cells (Sakmann & Stuart, 1995). For most experiments the pipette solution contained (mM): 140 potassium gluconate, 4 NaCl, 4 Mg-ATP, 0.3 Na-GTP, and 10 Hepes, pH adjusted to 7.2–7.4 with KOH. This solution was supplemented with 150–200 µM bis-fura-2 (a high-affinity indicator) or 300 µM furaptra (a low-affinity indicator; Molecular Probes, Eugene, OR, USA). Most experiments were repeated using both indicators. Synaptic stimulation was evoked with 100 µs pulses with glass or tungsten electrodes placed on the slice about 10–30 µm to the side of the main apical dendritic shaft and at varying distances from the soma. The glass electrodes were low resistance patch electrodes (less than 5 M
) filled with ACSF with a tungsten wire glued to the side. The bipolar tungsten electrodes (used in only a few experiments) had one sharpened electrode (WPI, model TM33B01KT) with a second tungsten wire glued to the side about 1 mm behind the tip of first electrode (Nakamura et al. 1999). Temperature in the chamber was maintained between 31 and 33°C. trans-1-Amino-cyclopentyl-1,3-dicarboxylate (t-ACPD) was obtained from Tocris-Cookson (Ellisville, MO, USA). All other chemicals were obtained from Fisher Scientific (Piscataway, NJ, USA) or Sigma Chemical (St Louis, MO, USA).
Dynamic [Ca2+]i measurements
Time-dependent [Ca2+]i measurements from different regions of the pyramidal neuron were made as previously described (Lasser-Ross et al. 1991; Nakamura et al. 2002). Briefly, a Photometrics (Tucson, AZ, USA) AT300 or Quantix cooled CCD camera, operated in the frame transfer mode, was mounted on the camera port of the microscope. Custom software (original version described in Lasser-Ross et al. 1991) controlled readout parameters and synchronization with electrical recordings. A second custom program was used to analyse and display the data. Pixels were binned in the cameras to allow frame rates of 30–50 Hz. Fluorescence changes of bis-fura-2 and furaptra were measured with single wavelength excitation (382 ± 10 nm) and emission >455 nm. [Ca2+]i changes are expressed as –
F/F, where F is the fluorescence intensity when the cell is at rest and F is the change in fluorescence during activity. Corrections were made for indicator bleaching during trials by subtracting the signal measured under the same conditions when the cell was not stimulated.
To examine the spatial distribution of postsynaptic [Ca2+]i changes, we selected pyramidal neurons that were in the plane of the slice and close to the surface. In these neurons, we could examine [Ca2+]i increases over a range of 140–230 µm with the cameras and lenses selected for these experiments. Increases in different parts of the cell are displayed using either selected regions of interest (ROIs) or a pseudo ‘line scan’ display (Nakamura et al. 2000).
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Results |
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F/F at the ROI positioned at the initiation site (related to the change in [Ca2+]i; Lev-Ram et al. 1992) increased rapidly and then appeared to saturate (Nakamura et al. 1999). In contrast, the spatial extent of the release wave increased more gradually, as illustrated with the ‘line scan’ plots. For these initial experiments we maintained the amplitude of the summating EPSPs below action potential threshold (in some cases by injecting hyperpolarizing current into the somatic electrode) to avoid the complication of the synergistic action of spike evoked calcium entry and synaptic mobilization of IP3 (Nakamura et al. 1999; see Fig. 5). Subthreshold EPSPs by themselves evoke little [Ca2+]i increase in the proximal apical dendrites or soma (e.g. see Fig. 3). This was the typical pattern of response over many experiments, with some variation mostly related to the position of the stimulating electrode and the branching pattern of the dendrites. A plot of the average signal amplitude and wave extent as a function of the stimulation current for six cells is shown below the traces, confirming that the waves spread over a larger area with increasing intensity.
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A second reason for repeating the experiments with furaptra was that the signal amplitude saturated in experiments using the high-affinity indicator bis-fura-2, Using furaptra the amplitude, as expected, did not saturate and grew gradually after an initial jump as the stimulus intensity increased. This pattern is consistent with regenerative release although it is not strictly ‘all-or-none’. The peak change of 15% corresponds to a [Ca2+]i increase of about 7 µM (Nakamura et al. 1999) and is much higher than can be detected accurately with bis-fura-2 (Larkum et al. 2003).
As discussed previously (Nakamura et al. 2002), a reasonable hypothesis for the extent of wave propagation is that increasing stimulus intensity activates more synapses, which mobilize increasing amounts of IP3 distributed over a region largely determined by the synaptic sites contacted by the activated presynaptic fibres. The regenerative propagating wave fails when it reaches a region with low IP3 concentration ([IP3]i).
Since the region of Ca2+ wave activation was generally near the location of the stimulation electrode (Nakamura et al. 1999) and this region expanded with increasing stimulation intensity, we thought that stimulating near the soma with sufficiently high intensity would evoke waves that entered the soma. However, that was generally not the case. Figure 2A shows a typical response that generated large amplitude [Ca2+]i increases in the dendrite close to the cell body, but almost no increase in the soma. Figure 2B summarizes the results of many experiments where stimulation was near the soma (exact positions shown in the figure). Almost every wave stopped near the soma–dendrite border when the high-affinity indicator bis-fura-2 was included in the patch pipette. Using the low-affinity indicator furaptra to reduce Ca2+ buffering of regenerative propagation slightly extended the zone of propagation but did not change the general conclusion (Fig. 2C). However, a few waves propagated through the soma to the basal dendrites. These will be discussed below.
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We tried to use the same protocol to extend the waves into the soma without success. We tested eight neurons (four using bis-fura-2 and four using furaptra), with many trials on each cell. The second electrode was positioned next to the soma or next to the main dendrite near the soma dendrite border. Figure 3C shows an example of this effort and the results from all eight cells are shown in Fig. 3D. The synaptic response from stimulating electrode close to the soma was hyperpolarizing in some cases (n = 3), reflecting the predominance of inhibitory contacts on this region of the pyramidal neuron (Megias et al. 2001). Therefore, it appears that neither directly activating synapses near the soma nor associatively activating synapses in this region is an effective mechanism for generating waves that propagate through the cell body region.
A second possible mechanism to modulate wave propagation is to vary the extent that stores are filled. Previous experiments in pyramidal neurons (Jaffe & Brown, 1994; Pozzo-Miller et al. 1996; Stutzmann et al. 2003; Power & Sah, 2005) and Purkinje cells (Finch & Augustine, 1998) indicated that Ca2+ release from stores was enhanced by priming that filled the stores before stimulation. If regenerative release is enhanced it might also extend the region of active wave propagation. Figure 4A shows typical results of this kind of experiment. The cell was tetanically stimulated at the same intensity 8 times every 2 min. Action potentials were evoked intrasomatically at 4 Hz in the interval preceding some trials (‘Primed’). Other trials were not preceded by priming. In this cell priming slightly extended the range of wave propagation and made it more likely to observe waves. The extent was reduced or the wave failed altogether when there was no priming. A cumulative analysis from nine cells is presented in Fig. 4B. In general, priming increased the spatial extent of the waves when the previous trial evoked a wave and stimulation evoked a wave of about the same size or smaller when priming was not used. None of these waves extended significantly into the soma. A more extensive analysis of the effects of priming will be presented elsewhere.
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One possibility for failure to propagate to the soma is that the patch electrode on the cell body washed out components that were essential for allowing Ca2+ release from stores in that region. However, two different control experiments argue against that conclusion. First, we found that patching the cell on the dendrites about 50 µm from the soma and stimulating the cell with an extracellular electrode near the soma evoked waves proximal to the patch electrode that failed to enter the cell body (n = 2; data not shown). When the stimulating electrode was distal to the recording electrode the waves passed through the location of the dendritic patch without any effect on the amplitude or propagation velocity of the wave (n = 3). Second, we found that we could evoke waves that propagated into the soma by intrasomatically generating action potentials in ACSF containing 30 µM t-ACPD (Nakamura et al. 1999, 2000).
This last control suggested the fourth possibility, that the range of wave propagation might be extended by increasing the basal level of [IP3]i by applying neuromodulators (Nash et al. 2004). This strategy was successful as shown in Fig. 6A. Synaptically stimulated waves in normal ACSF were confined to the apical dendrites as shown in Fig. 2. However, when 10 µM CCh was added to the ACSF the waves consistently (n = 6/6) spread into and through the cell body. Even 3 µM CCh was effective in 2/3 experiments. This effect did not involve voltage gated calcium entry since the synaptic response was kept below spike threshold. Interestingly, these successful experiments required a low affinity Ca2+ indicator in the pipette (in this case 300 µM furaptra). When the usual 150 µM bis-fura-2 was used the waves spread over a larger region of the dendrites but still failed to fully invade the soma in the presence of 10 µM CCh (Fig. 6B; n = 5/5). This indicates that regenerative propagation in this region is very sensitive to Ca2+ buffering (see also Nakamura et al. 2000). In this experiment bath application of CCh by itself did not evoke Ca2+ release (Nakamura et al. 2000) although acute application at higher concentration evoked waves (Power & Sah, 2002). Similar experiments using 30 µM t-ACPD showed that this modulator also extended waves into the soma if furaptra was used as the Ca2+ indicator (n = 2; data not shown). However, it was hard to synaptically evoke Ca2+ release in the presence of t-ACPD in most cells, even though release was easily evoked by spikes (Nakamura et al. 2000) or could be synaptically evoked after the t-ACPD was washed out. The failure to evoke release in t-ACPD was probably because this bath-applied agonist desensitized the mGluRs preventing their activation by synaptically released glutamate (e.g. Dale et al. 2002). It is also possible that t-ACPD acted through group II presynaptic mGluRs to depress the release of glutamate (e.g. Vignes et al. 1995).
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Discussion |
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There are two likely hypotheses to explain why waves stop near the soma–dendritic boundary. One idea is that the properties of the endoplasmic reticulum (ER), IP3 receptors and their density are approximately uniform in all cell compartments and that the major differences among compartments are their geometry (i.e. the much larger volume of the soma compared to the dendrites) and the distribution of mGluRs on the surface of the cell. Although the distribution of mGluRs has never been accurately determined, the density of spines is low on the soma and main apical shaft (Bannister & Larkman, 1995; Megias et al. 2001). Most mGluRs are located perisynaptically near the base of the spines (Lujan et al. 1996). If this distribution also reflects the likelihood of activating mGluRs then synaptically mobilized IP3 will not be produced significantly in the soma and apical dendrite. Rather it will be produced in the oblique dendrites where it can then diffuse rapidly (Allbritton et al. 1992) to the main shaft. When IP3 then diffuses further into the soma it will be diluted by the large volume of the cell body and may then be below the threshold concentration needed to support regenerative Ca2+ release. This mechanism resembles the ‘impedance mismatch’ that has often been used to explain the failure of action potentials to pass through branch points (e.g. Parnas & Segev, 1979) or to activate the soma (e.g. Mainen et al. 1995). This model also explains why the addition of CCh or t-ACPD enabled the waves to consistently overcome the failure to invade the soma. These bath-applied metabotropic agonists probably produced a low level of IP3 in the pyramidal neuron that reached diffusional equilibrium, limited only by the desensitization of receptors and the rate of IP3 breakdown. The resulting steady state level of [IP3]i in the soma would be sufficient to support wave propagation into this region. Consistent with this hypothesis direct injection of IP3 into the soma promoted wave propagation into this region (Fig. 7). The failure of spikes to promote wave propagation to the soma or even to extend propagation in the dendrites (Fig. 5) suggests that once waves are initiated exogenous Ca2+ plays no further role in wave propagation; this Ca2+ is supplied abundantly by the release process. The critical factor is the supply of IP3, which apparently does not normally rise to threshold levels in the soma.
The second possibility is that the properties and density of IP3 receptor isoforms and associated signalling molecules is different in the soma and in the dendrites. For example, Jacob et al. (2005) found many differences among relevant molecules in cultured hippocampal neurons. The PMCA1 and SERCA pumps were distributed relatively uniformly while PIPKI
, IP3R1, RyR1 and chromogranin B (CGB) were more concentrated in the somatic region, and these differences affected the pattern of Ca2+ signals. However, it is not clear how any of these patterns found in cultured hippocampal neurons could explain the difficulty in propagating synaptically activated Ca2+ waves into the soma in intact neurons. Furthermore, it is not clear that the same distributions are found in the intact pyramidal neurons we examined in acute slices. Interestingly, the same group (Jacob et al. 2005) found that the distribution of the low threshold IP3R1 was uniform in PC12 neurons while the high threshold IP3R3 was targeted to the soma, a pattern that could help explain our results if it is also found in intact hippocampal neurons.
Associative propagation
It was difficult to associatively extend the range of wave propagation in the distal direction, but the reasons for this difficulty are not clear. Previous experiments suggest that it should be easier to open IP3Rs if both [Ca2+]i and [IP3]i are raised and that a lower level of [IP3]i should be needed if [Ca2+]i is high (Moraru et al. 1999; Mak et al. 2001). If this conclusion is valid for the dendritic environment, then at the wave front, following massive Ca2+ release, a lower [IP3]i should be needed to extend propagation than to initiate regenerative Ca2+ release. The modest success we achieved with this experiment (Fig. 3A) supports this model. However, a simple reading of the single channel data (Moraru et al. 1999) suggests that a significantly lower level of mGluR activation and IP3 mobilization by synaptic activity should have been effective instead of the just subthreshold levels we needed. Most likely there are too many steps and unknown signalling mechanisms in this process to fit neatly into this simple model. In contrast, the failure to associatively extend propagation into the soma is more likely due to the paucity of synaptic contacts on the cell body and the consequent low level of [IP3]i mobilized in that region by the second electrode. This is the same reason why direct synaptic stimulation in this region, even at high intensity, failed to make most waves enter the soma.
Nevertheless, if this model of associative wave extension has some validity then it may supply an alternative explanation for the associativity that is one of the hallmarks of LTP. In the usual model of LTP induction associativity is explained by having the membrane depolarization achieved by a strong synaptic input supply the potential needed to open the Ca2+-permeable NMDA receptors activated by a weak synaptic input. In the alternative model associativity is achieved by a mechanism independent of a change in membrane potential. Instead, the rise in [Ca2+]i at the wave front lowers the threshold level of [IP3]i needed for Ca2+ release at the site of the weaker input. These models are not mutually exclusive.
Conditions for successful Ca2+ wave propagation into the soma
In a few experiments in normal ACSF we observed Ca2+ wave propagation into the soma. In addition, in the presence of low concentrations of CCh or t-ACPD synaptically activated Ca2+ waves always propagated further than in normal ACSF and usually propagated through the soma. In most of the experiments in this paper these waves were evoked with a tetanus that stimulated EPSPs that were subthreshold for generating action potentials. Since subthreshold EPSPs cause little [Ca2+]i increase from voltage gated Ca2+ entry the extended propagation cannot be due to the synergism of Ca2+ entry with mGluR mobilized IP3 (Nakamura et al. 1999). Furthermore, in a direct test of the effect of synergistic wave activation (Fig. 5) we found that backpropagating action potentials had no detectable effect on the extent of Ca2+ wave propagation. The most likely explanation for wave extension is that (as mentioned above) the bath applied agonists mobilized a level of [IP3]i in the soma that was higher than could be achieved by synaptic activation alone. Since the threshold level of CCh (3 µM) was similar to that required to evoke release by backpropagating action potentials (Nakamura et al. 2000), it is likely that a similar mechanism promotes Ca2+ release in the soma. In this case the Ca2+ is supplied by the propagating wave front instead of entry through voltage gated Ca2+ channels.
We also note that consistent propagation through the soma in the presence of CCh was only observed when the low-affinity indicator furaptra was included in the patch pipette. With low concentrations of bis-fura-2 (150 µM) we could evoke Ca2+ release in normal ACSF and measure an increase in spatial extent of the wave in CCh (Fig. 6B), but these waves did not extend through the soma. Previously (Nakamura et al. 2000), we found that higher concentrations of bis-fura-2 blocked Ca2+ release completely, which we explained by the interference of the indicator with the regenerative Ca2+ release mechanism. These new experiments suggest that regenerative propagation into the soma is particularly sensitive to Ca2+ buffering. In contrast, the experiments examining the modulation of wave propagation within the dendrites produced results that were relatively insensitive to the choice of Ca2+ indicator. Since the spatial extent of the waves was increased in CCh without increasing the stimulus intensity the spatial increase cannot be due to activating more synapses and is most likely a result of an increase in [IP3]i. Following bath application of CCh the simplest assumption is that the concentration of IP3 is the same in the soma and proximal dendrites, which should allow propagation into the soma if all other parameters are the same, as shown in the IP3 injection experiments. The greater sensitivity to Ca2+ buffering in the soma could be explained either by a different level of endogenous buffer in this compartment or if the regenerative release mechanism is different, e.g. if there is a mix of IP3Rs in the soma with lower Ca2+ affinity than the receptors in the apical dendrite (Koulen et al. 2005), or if the receptors are organized in a different pattern (Delmas & Brown, 2002; Shuai & Jung, 2003) that affects their sensitivity to IP3 and/or Ca2+.
We do not have a clear explanation for the few examples of wave propagation into the soma in normal ACSF. Most likely in these cells there was an increase in one of the critical parameters (e.g. [IP3]i or the density of IP3Rs) that allowed the propagating wave to become suprathreshold in the soma. Another possibility is that some cholinergic fibres were activated along with the Schaffer collaterals and they generated IP3 in the soma. Whether this was just normal variation among pyramidal neurons or a separate category of cells is unknown.
Functional significance
Since Ca2+ waves propagate into the soma only in certain conditions these results suggest that the effects of Ca2+ release in pyramidal neurons should be divided into two classes – those effects that are activated by large amplitude [Ca2+]i increases in the proximal apical dendrites and those that are activated by [Ca2+]i increases in the soma. One example in the first group would be endocannabinoid mediated suppression of synaptic inhibition (e.g. Wilson & Nicoll, 2001) since there is a large concentration of inhibitory inputs targeted to this region (Megias et al. 2001). A classic example in the second group is Ca2+-activated gene transcription (Dolmetsch et al. 1998; Hardingham et al. 2001). Our results suggest that in most cases, where Ca2+ waves do not reach the soma and nucleus, the consequences are confined to the first group. However, when cholinergic inputs are also activated (Cole & Nicoll, 1984) waves may reach the nucleus and activate gene expression and other signalling mechanisms. Indeed there is evidence that cholinergic modulation enhances protein synthesis induced by synaptic activation (Feig & Lipton, 1993) and enhances late-phase transcription-dependent LTP activated by tetanic stimulation (Dringenberg et al. 2004).
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Footnotes |
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