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. 2000 Sep 15;527(Pt 3):507–513. doi: 10.1111/j.1469-7793.2000.00507.x

Single channel properties of neuronal nicotinic ACh receptors in stratum radiatum interneurons of rat hippocampal slices

Zuoyi Shao 1, Jerrel L Yakel 1
PMCID: PMC2270095  PMID: 10990537

Abstract

  1. The single channel properties of neuronal nicotinic ACh receptors (nAChRs) were investigated in outside-out patches from CA1 stratum radiatum interneurons from thin slices of rat hippocampus.

  2. The application of ACh (10 μm to 1 mm) induced the opening of observable single channel currents with two distinct current levels, which corresponded to conductance levels of 38 ± 3 and 62 ± 2 pS. The 38 pS channel was observed in 10 % (n = 260) of patches, whereas the 62 pS channel was observed in 4 % of patches; these two channel types were most often observed independently.

  3. The α7-selective nAChR antagonist methyllycaconitine (MLA; 50 nm) reduced the open probability of the 38 pS channel by 73 %. In contrast, the 62 pS channel was unaffected by MLA, but instead was blocked by dihydro-β-erythroidine (DHβE; 10 μm), a broad spectrum nAChR antagonist.

  4. These data suggest that rat hippocampal CA1 stratum radiatum interneurons in the slice possess at least two different types of functional nAChRs, an α7-containing subtype with a single channel conductance of 38 pS, and a non-α7 subtype with a single channel conductance of 62 pS.

The neuronal nicotinic ACh receptor (nAChR) belongs to the superfamily of ligand-gated ion channels and is widely expressed throughout the nervous system where it participates in a variety of physiological processes including cognition, reward, development and analgesia (see review by Jones et al. 1999). Until recently the neuronal nAChR in the brain was thought to serve primarily a modulatory role as a presynaptic receptor to regulate neurotransmitter release from nerve terminals (McGehee & Role, 1995; Wonnacott, 1997). However, several recent reports have clearly demonstrated that nAChRs in the brain also function in a postsynaptic role by mediating fast cholinergic synaptic transmission (Roerig et al. 1997; Alkondon et al. 1998; Frazier et al. 1998a; Pettit & Yakel, 1999; but see McQuiston & Madison, 1999).

Currently at least 10 different nAChR subunits are known to be expressed in the rat CNS (McGehee & Role, 1995; McGehee, 1999). Until recently, neuronal nAChRs in the mammalian brain (and in particular the hippocampus) were thought to consist primarily of either heteromers of α4β2 subunits and possibly α3β4 subunits, or of homomers of the α7 subunit (Alkondon & Albuquerque, 1993; Zoli et al. 1998; Alkondon et al. 1999). However, it is becoming clear that there is much more diversity in the molecular makeup of neuronal nAChRs, and that other nAChR subunits are combining to form functional nAChRs, with different subtypes playing roles in different regions of the CNS (Alkondon & Albuquerque, 1993; Alkondon et al. 1997; Zoli et al. 1998; Jones et al. 1999; Léna et al. 1999; McGehee, 1999). In addition, whether α7-containing nAChRs are homomeric or heteromeric assemblies (i.e. combining with other nAChR subunits to form functional channels) in vivo still remains to be determined.

In many cases, the molecular makeup of nAChRs can be inferred from their functional properties (McGehee & Role, 1995). Therefore, we have investigated the properties of the single channel currents resulting from the activation of nAChRs in outside-out membrane patches from rat hippocampal CA1 stratum radiatum interneurons in the slice. We have found that ACh (10 μm to 1 mm) induced the opening of two distinct single channel types, one corresponding to a conductance level of 38 pS (observed in 10 % of 260 patches), and the other of 62 pS (4 % of patches). The pharmacological and physiological data presented here suggest that the 38 pS channel is an α7-containing nAChR that may include other non-α7 subunits, and that the 62 pS channel is a non-α7-containing receptor, thus further confirming the notion of the complex molecular subunit diversity of nAChR channels in the brain and hippocampus in vivo.

METHODS

Hippocampal slice preparation

Experiments were performed on rat hippocampal slices using procedures similar to those previously described (Jones & Yakel, 1997). Briefly, 1- to 3-week-old Wistar rats were anaesthetized with halothane and decapitated, and the brain was removed and placed into ice-cold artificial cerebrospinal fluid (ACSF; gassed with 95 % O2 and 5 % CO2) containing (mm): NaCl 126, KCl 3.5, CaCl2 2, MgCl2 6, NaH2PO4 1.2, NaHCO3 25 and glucose 11; pH 7.4. Coronal sections of brain, which included the hippocampus, were cut into 350 μm slices using a Vibratome (Series 1000, Ted Pella, Inc., Redding, CA, USA). Slices were transferred to an incubation chamber containing experimental ACSF (with 1.3 mm MgCl2 instead of 6 mm MgCl2, gassed with 95 % O2 and 5 % CO2) at 30°C. All experiments were carried out in accordance with guidelines approved by the NIEHS Animal Care and Use Committee.

Single channel recordings

To study the single channel currents from outside-out membrane patches, patch pipettes were pulled from thick-walled borosilicate glass (catalogue no. B150-86-10; o.d. 1.5 mm, i.d. 0.86 mm; Sutter Instrument Co.) and had resistances of 5–10 MΩ. The patch pipette filling solution contained (mm): caesium gluconate 140, MgCl2 2, CaCl2 0.5, Mg-ATP 2, BAPTA 5 and Hepes 10; and was adjusted to pH 7.2 with CsOH. Slices that had been incubated for at least 1 h were placed in the recording chamber and perfused with experimental ACSF at room temperature (18–22°C). Hippocampal CA1 stratum radiatum interneurons were visually identified by their location and morphology; outside-out patches were obtained from the soma of these cells. Single channel currents were obtained using an Axopatch 200B amplifier (Axon Instruments), lowpass filtered at 2–5 kHz and digitized at 10–20 kHz. All data were acquired with pCLAMP 7 software (Axon Instruments).

After excising patches, ACh (10 μm, unless otherwise specified) was applied (< 20 ms) to the patch via a synthetic quartz tube (i.d. 320 μm; Polymicro Technologies, Phoenix, AZ, USA) positioned ∼150–200 μm from the patch; the delivery of ACh was controlled by a computer-driven valve (General Valve, Fairfield, NJ, USA). As previously observed for central nAChR single channel currents in outside-out patches (Lester & Dani, 1994; Connolly et al. 1995), the activity of the channels tended to run down with time; single channel activity was usually gone after 10 min.

Single channel analysis

pCLAMP 7 software was used for the data analysis. Briefly, the average amplitudes of single channel currents were measured using all-points histograms that were fitted by Gaussian distributions. The accuracy of these amplitude values was confirmed by the measure, by hand, of individual longer duration events. The open probability and dwell times were estimated using Fetchan and pSTAT (pCLAMP 7 software, Axon Instruments). The detection of events was determined by the ‘50 % threshold’ method. The dwell-time analysis was obtained from patches containing only a single channel, and was fitted by single or double exponential functions where appropriate. Differences between means were compared using one-way analysis of variance; P values of less than 0.05 were considered significantly different. All chemicals were obtained from Sigma except MLA, which was obtained from Research Biochemicals International.

RESULTS

ACh activates single channel currents with two distinct conductances

We obtained 260 outside-out patches from rat hippocampal CA1 stratum radiatum interneurons in the slice. The application of ACh (10 μm) to these patches induced the opening of two distinct (i.e. different current levels) and very brief single channel events (Fig. 1). At a holding potential of −60 mV, these two current levels were 2.3 and 3.7 pA, which corresponded to conductance levels of 38 ± 3 and 62 ± 2 pS, respectively. These two nAChR channel types were most often observed independently; the 38 pS channel was observed in 10 % of patches, whereas the 62 pS channel was observed in 4 % of patches. Only in two patches were both channel types observed. The single channel current-voltage (I–V) relation for both channel types was linear for negative voltage ranges; no observed outward single channel events were ever observed at positive holding potentials, indicating strong inward rectification for both channel types (Fig. 1C and D).

Figure 1. ACh induces the opening of two distinct single channel currents in rat hippocampal CA1 stratum radiatum interneurons.

Figure 1

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A, the rapid application of ACh (10 μm) induced observable single channel currents at a holding potential (Vh) of −60 mV. Two distinct single channel current levels (a and b) co-existed in this patch. B, the amplitude histogram from the patch in A confirmed the existence of two populations of channels, with current levels of 2.3 and 3.7 pA. The current-voltage (I–V) relation for the smaller (C) and larger (D) single channel currents from multiple patches are shown. The slope conductance, from the linear portion of the I–V plot at negative holding potentials (dashed line), averaged 38 ± 3 pS for the smaller conductance channel (C; n = 4), and 62 ± 2 pS for the larger conductance channel (D; n = 7). No outward current was seen at positive holding potentials for either channel type.

Characterization of the 38 pS channel

The α7-selective nAChR antagonist methyllycaconitine (MLA) was used to test whether the 38 pS channel contained the α7 nAChR subunit. MLA (50 nm) dramatically reduced the opening of the 38 pS channel (Fig. 2). For the patch shown in Fig. 2A, the application of ACh induced the opening of only the 38 pS channel (middle traces), and the subsequent addition of MLA blocked these channel events (right traces). In another patch, the open probability of the 38 pS channel was greatly reduced by MLA (by 84 %); the block by MLA was partly reversible after its removal (Fig. 2B). It should be noted that the lack of full reversibility is most probably due to the rundown of channel activity, which is often observed for central nAChR single channel currents in outside-out patches (Lester & Dani, 1994; Connolly et al. 1995). In four patches, MLA significantly reduced both the frequency of channel opening (by 58 %) and the open probability (by 73 %) as compared with control patches (8 patches; Fig. 2C); MLA had no effect on the amplitude of the single channel current (data not shown).

Figure 2. Methyllycaconitine (MLA) blocks the 38 pS channel.

Figure 2

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A, in the absence of agonist (left traces), no single channel events are seen at various holding potentials. The addition of ACh to this patch resulted in the opening of only the 38 pS channel (centre traces). The addition of MLA (50 nm) dramatically reduced the opening of this channel (right traces). B, in another patch, the open probability of the 38 pS channel (activated by 10 μm ACh) is plotted, with and without MLA; Vh =−60 mV. C, the frequency of channel opening (s−1; left) and the open probability (right) are both significantly decreased by MLA (*P < 0.05 and **P < 0.01).

We analysed the open dwell times from patches containing the 38 pS channel before (8 patches) and during (4 patches) exposure to MLA; the open dwell time histograms were best fitted by a double exponential function (Fig. 3A). MLA significantly decreased the fast open dwell time by 43 % (from 0.23 ± 0.02 to 0.13 ± 0.03 ms); the slow open dwell time was not significantly altered by MLA (Fig. 3B). The quantification of these very brief open time values should be interpreted with caution in the context of the filter frequency (see Methods). The broad spectrum nAChR antagonist dihydro-β-erythroidine (DHβE; 10 μm), which has a relatively low affinity for the α7 nAChR (Alkondon & Albuquerque, 1993; McQuiston & Madison, 1999), had no effect on the kinetics of the 38 pS channel (2 patches; data not shown). At a holding potential of −30 mV, the fast and slow open dwell times from patches (2) containing the 38 pS channel were 0.17 ± 0.01 and 1.6 ± 0.8 ms, respectively.

Figure 3. Effect of MLA on open dwell times of the 38 pS channel.

Figure 3

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The open dwell time distribution for control patches (n = 8) exposed to ACh (10 μm) containing only the 38 pS channel is shown in A, plotted as log time versus square root bin frequency (number of observations; Connolly et al. 1995); the histogram was best fitted by a double exponential function. The fast (τfast) and slow (τslow) time constant values are indicated on the figure; the ratio of the zero time intercepts of the fast and slow components was 5. B, MLA (50 nm; 4 patches) significantly decreased τfast without affecting τslow; *P < 0.05.

The activity of the 38 pS channel appeared to decrease in the continued presence of ACh, a process commonly referred to as desensitization. In 11 patches that were continually exposed to ACh (10 μm) and that contained only the 38 pS channel, the activity of the channel completely disappeared by 25 ± 10 s. Although it can be difficult to distinguish between desensitization and rundown, the kinetics of desensitization were in general more rapid and reversible.

Characterization of the 62 pS channel

MLA had no significant effect on the kinetics, the amplitude or the open probability of the 62 pS channel (Fig. 4A and B; 2 patches), suggesting that this type of nAChR does not contain the α7 nAChR subunit. However, DHβE (10 μm) greatly reduced the open probability (2 patches) of the 62 pS channel (by 83 % for the patch shown; Fig. 4C and D); the block by DHβE was mostly reversible after its removal (Fig. 4D). Like the 38 pS channel, the open time of the 62 pS channel was very brief. The open dwell time histogram (from 4 patches) was best fitted by a single exponential function with a time constant of 0.26 ± 0.1 ms.

Figure 4. Pharmacology of the 62 pS channel.

Figure 4

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A and B, MLA (50 nm) had no effect on the opening, amplitude or open probability of the 62 pS channel. C and D, dihydro-β-erythroidine (DHβE; 10 μm) dramatically reduced the opening, and open probability, of the 62 pS channel. ACh (1 mm) was applied for 3 s (D; left), the bath solution was then washed out for 5 min, after which ACh and DHβE were applied for 3 s (D; middle). After washing for 5 min, ACh was reapplied (D; right).

DISCUSSION

The activation of nAChRs in outside-out membrane patches from rat hippocampal CA1 stratum radiatum interneurons in the slice induced the opening of two distinct single channel conductance levels; the first had a conductance of 38 pS and contained the α7 nAChR subunit, and the second had a conductance of 62 pS and did not contain the α7 subunit. Both channel types strongly rectified (i.e. no outward current was ever observed at positive holding potentials), and had brief open time kinetics. Strong rectification of neuronal nAChR channels is often not observed in excised patches, perhaps due to the relief of spermine block (Connolly et al. 1995; Haghighi & Cooper, 1998); this suggests that the molecular makeup and/or the regulation of nAChRs in rat hippocampal interneurons may be different. These data are consistent with the previous functional identification from our laboratory and from others of the expression of diverse subtypes of nAChRs in rat hippocampal interneurons (see review by Jones et al. 1999).

The nAChRs are widely expressed throughout the CNS and are thought to be involved in a variety of different physiological and pathological conditions. One major issue concerning nAChRs in the brain is their molecular makeup. At least 10 different nAChR subunits are known to be expressed in the rat nervous system, and the properties of the channels are determined principally by the particular subunits that are forming channels. Pharmacological criteria have identified both α7 and non-α7 subtypes as major components of the nAChRs in the rat hippocampal interneurons; however, the precise molecular identity of both the α7 and non-α7 receptors remains to be determined (Jones et al. 1999).

Although native α7-containing nAChRs were initially conceived to be homomers of only the α7 subunits, much recent evidence suggests a marked diversity of native α7-containing nAChRs, strongly suggesting the possibility that other subunits may be combining with the α7 subunit in vivo (Girod et al. 1999). For example in chick sympathetic neurons, the α7 subunit contributes to the formation of at least three different types of native nAChRs, all of which are distinct from homomeric α7-containing receptors (Yu & Role, 1998a). Interestingly, both homomeric and heteromeric assemblies of α7-containing nAChRs, possibly involving the α5, β2 and/or β3 subunits, can be formed in Xenopus oocytes (Revah et al. 1991; Palma et al. 1999; Girod et al. 1999).

Therefore what might be the molecular ‘identity’ of the 38 pS channel that we have identified as the primary functional nAChR channel in patches excised from the soma of rat CA1 hippocampal stratum radiatum interneurons? One of the α7-containing ‘heteromeric’ nAChRs previously described in chick sympathetic neurons (Yu & Role, 1998a) has properties very similar to those of the 38 pS channel described here; it had a unitary conductance of ∼35 pS, was blocked by MLA, had a relatively brief mean open time and desensitized relatively slowly, all properties which differ from those of homomeric α7-containing nAChRs (Revah et al. 1991). Yu & Role (1998a) also found that the α7 subunit contributed to an 18 pS channel; this channel was blocked by α-bungarotoxin (α-BgTx), and appeared to also contain the α5 subunit (Yu & Role, 1998b). Therefore the 35 pS channel from chick sympathetic ganglia and the 38 pS channel from rat stratum radiatum interneurons are possibly similar α7-containing heteromeric nAChRs. Although for these receptors it appears as if the α7 subunit may not be combining with the α5 subunit, some indications suggest the possible involvement with a β subunit. The α7 subunit has been reported to co-assemble with either the β2 or β3 subunits in Xenopus oocytes (Palma et al. 1999; Girod et al. 1999). In the accompanying paper (Sudweeks & Yakel, 2000), we have shown, using single-cell RT-PCR techniques in conjunction with whole-cell patch-clamp recordings, that these rat stratum radiatum interneurons co-express both the α7 and β2 subunits, and that both of the subunits are associated with fast-activating nAChR-mediated responses. Thus perhaps the 38 pS channel described here can be proposed to be an α7β2-containing receptor.

Previously Castro & Albuquerque (1993) reported that in cultured rat hippocampal neurons, nAChR activation induced the opening of a channel with a conductance of 73 pS, that had brief open time and desensitization kinetics, and that was blocked by MLA; thus this channel most probably contained the α7 nAChR subunit. Perhaps the reason why the properties of this α7-containing channel differed from those reported here for the α7-containing 38 pS channel in interneurons from rat hippocampal slices was that different experimental conditions were used. Cultured hippocampal neurons (presumably comprising mostly pyramidal neurons) are well known to express functional nAChRs (Zorumski et al. 1992; Alkondon & Albuquerque, 1993), whereas many investigators have reported that pyramidal neurons in slices have either no, or occasionally very small, nAChR-mediated responses (Alkondon et al. 1997; Jones & Yakel, 1997; Frazier et al. 1998b; McQuiston & Madison, 1999). As these pyramidal neurons in the slice express various nAChR subunits as detected using single-cell RT-PCR analysis (Sudweeks & Yakel, 2000), perhaps the expression of functional nAChRs is developmentally regulated and is altered under culture conditions. Interestingly single-channel recordings from thin slices from rat medial habenula also demonstrated multiple diverse types of nAChRs (Connolly et al. 1995).

In conclusion, our single channel data suggest that the two major types of functional nAChR channels in membrane patches excised from the soma of rat CA1 hippocampal stratum radiatum interneurons are an α7-containing receptor that may include other non-α7 subunits, and another non-α7-containing receptor that may include the α5 subunit. Thus from the data presented here and from several other labs, it is becoming clear that the in vivo subunit diversity of nAChR channels in the brain, and in the hippocampus in particular, is even much more complex than previously imagined.

Acknowledgments

We would like to thank Drs David Armstrong and Christian Erxleben for critical reading of this manuscript. This work was supported by the NIEHS Intramural program.

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