 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
Previous Article | Next Article
Volume 16, Number 13, Issue of July 1, 1996 pp. 4113-4128
Copyright ©1996 Society for NeuroscienceCholinergic-Dependent Plateau Potential in Hippocampal CA1 Pyramidal Neurons
Douglas D. Fraser and Brian A. MacVicar Neuroscience Research Group, Faculty of Medicine, University of Calgary, Calgary, Alberta, Canada T2N 4N1
ABSTRACT
Cholinergic stimulation of the hippocampal formation results in excitation and/or seizure. We report here, using whole-cell patch-clamp techniques in the hippocampal slice (34-35°C), a cholinergic-dependent slow afterdepolarization (sADP) and long-lasting plateau potential (PP). In the presence of 20 µM carbachol, action potential firing evoked by weak intracellular current injection elicited an sADP that lasted several seconds. Increased spike firing evoked by stronger depolarizing stimuli resulted in long-duration PPs maintained close to
Key words: muscarinic stimulation; Ca2+-activated nonselective cation conductance; HVA Ca2+ currents; ictal depolarization; epilepsy; slice-patch technique20 mV. Removal of either Na+ or Ca2+ from the external media, intracellular Ca2+ ([Ca2+]i) chelation with 10 mM bis(2-aminophenoxy)ethane-N,N,N
,N
-conotoxin, whereas 1.2 µM tetrodotoxin was ineffective. The involvement of a Na+/Ca2+ exchanger was minimal because both the sADP and PP persisted after equimolar substitution of 50 mM Li+ for Na+ in the external media or reduction of the bath temperature to 25°C. Finally, in the absence of carbachol the sADP and PP could not be evoked when K+ channels were suppressed, suggesting that depression of K+ conductances alone was not sufficient to unmask the conductance. Based on these data, we propose that a Ca2+-activated nonselective cation conductance was directly enhanced by muscarinic stimulation. The sADP, therefore, represents activation of this conductance by residual [Ca2+]i, whereas the PP represents a novel regenerative event involving the interplay between high-voltage-activated Ca2+ channels and the Ca2+-activated nonselective cation conductance. This latter mechanism may contribute significantly to ictal depolarizations observed during cholinergic-induced seizures.
INTRODUCTION
The hippocampal formation receives cholinergic afferents from the medial septum/diagonal band that terminate on dendritic segments located in both the cornu Ammonis and dentate gyrus (Wainer et al., 1993). This septohippocampal pathway is critical in the generation of rhythmical slow activity (Bland, 1986
The electrophysiological actions of cholinergic agonists on neurons have been studied extensively in vitro and, for the most part, are considered excitatory (Halliwell, 1990
, 1993
Although there are multiple reports of sADPs after muscarinic stimulation, cholinergic-dependent plateau potentials (PPs) have not been reported. This PP may represent a novel regenerative event involving interactions between IHVA and ICAN. It is conceivable that interplay between these channels could contribute significantly to ictal depolarizations observed during cholinergic-induced seizures (Lothman et al., 1991
These results have been presented in abstract form (Fraser and MacVicar, 1995
MATERIALS AND METHODS
Hippocampal slice preparation. Sprague-Dawley rats, postnatal 15-23 d, were decapitated and the brains were immersed in chilled artificial CSF (aCSF) containing (in mM): 126 NaCl, 2.5 KCl, 2 MgCl2, 2 CaCl2, 1.25 NaH2PO4, 26 NaHCO3, and 10 D-glucose, pH 7.3. The hippocampi were isolated and attached to the stage of a vibrating micro-slicer with cyanoacrylate glue. Tissue orientation and stability were ensured by propping the hippocampi against an immobilized block of 2% agar dissolved in physiological saline followed by a light application of low-melt gelatin around the tissue base. Transverse slices (150-400 µm) were prepared by sectioning the hippocampus perpendicular to its septotemporal axis. The slices were then transferred to a glass vial filled with oxygenated aCSF and incubated at room temperature.
Whole-cell patch-clamp recording. Whole-cell current-clamp recordings from neurons within hippocampal slices were obtained using either the ``blind-patch'' technique (Blanton et al., 1989
) were pulled from 1.5 outer diameter thin-walled glass (150F-4, World Precision Instruments) in two stages on a Narishige puller (PP-83; Tokyo, Japan) and filled with intracellular solution (in mM): 140 K-gluconate, 1.1 EGTA, 0.1 CaCl2, 10 HEPES, 2 Mg-ATP, and 0.3 Na-GTP, pH 7.2. Intracellular Ca2+ concentration was calculated to be 16 nM. In some experiments, Cs-gluconate or KCl was substituted for equimolar K-gluconate (see Table 1 for description of intracellular solutions). Voltage recordings were obtained in bridge mode (Axoclamp-2A, Axon Instruments, Foster City, CA) and were low-pass filtered (4-pole Bessel) at 10 kHz (
Table 1. Membrane properties of CA1 pyramidal neurons under whole-cell current clamp
rp (mV) RIN (M APAMP (mV) APTH (mV) APDUR (msec) (msec)
n K-gluconatea 149 ± 3 92 ± 1 1.6 ± 0.01 20.7 ± 0.4 188 Cs-gluconateb 183 ± 12 - - - 23.6 ± 1.8 11 KClc 173 ± 24 92 ± 5 1.8 ± 0.06 22.8 ± 3.0 8 BAPTAd 164 ± 47 88 ± 2 2.4 ± 0.15 21.6 ± 1.1 4 Abbreviations: rp, resting potential; RIN, input resistance; APAMP, action potential amplitude; APTH, action potential threshold; APDUR, action potential duration; Intracellular solutions (in mM): a 140 K-gluconate; 1.1 EGTA; 0.1 CaCl2; 10 HEPES; 2 Mg-ATP; 0.3 Na-GTP. b 40 Cs-gluconate; 100 K-gluconate; 1.1 EGTA; 0.1 CaCl2; 10 HEPES; 2 Mg-ATP; 0.3 Na-GTP. c70 KCl; 70 K-gluconate; 1.1 EGTA; 0.1 CaCl2; 10 HEPES; 2 Mg-ATP; 0.3 Na-GTP. d100 K-gluconate; 10 K-BAPTA; 40 HEPES; 2 Mg-ATP; 0.3 Na-GTP. Measurement of electrophysiological properties. Membrane characteristics were determined after patch rupture and sampled throughout the experiment. Series resistance was determined via a bridge potentiometer by balancing the voltage drop across the patch in response to a negative current pulse (
RESULTS
The results in this paper were obtained from 211 CA1 pyramidal neurons in the hippocampal slice preparation, recorded with whole-cell patch-clamp techniques. The average series resistance was 14.0 ± 0.2 MCholinergic stimulation of CA1 pyramidal neurons
Hippocampal CA1 pyramidal neurons were stimulated by bath application of carbachol, a nonhydrolyzable cholinergic agonist. Consistent with previous reports, 20 µM carbachol depolarized the membrane potential by 3-11 mV (n = 188) and increased RIN by 16 ± 1% (range 5-30; 50 neurons sampled). Spike frequency adaptation was reduced, and the action potential afterhyperpolarization was abolished (Fig. 1A). In thicker slices (300-400 µm), an increase in synaptic noise was commonly observed with carbachol application that could be differentiated into discrete excitatory and inhibitory postsynaptic potentials (data not shown) (MacVicar and Tse, 1989
Fig. 1. In the presence of carbachol, a nonhydrolyzable cholinergic agonist, depolarizing current injection resulted in either an sADP or a PP. A, Typical responses of a hippocampal CA1 pyramidal neuron to hyperpolarizing and depolarizing current injection. Neither an sADP nor a PP was observed in the absence of cholinergic agonists. The resting membrane potential of this neuron was
[View Larger Version of this Image (31K GIF file)]
Cholinergic-dependent sADP and PP
In the absence of a cholinergic agonist, positive current injection (0.1 nA) resulted in repetitive action potential firing in all CA1 pyramidal neurons tested (Fig. 1A,B; n = 196). After cessation of current injection, the membrane potential rapidly returned to resting levels. In contrast, after a 5 min application of 20 µM carbachol, weak current injection (~0.1 nA; 0.8 sec) resulted in repetitive firing at higher frequency, which was commonly superimposed on a depolarizing ramp. After cessation of evoked action potentials, a depolarizing afterpotential was observed that declined slowly over several seconds (Fig. 1A,B; n = 188/188). This potential was termed an sADP. The average duration and maximal amplitude of the sADP was 6.1 ± 0.2 sec (range 2.8-8.5; n = 50) and 9 ± 1 mV (range 3-20; n = 50), respectively. Injection of stronger current (
Fig. 2. Both the sADP and PP were depressed by coapplication of the muscarinic receptor antagonist atropine. In control, the resting membrane potential of this neuron was
[View Larger Version of this Image (20K GIF file)]
Each PP consisted of at least four distinct phases (Fig. 3A, arrows). The first phase consisted of a steep depolarizing shift that accompanied action potential firing during intracellular current injection. The second phase consisted of the prolonged PP. The third phase, lasting up to several seconds, was a repolarization that commonly hyperpolarized beyond the resting membrane potential. The final phase consisted of this hyperpolarization, which, over a prolonged period of time, returned to the baseline. The data in Figure 3A also demonstrate the reproducibility of the PP waveform in any one cell. In this neuron, five PPs were evoked, separated by 10 min between stimuli.
Fig. 3. The cholinergic-dependent PP consisted of at least four distinct phases, and the likelihood of generating a PP increased with the number of action potentials elicited. A, In the absence of cholinergic stimulation, the resting membrane potential of the neuron illustrated was
[View Larger Version of this Image (31K GIF file)]
Increasing the number of evoked action potentials enhanced the sADP amplitude until a critical threshold for PP genesis was achieved. For example, gradually increasing the intensity of the injected current resulted in increased spike firing (Fig. 3B). As a result, the amplitude of the sADP increased accordingly until the PP was elicited. Conversely, for a current pulse of a given amplitude, increasing the duration of the stimuli also increased the number of action potentials, thereby enhancing the sADP amplitude (Fig. 3C). A critical threshold for PP genesis was also obtained. Even though a clear transition from sADP to PP genesis was observed, the two phenomena may be related because both required cholinergic stimulation and followed a burst of action potentials.
The amplitude of the sADP and the duration of the PP were dependent on the holding potential (Fig. 4). As before, in the absence of a cholinergic agonist, the membrane potential returned to resting levels after a burst of evoked action potentials (Fig. 4A). In the presence of carbachol, however, both the sADP and PP were observed after identical stimuli (Fig. 4B). The membrane potential in this case was maintained at
Fig. 4. The amplitude of the sADP and the duration of the PP decreased with negative membrane potentials. A, Typical response of a hippocampal pyramidal neuron to hyperpolarizing and depolarizing current injection. Neither an sADP nor a PP was observed in the absence of cholinergic stimulation. The resting membrane potential of this pyramidal neuron was
[View Larger Version of this Image (37K GIF file)]
Ionic dependency of the sADP and PP
The ion(s) mediating the sADP and PP were investigated either by substitution experiments or by including specific channel blockers in the perfusate. In the first experiment, a role for Na+ was investigated by replacing extracellular Na+ with equimolar choline. When extracellular Na+ was reduced from 152 to 26 mM, both the sADP and PP were reversibly depressed (Fig. 5A; n = 6/6). A small amplitude sADP was still observed in low extracellular Na+ (6 ± 1 mV; range 3-10; n = 6), however, the amplitude of the depolarizing current injected was twofold greater. In a similar experiment, both the sADP and PP were reversibly abolished when extracellular Ca2+ was reduced from 2 to 0.1 mM (Fig. 5B; n = 4/4). In this experiment, extracellular Mg2+ was simultaneously increased from 2 to 10 mM to maintain the divalent cation surface charge (Hille, 1984
Fig. 5. Both the sADP and PP were dependent on Na+ influx, independent of TTX-sensitive channels and Ca2+ influx via HVA channels. A, In 20 µM carbachol, depolarizing current injection evoked both an sADP and a PP. Lowering external Na+ from 152 to 26 mM reversibly depressed the sADP and abolished the PP, suggesting that Na+ influx was required for these afterpotentials. The resting potentials before and after cholinergic stimulation were
[View Larger Version of this Image (39K GIF file)]
To determine whether voltage-activated Na+ channels were involved in sADP and PP genesis, 1.2 µM tetrodotoxin (TTX) was included in the perfusate (Fig. 5C; n = 5). In all neurons, both the sADP and PP were still observed after application of TTX. In the presence of TTX, not only were fast action potentials blocked, but the low-amplitude oscillations observed superimposed on the PP were also abolished (MacVicar, 1985
To determine the HVA channel subtypes involved in sADP and PP genesis, blockers of either L- or N-type channels were included in the perfusate (Fig. 6). In the presence of 20 µM carbachol, both a sADP and PP were evoked after intracellular current injection and spike firing. The addition of 10 µM nimodipine, an L-type channel blocker, to the perfusate depressed the sADP and abolished the PP (Fig. 6A; n = 4/4). Although an sADP of 11 ± 4 mV (range 6-22; n = 4) was still observed, the amplitude of the depolarizing current had been increased twofold. Similarly, coapplication of 1 µM
Fig. 6. The sADP and PP required Ca2+ influx through L- and N-type Ca2+ channels. A, In a CA1 pyramidal neuron, intracellular current injection revealed an sADP and a PP in the presence of 20 µM carbachol. The resting membrane potentials before and after cholinergic stimulation were
[View Larger Version of this Image (20K GIF file)]
Taken together, these data demonstrated that both Na+ and Ca2+ influx was critical for sADP and PP genesis. Moreover, Ca2+ influx occurred via HVA Ca2+ channels, predominantly of the L and N subtypes, whereas Na+ influx occurred independently of TTX-sensitive channels.
Ionic mechanisms underlying the sADP and PP
To elucidate whether Ca2+ influx functioned primarily as a charge carrier or as an intracellular messenger, [Ca2+]i was chelated by inclusion of 10 mM bis(2-aminophenoxy)ethane-N,N,N
Fig. 7. Both the sADP and PP were blocked by intracellular BAPTA. A, Typical responses of a hippocampal pyramidal neuron to hyperpolarizing and depolarizing current injection. Neither an sADP nor a PP was observed in the absence of cholinergic stimulation (A1). The calibration bars in the inset represent 40 msec and 20 mV. In the presence of carbachol, however, depolarizing current injection evoked a long-lasting PP (A2). This pyramidal neuron was loaded with pipette solution containing 1.1 mM EGTA and 0.1 mM Ca2+ and, thus, intracellular Ca2+ was bufferred to ~16 nM. B, A different pyramidal neuron, recorded from the same slice as the neuron illustrated in A, loaded with 10 mM BAPTA. In control aCSF, neither an sADP nor a PP was observed (B1). The calibration bars in the inset represent 40 msec and 20 mV. In the presence of carbachol, neither an sADP nor a PP could be evoked, suggesting that elevated [Ca2+]i was necessary for these potentials (B2).
[View Larger Version of this Image (23K GIF file)]
The goal of the next set of experiments was to determine whether the sADP and PP could be evoked by maximizing Ca2+ influx via K+ channel suppression. Two methods were used independently to suppress K+ channels. First, external K+ channel blockers [10 mM tetraethylammonium (TEA), 5 mM 4-aminopyridine (4-AP), 100 µM Ba2+; Fig. 8A; n = 9] were included in the perfusate, and when applied to pyramidal neurons, depolarized the membrane potential by 9 ± 1 mV (range 5-10; n = 9). Second, 40 mM Cs+ was included in the pipette solution ([Cs+]i; Fig. 8B; Table 1; n = 11). Both conditions would independently increase Ca2+ influx, and yet neither the sADP nor the PP could be elicited from a membrane potential maintained at
Fig. 8. Blockers of K+ channels failed to unmask either the sADP or the PP in the absence of cholinergic stimulation. A, The sADP and PP were not observed after application of 1.2 µM TTX and K+ channel blockers (10 mM TEA, 5 mM 4-AP, 100 µM Ba2+). Cholinergic stimulation, however, revealed a PP that was reversibly depressed by lowering Na+ from 152 to 26 mM in the external media (A1). Notice that robust Ca2+ spikes remained in low Na+, whereas the PP was reversibly depressed (A2). B, In addition, neither the sADP nor the PP was observed in pyramidal neurons loaded with 40 mM intracellular Cs+ and bathed in 1.2 µM TTX. As above, cholinergic stimulation revealed a PP that was reversibly depressed by lowering Na+ in the external media (B1). In this example, robust Ca2+ spikes also remained in low Na+, whereas the PP was reversibly depressed (B2).
[View Larger Version of this Image (32K GIF file)]
In the following experiments, the involvement of a Na+/Ca2+ exchanger was tested in two ways (Crépel et al., 1994
Fig. 9. The sADP and PP were independent of a Na+/Ca2+ exchanger. A, Intracellular current injection revealed an sADP and a PP in the presence of 20 µM carbachol. The resting membrane potentials before and after cholinergic stimulation were
[View Larger Version of this Image (35K GIF file)]
Taken together, these experiments indicate that both the sADP and PP require three events: cholinergic stimulation, an elevation in [Ca2+]i via HVA Ca2+ channels (L- and N-type), and activation of the Ca2+-activated nonselective cation conductance.
Effects of individual K+ channel blockers on the sADP and PP
Although the sADP and PP could not be unmasked by K+ channel suppression, once elicited, these waveforms are likely to be modulated by concurrent outward K+ conductances. The effects of individual K+ channel blockers, therefore, were tested on the sADP and PP to determine whether individual K+ conductances influenced the shape and/or duration of the afterpotential waveforms. In the absence of carbachol, the addition of 10 mM TEA to the perfusate resulted in an initial 5 ± 2 mV (range 2-7 mV; n = 3) depolarization of the membrane potential. When the membrane potential was stable, spike firing elicited by intracellular current injection revealed a brief PP, probably mediated by HVA Ca2+ channels activated by action potential firing (Fig. 10A; n = 3/3) (Bourque et al., 1986
Fig. 10. Individual K+ channel blockers modulate the PP waveform. A, Action potential firing in the presence of 10 mM TEA resulted in a brief plateau potential that was presumably Ca2+-dependent (A1). Neither an sADP nor a PP was observed after cessation of the depolarizing stimulus. The calibration bars in the inset represent 40 msec and 20 mV. In a different neuron, both the sADP and PP were observed in the presence of 20 µM carbachol (A2). Coapplication of 10 mM TEA abolished the sADP and decreased the duration of the PP. B, In the presence of 5 mM 4-AP, individual action potentials activated brief afterdepolarizations that presumably were Ca2+-dependent (B1). After cessation of the depolarizing current stimuli, a brief afterpotential was commonly observed. Neither the sADP nor the PP was observed. The calibration bars in the inset represent 40 msec and 20 mV. In another neuron, a PP was evoked in the presence of 20 µM carbachol (B2). Coapplication of 5 mM 4-AP slightly prolonged the PP. C, Application of 100 µM Ba2+ to the perfusate resulted in a brief afterpotential and subsequent spike broadening (C1). Brief afterpotentials were also observed after depolarizing current stimuli, however, neither the sADP nor the PP was evoked. In the presence of 20 µM carbachol, a different neuron exhibited an sADP and a PP after cessation of stimuli (C2). Coapplication of 100 µM Ba2+ to the perfusate increased the PP duration.
[View Larger Version of this Image (30K GIF file)]
In separate experiments, the addition of 5 mM 4-AP to the perfusate, in the absence of carbachol, resulted in a 3 ± 1 mV (range 1-4 mV; n = 3) depolarization of the membrane potential. This K+ channel blocker also increased Ca2+ influx, but instead of a single PP, which was observed after TEA perfusion, a transient potential followed each action potential (Fig. 10B; n = 3). After a burst of evoked action potentials, only a brief afterpotential was observed in 4-AP. In a different pyramidal neuron, a PP was evoked in the presence of 20 µM carbachol that was slightly prolonged by coapplication of 4-AP (Fig. 10B; n = 3/3). The duration of the PP was 11.3 ± 0.9 sec (range 9.7-12.8; n = 3) in carbachol versus 14.3 ± 1.1 sec (range 11.4-15; n = 3) in 4-AP. In addition, the membrane potential of the PP measured at 0.2 sec after cessation of the stimuli was increased from
In the absence of carbachol, the addition of 100 µM Ba2+ to the perfusate resulted in a 4 ± 1 mV (range 2-5; n = 3) depolarization of the membrane potential. This K+ channel blocker increased Ca2+ influx as evidenced by increased spike broadening (Fig. 10C; n = 3) (Bourque et al., 1986
In the absence of carbachol, the simultaneous addition of Ca2+-activated K+ channel blockers [100 nM iberiotoxin (ITX), 100 nM apamin] to the perfusate depolarized the neurons by 3 ± 1 (range 0-4; n = 4) and completely blocked the afterhyperpolarization after each action potential. In the presence of these blockers, however, neither the sADP nor the PP could be evoked (data not shown; n = 4/4). In different pyramidal neurons, both ITX and apamin failed to affect either the sADP or PP observed after carbachol application (n = 3/3). These experiments indicate that Ca2+-activated K+ conductances did not shape either the sADP or PP waveforms.
Taken together, these experiments again illustrate that although Ca2+ influx was increased via K+ channel depression, the sADP and PP required cholinergic stimulation. In addition, TEA may have an inhibitory affect on the Ca2+-activated nonselective cation channel, whereas a Ba2+-sensitive current (e.g., IM) was important for determining the duration of the PP waveform.
Conductance changes accompanying the PP
In the final experiments, changes in RIN were examined during the PP by injection of low-amplitude current pulses (
Fig. 11. The PP was associated with a large RIN decrease and could not be terminated by hyperpolarizing pulses. A, Cholinergic-dependent PPs illustrated on two time scales. In the latter, brief current injection (
[View Larger Version of this Image (29K GIF file)]
DISCUSSION
In this study, we report a cholinergic-induced sADP and PP recorded from hippocampal CA1 pyramidal neurons with the whole-cell patch-clamp technique. We propose that the PP represents a novel regenerative event involving the interplay between HVA Ca2+ channels (L- and N-type) and the Ca2+-activated nonselective cation conductance. These ionic mechanisms may contribute significantly to ictal depolarizations observed during temporal-lobe seizures of the partial-complex subtype (Lothman et al., 1991Both the sADP and PP were depressed by removal of either Na+ or Ca2+ from the external media, and blocked by either extracellular Cd2+ or chelation of [Ca2+]i by inclusion of BAPTA in the intracellular solution. Moreover, the sADP was depressed and the PP was abolished by either the L-type channel blocker, nimodipine, or the N-type channel blocker
One possible mechanism contributing to the sADP and PP described here is the Na+/Ca2+ exchanger (Friedman et al., 1992
A major question is whether the Ca2+-activated nonselective cation conductance was directly enhanced by carbachol or simply unmasked by cholinergic-induced suppression of K+ conductances (Caesar et al., 1993). Our data indicate that the Ca2+-activated nonselective cation conductance was directly enhanced by cholinergic stimulation. In the presence of either K+ channel blockers or [Cs+]i, neither the sADP nor the PP was observed. The sADP and PP were only elicited after carbachol was added to the perfusate. Because HVA Ca2+ channels are depressed by cholinergic stimulation (Toselli and Lux, 1989
Previous studies have shown that PPs can be generated by either voltage-activated Ca2+ or Na+ channels. PPs generated by Ca2+ channels alone, however, are observed only when K+ channel blockers are present, intracellular Ca2+ is chelated, and/or Ba2+ ions are used as the charge carriers (Llinas and Yarom, 1981
The Ca2+-activated nonselective cation conductance implicated in this study is present in a broad range of cell types (Partridge and Swandulla, 1988
Based on our findings, the sADP represents an afterpotential due to the Ca2+-activated nonselective cation conductance activated by Ca2+ influx via HVA channels. The PP, however, represents a novel regenerative event involving the interplay between HVA Ca2+ channels and the Ca2+-activated nonselective cation conductance. This interplay between channels may occur at a distal dendritic site because both a Ca2+-sensitive inward current (Benson et al., 1988
The sADP and PP described here involved intrinsic mechanisms directly modulated by cholinergic stimulation. These included enhancement of the Ca2+-activated nonselective cation conductance and depression of several K+ conductances. It is unlikely that other neurotransmitters (e.g., glutamate) or synaptic interactions played a significant role in this study because both the sADP and PP were observed in TTX. Moreover, thin slices (150 µm) were commonly used where synaptic connections and recurrent collaterals were minimal. Although other neurotransmitters and synaptic interactions were presumably not involved in sADP and PP genesis in this study, they likely play a significant physiological role. For example, previous work in cortical neurons has demonstrated a cholinergic-sensitive slow inward conductance potentiated by low-frequency synaptic stimulation of white matter (Andrade, 1991
Functional significance
Cholinergic agents are effective in generating hippocampal seizures both in vivo and in vitro (Lothman et al., 1991
FOOTNOTES
Received Feb. 27, 1996; revised April 2, 1996; accepted April 8, 1996.
This work was supported by a grant from the Medical Research Council of Canada (MRC). D.D.F. is a recipient of studentships from the MRC, Alberta Heritage Foundation for Medical Research (AHFMR), and Savoy Foundation for Epilepsy Research. B.A.M. is an AHFMR scientist and the Ciba Geigy chair for schizophrenia research. We are grateful to Drs. S. Barnes and G. Spencer for critical comments on this manuscript and Drs. A. R. McQuiston and W. F. Colmers for slice-patch advice.
Correspondence should be addressed to Douglas D. Fraser, Department of Neuroscience, 3330 Hospital Drive N.W., Health Sciences Building, University of Calgary, Alberta, Canada, T2N 4N1.
REFERENCES
- Alonso A, Llinas RR (1989) Subthreshold Na+-dependent theta-like rhythmicity in stellate cells of entorhinal cortex layer II. Nature 342:175-177 . [Medline]
- Alzheimer C (1994) A novel voltage-dependent cation current in rat neocortical neurones. J Physiol (Lond) 479:199-205 .
[Abstract/Free Full Text] - Andrade R (1991) Cell excitation enhances muscarinic cholinergic responses in rat association cortex. Brain Res 548:81-93 . [Web of Science][Medline]
- Behrends JC, Bruggencate G (1993) Cholinergic modulation of synaptic inhibition in the guinea pig hippocampus in vitro: excitation of GABAergic interneurons and inhibition of GABA-release. J Neurophysiol 69:626-629 .
[Abstract/Free Full Text] - Benson DM, Blitzer RD, Landau EM (1988) An analysis of the depolarization produced in guinea-pig hippocampus by cholinergic receptor stimulation. J Physiol (Lond) 404:479-496 .
[Abstract/Free Full Text] - Bernardo LS, Prince DA (1982) Cholinergic excitation of mammalian hippocampal pyramidal cells. Brain Res 249:315-331. [Web of Science][Medline]
- Bianchi R, Wong RKS (1994) Carbachol-induced synchronized rhythmic bursts in CA3 neurons of guinea pig hippocampus in vitro. J Neurophysiol 72:131-138 .
[Abstract/Free Full Text] - Bianchi R, Wong RKS (1995) Excitatory synaptic potentials dependent on metabotropic glutamate receptor activation in guinea pig hippocampal pyramidal neurons. J Physiol (Lond) 487:663-676 .
[Abstract/Free Full Text] - Bland BH (1986) The physiology and pharmacology of hippocampal formation theta rhythms. Prog Neurobiol 26:1-54 . [Web of Science][Medline]
- Blanton MG, Lo Turco JJ, Kriegstein AR (1989) Whole cell recording from neurons in slices of reptilian and mammalian cerebral cortex. J Neurosci Methods 30:203-210 . [Web of Science][Medline]
- Blitzer RD, Gil O, Omri G, Landau E (1991) Nifedipine blocks calcium-dependent cholinergic depolarization in the guinea pig hippocampus. Brain Res 542:293-299 . [Web of Science][Medline]
- Bourque CW, Brown DA, Renaud LP (1986) Barium ions induce prolonged plateau depolarizations in neurosecretory neurones of the adult rat supraoptic nucleus. J Physiol (Lond) 375:573-586 .
[Abstract/Free Full Text] - Brown KT, Flaming DG (1992) Advanced micropipette techniques for cell physiology, pp 176-203. .
- Caeser M, Brown DA, Gähwiler BH, Knöpfel T (1993) Characterization of a calcium-dependent current generating a slow afterdepolarization of CA3 pyramidal cells in rat hippocampal slice cultures. Eur J Neurosci 5:560-569 . [Web of Science][Medline]
- Colino A, Halliwell JV (1993) Carbachol potentiates Q current and activates a calcium-dependent non-specific conductance in rat hippocampus in vitro. Eur J Neurosci 5:1198-1209 . [Web of Science][Medline]
- Constanti A, Bagetta G (1991) Muscarinic receptor activation induces a prolonged post-stimulus afterdepolarization with a conductance decrease in guinea-pig olfactory cortex neurones in vitro. Neurosci Lett 131:27-32 . [Web of Science][Medline]
- Constanti A, Bagetta G, Libri V (1993) Persistent muscarinic excitation in guinea pig olfactory cortex neurons: involvement of a slow post-stimulus afterdepolarizing current. Neuroscience 56:887-904 . [Web of Science][Medline]
- Crépel V, Aniksztejn L, Ben-Ari Y, Hammond C (1994) Glutamate metabotropic receptors increase a Ca2+-activated nonspecific cationic current in CA1 hippocampal neurons. J Neurophysiol 72:1561-1569 .
[Abstract/Free Full Text] - Deisz RA (1996) A tetrodotoxin-insensitive sodium current initiates burst firing of neocortical neurons. Neuroscience 70:341-351. [Web of Science][Medline]
- Edwards FA, Konnerth A, Sakmann B, Takahashi T (1989) A thin slice preparation for patch clamp recordings from neurons of the mammalian central nervous system. Pflügers Arch 414:600-612 . [Web of Science][Medline]
- Fraser DD, MacVicar BA (1991) Low-threshold transient Ca2+ current in lacunosum-moleculare interneurons: kinetics and modulation by neurotransmitters. J Neurosci 11:2812-2820 . [Abstract]
- Fraser DD, MacVicar BA (1995) Ionic mechanisms underlying the cholinergic-dependent plateau potentials in hippocampal CA1 pyramidal neurons. Soc Neurosci Abstr 25:32.
- Friedman A, Arens J, Heinemann U, Gutnick MJ (1992) Slow depolarizing afterpotentials in neocortical neurons are sodium and calcium dependent. Neurosci Lett 135:13-17 . [Web of Science][Medline]
- Gähwiler BH (1984) Facilitation by acetylcholine of tetrodotoxin-resistant spikes in rat hippocampal pyramidal cells. Neuroscience 11:381-388 . [Web of Science][Medline]
- García-Muñoz A, Barrio LC, Buno W (1993) Membrane potential oscillations in CA1 hippocampal pyramidal neurons in vitro: intrinsic rhythms and fluctuations entrained by sinusoidal injected current. Exp Brain Res 97:325-333. [Web of Science][Medline]
- Glynn IM (1993) All hands to sodium pump. J Physiol (Lond) 462:1-30 .
[Free Full Text] - Halliwell JV (1990) Physiological mechanisms of cholinergic action in the hippocampus. Prog Brain Res 84:255-272 . [Web of Science][Medline]
- Halliwell JV, Adams PR (1982) Voltage-clamp analysis of muscarinic excitation in hippocampal neurons. Brain Res 250:71-92 . [Web of Science][Medline]
- Hasuo H, Gallagher JP (1990) Facilitatory action of muscarine on the slow afterdepolarization of rat dorsolateral septal nucleus neurons in vitro. Neurosci Lett 112:234-238 . [Web of Science][Medline]
- Hasuo H, Phelan KD, Twery MJ, Gallagher JP (1990) A calcium-dependent afterdepolarization recorded in rat dorsolateral septal nucleus neurons in vitro. J Neurophysiol 64:1838-1846 .
[Abstract/Free Full Text] - Hess P, Tsien RW (1984) Mechanism of ion permeation through calcium channels. Nature 309:453-456 . [Medline]
- Hille BH (1984) Ionic channels of excitable membranes. .
- Hoehn K, Watson TWJ, MacVicar BA (1993) A novel tetrodotoxin-insensitive, slow sodium current in striatal and hippocampal neurons. Neuron 10:543-552 . [Web of Science][Medline]
- Jones OT, Kunze DL, Angelides KJ (1989) Localization and mobility of
[Abstract/Free Full Text] - Kimura JE, Reeves H (1979) The effect of temperature on the asymmetrical charge movement in squid giant axons. J Physiol (Lond) 289:479-500 .
[Abstract/Free Full Text] - Kimura J, Miyamae S, Noma A (1987) Identification of a sodium-calcium exchange current in single ventricular cells of guinea-pig. J Physiol (Lond) 384:199-222 .
[Abstract/Free Full Text] - Konopacki J, Bland BH, MacIver MB, Roth SH (1987) Cholinergic theta rhythm in transected hippocampal slices: independent CA1 and dentate generators. Brain Res 417:399-407 . [Web of Science][Medline]
- Krnjevi
K (1993) Central cholinergic mechanisms and function. Prog Brain Res 98:285-292 . [Web of Science][Medline]
- Leung LS, Yim CYC (1991) Intrinsic membrane potential oscillations in hippocampal neurons in vitro. Brain Res 553:261-274. [Web of Science][Medline]
- Llinas R, Yarom Y (1981) Properties and distribution of ionic conductances generating electroresponsiveness of mammalian inferior olivary neurones in vitro. J Physiol (Lond) 315:569-584 .
[Abstract/Free Full Text] - Lothman EW, Bertram EH, Stringer JL (1991) Functional anatomy of hippocampal seizures. Prog Neurobiol 37:1-82 . [Web of Science][Medline]
- MacVicar BA (1985) Depolarizing prepotentials are Na+ dependent in CA1 pyramidal neurons. Brain Res 333:378-381 . [Web of Science][Medline]
- MacVicar BA, Tse FWY (1989) Local neuronal circuitry underlying cholinergic rhythmical slow activity in CA3 area of rat hippocampal slices. J Physiol (Lond) 417:197-212 .
[Abstract/Free Full Text] - Madison DV, Malenka RC, Nicoll RA (1987) Voltage clamp analysis of cholinergic action in the hippocampus. J Neurosci 7:733-741 . [Abstract]
- Magee JC, Johnston D (1995) Synaptic activation of voltage-gated channels in the dendrites of hippocampal pyramidal neurons. Science 268:301-304 .
[Abstract/Free Full Text] - Markram H, Segal M (1992) The inositol 1,4,5-triphosphate pathway mediates cholinergic potentiation of rat hippocampal neuronal responses to NMDA. J Physiol (Lond) 447:513-533 .
[Abstract/Free Full Text] - McCormick DA (1993) Actions of acetylcholine in the cerebral cortex and thalamus and implications for function. Prog Brain Res 98:303-308 . [Web of Science][Medline]
- McCormick DA, Prince DA (1986) Mechanisms of action of acetylcholine in the guinea-pig cerebral cortex in vitro. J Physiol (Lond) 375:169-194 .
[Abstract/Free Full Text] - Mills LR, Niesen CE, So AP, Carlen PL, Spigelman I, Jones OT (1994) N-type Ca2+ channels are located on somata, dendrites, and a subpopulation of dendritic spines on live hippocampal pyramidal neurons. J Neurosci 14:6815-6824 . [Abstract]
- Misgeld U, Calabresi P, Dodt HU (1986) Muscarinic modulation of calcium dependent plateau potentials in rat neostriatal neurons. Pflügers Arch 407:482-487 . [Web of Science][Medline]
- Müller W, Connor JA (1991) Cholinergic input uncouples Ca2+ changes from K+ conductance activation and amplifies intradendritic Ca2+ changes in hippocampal neurons. Neuron 6:901-905 . [Web of Science][Medline]
- Müller W, Misgeld U, Heinemann U (1988) Carbachol effects on hippocampal neurons in vitro: dependence on the rate of rise of carbachol tissue concentration. Exp Brain Res 72:287-298 . [Web of Science][Medline]
- Nakajima Y, Nakajima S, Leonard RJ, Yamaguchi K (1986) Acetylcholine raises excitability by inhibiting the fast transient potassium current in cultured hippocampal neurons. Proc Natl Acad Sci USA 83:3022-3026 .
[Abstract/Free Full Text] - Partridge LD, Swandulla D (1988) Ca2+-activated non-specific cation channels. Trends Neurosci 11:69-72 . [Web of Science][Medline]
- Penington NJ, Kelly JS (1993) Ionic dependence of a slow inward tail current in rat dorsal raphe neurones. J Physiol (Lond) 464:33-48 .
[Abstract/Free Full Text] - Pitler TA, Alger BE (1992) Cholinergic excitation of GABAergic interneurons in the rat hippocampal slices. J Physiol (Lond) 450:127-142 .
[Abstract/Free Full Text] - Reuter H, Porzig H (1995) Localization and functional significance of the Na+/Ca2+ exchanger in presynaptic boutons of hippocampal cells in culture. Neuron 15:1077-1084 . [Web of Science][Medline]
- Schwindt PC, Spain WJ, Foehring RC, Chubb MC, Crill WE (1988) Slow conductances in neurons from cat sensorimotor cortex in vitro and their role in slow excitability changes. J Neurophysiol 59:450-467 .
[Abstract/Free Full Text] - Segal M (1992) Acetylcholine enhances NMDA-evoked calcium rise in hippocampal neurons. Brain Res 587:83-87 . [Web of Science][Medline]
- Segal MM (1994) Endogenous bursts underlie seizurelike activity in solitary excitatory hippocampal neurons in microcultures. J Neurophysiol 72:1874-1884 .
[Abstract/Free Full Text] - Shen KZ, North RA (1992) Muscarine increases cation conductance and decreases potassium conductance in rat locus coeruleus neurones. J Physiol (Lond) 455:471-485 .
[Abstract/Free Full Text] - Shen Y, Specht SM, De Saint Ghislain I, Li R (1994) The hippocampus: a biological model for studying learning and memory. Prog Neurobiol 44:485-496 . [Web of Science][Medline]
- Spruston N, Johnston D (1992) Perforated patch-clamp analysis of the passive membrane properties of three classes of hippocampal neurons. J Neurophysiol 67:508-529 .
[Abstract/Free Full Text] - Stabel J, Ficker E, Heinemann U (1992) Young CA1 pyramidal cells of rats, but not dentate gyrus granule cells, express a delayed inward rectifying current with properties of IQ. Neurosci Lett 135:231-234 . [Web of Science][Medline]
- Staley KJ, Otis TS, Mody I (1992) Membrane properties of dentate gyrus granule cells: comparison of sharp microelectrodes and whole-cell recordings. J Neurophysiol 67:1346-1358 .
[Abstract/Free Full Text] - Taylor CP (1993) Na+ currents that fail to inactivate. Trends Neurosci 16:455-460 . [Web of Science][Medline]
- Toselli M, Lux HD (1989) Opposing effects of acetylcholine on the two classes of voltage-dependent calcium channels in hippocampal neurons. In: Central cholinergic synaptic transmission (Frotscher, M, Misgeld, U, eds) , p. 97. Basel: Birkhäuser.
- Vanderwolf CH (1988) Cerebral activity and behavior: control by central cholinergic and serotonergic systems. Int Rev Neurobiol 30:225-340 . [Web of Science][Medline]
- Wainer BH, Steininger TL, Roback JD, Burke-Watson MA, Mufson EJ, Kordower J (1993) Ascending cholinergic pathways: functional organization and implications for disease models. Prog Brain Res 98:9-30 . [Web of Science][Medline]
- Wasterlain CG, Fujikawa DG, Penix L, Sankar R (1993) Pathophysiological mechanisms of brain damage from status epilepticus. Epilepsia 34:S37-S53 .
- Westenbroek RE, Ahlijanian MK, Catterall WA (1990) Clustering of L-type Ca2+ channels at the base of major dendrites in hippocampal pyramidal neurons. Nature 347:281-284 . [Medline]
- Williams S, Samulack DD, Beaulieu C, Lacaille JC (1994) Membrane properties and synaptic responses of interneurons located near the stratum lacunosum-moleculare/radiatum border of area CA1 in whole-cell recordings from rat hippocampal slices. J Neurophysiol 71:2217-2235 .
[Abstract/Free Full Text] - Yaari Y, Jensen MS (1989) Cholinergic modulation of hippocampal epileptic activity in vitro. In: Central cholinergic synaptic transmission (Frotscher, M, Misgeld, U, eds) , p. 150. Basel: Birkhäuser.
- Yellen G (1982) Single Ca2+-activated non-selective cation channels in neuroblastoma. Nature 296:357-359 . [Medline]
Copyright ©1996 Society for Neuroscience 0270-6474/1996/164113-16$05.00/0
This article has been cited by other articles:
B. Javan and E. P. Zehr
Short-Term Plasticity of Spinal Reflex Excitability Induced by Rhythmic Arm Movement
J Neurophysiol, April 1, 2008; 99(4): 2000 - 2005.
[Abstract] [Full Text] [PDF]
R. Teruyama and W. E. Armstrong
Calcium-Dependent Fast Depolarizing Afterpotentials in Vasopressin Neurons in the Rat Supraoptic Nucleus
J Neurophysiol, November 1, 2007; 98(5): 2612 - 2621.
[Abstract] [Full Text] [PDF]
R. T. Pressler, T. Inoue, and B. W. Strowbridge
Muscarinic Receptor Activation Modulates Granule Cell Excitability and Potentiates Inhibition onto Mitral Cells in the Rat Olfactory Bulb
J. Neurosci., October 10, 2007; 27(41): 10969 - 10981.
[Abstract] [Full Text] [PDF]
R. Yamamoto, Y. Ueta, and N. Kato
Dopamine Induces a Slow Afterdepolarization in Lateral Amygdala Neurons
J Neurophysiol, August 1, 2007; 98(2): 984 - 992.
[Abstract] [Full Text] [PDF]
S. Makani and M. Chesler
Endogenous Alkaline Transients Boost Postsynaptic NMDA Receptor Responses in Hippocampal CA1 Pyramidal Neurons
J. Neurosci., July 11, 2007; 27(28): 7438 - 7446.
[Abstract] [Full Text] [PDF]
A. Y. Hung and N. S. Magoski
Activity-Dependent Initiation of a Prolonged Depolarization in Aplysia Bag Cell Neurons: Role for a Cation Channel
J Neurophysiol, March 1, 2007; 97(3): 2465 - 2479.
[Abstract] [Full Text] [PDF]
D. A. Lupinsky and N. S. Magoski
Ca2+-dependent regulation of a non-selective cation channel from Aplysia bag cell neurones
J. Physiol., September 1, 2006; 575(2): 491 - 506.
[Abstract] [Full Text] [PDF]
C. Tai, J. B. Kuzmiski, and B. A. MacVicar
Muscarinic enhancement of R-type calcium currents in hippocampal CA1 pyramidal neurons.
J. Neurosci., June 7, 2006; 26(23): 6249 - 6258.
[Abstract] [Full Text] [PDF]
W.-C. Li, S. R. Soffe, E. Wolf, and A. Roberts
Persistent Responses to Brief Stimuli: Feedback Excitation among Brainstem Neurons
J. Neurosci., April 12, 2006; 26(15): 4026 - 4035.
[Abstract] [Full Text] [PDF]
N. S. Desai and E. C. Walcott
Synaptic bombardment modulates muscarinic effects in forelimb motor cortex.
J. Neurosci., February 22, 2006; 26(8): 2215 - 2226.
[Abstract] [Full Text] [PDF]
S.-i. Sekizawa and A. C. Bonham
Group I Metabotropic Glutamate Receptors on Second-Order Baroreceptor Neurons Are Tonically Activated and Induce a Na+-Ca2+ Exchange Current
J Neurophysiol, February 1, 2006; 95(2): 882 - 892.
[Abstract] [Full Text] [PDF]
K. P. Carlin, Y. Dai, and L. M. Jordan
Cholinergic and Serotonergic Excitation of Ascending Commissural Neurons in the Thoraco-Lumbar Spinal Cord of the Neonatal Mouse
J Neurophysiol, February 1, 2006; 95(2): 1278 - 1284.
[Abstract] [Full Text] [PDF]
J. I. Kass and I. M. Mintz
Silent plateau potentials, rhythmic bursts, and pacemaker firing: Three patterns of activity that coexist in quadristable subthalamic neurons
PNAS, January 3, 2006; 103(1): 183 - 188.
[Abstract] [Full Text] [PDF]
J. P Meeks, X. Jiang, and S. Mennerick
Action potential fidelity during normal and epileptiform activity in paired soma-axon recordings from rat hippocampus
J. Physiol., July 15, 2005; 566(2): 425 - 441.
[Abstract] [Full Text] [PDF]
W. W. Wu, C. S. Chan, and J. F. Disterhoft
Slow Afterhyperpolarization Governs the Development of NMDA Receptor-Dependent Afterdepolarization in CA1 Pyramidal Neurons During Synaptic Stimulation
J Neurophysiol, October 1, 2004; 92(4): 2346 - 2356.
[Abstract] [Full Text] [PDF]
J. Magistretti, L. Ma, M. H. Shalinsky, W. Lin, R. Klink, and A. Alonso
Spike Patterning by Ca2+-Dependent Regulation of a Muscarinic Cation Current in Entorhinal Cortex Layer II Neurons
J Neurophysiol, September 1, 2004; 92(3): 1644 - 1657.
[Abstract] [Full Text] [PDF]
Y. Schiller
Activation of a Calcium-Activated Cation Current During Epileptiform Discharges and Its Possible Role in Sustaining Seizure-Like Events in Neocortical Slices
J Neurophysiol, August 1, 2004; 92(2): 862 - 872.
[Abstract] [Full Text] [PDF]
N. C. Dembrow, J. Jing, V. Brezina, and K. R. Weiss
A Specific Synaptic Pathway Activates a Conditional Plateau Potential Underlying Protraction Phase in the Aplysia Feeding Central Pattern Generator
J. Neurosci., June 2, 2004; 24(22): 5230 - 5238.
[Abstract] [Full Text] [PDF]
F. J. Michel, J. M. Robillard, and L.-E. Trudeau
Regulation of rat mesencephalic GABAergic neurones through muscarinic receptors
J. Physiol., April 15, 2004; 556(2): 429 - 445.
[Abstract] [Full Text] [PDF]
P. Nickolls, D. F. Collins, R. B. Gorman, D. Burke, and S. C. Gandevia
Forces consistent with plateau-like behaviour of spinal neurons evoked in patients with spinal cord injuries
Brain, March 1, 2004; 127(3): 660 - 670.
[Abstract] [Full Text] [PDF]
P. Zhong, Z. Gu, X. Wang, H. Jiang, J. Feng, and Z. Yan
Impaired Modulation of GABAergic Transmission by Muscarinic Receptors in a Mouse Transgenic Model of Alzheimer's Disease
J. Biol. Chem., July 11, 2003; 278(29): 26888 - 26896.
[Abstract] [Full Text] [PDF]
J. Baufreton, M. Garret, A. Rivera, A. de la Calle, F. Gonon, B. Dufy, B. Bioulac, and A. Taupignon
D5 (Not D1) Dopamine Receptors Potentiate Burst-Firing in Neurons of the Subthalamic Nucleus by Modulating an L-Type Calcium Conductance
J. Neurosci., February 1, 2003; 23(3): 816 - 825.
[Abstract] [Full Text] [PDF]
J. Kim, M. Isokawa, C. Ledent, and B. E. Alger
Activation of Muscarinic Acetylcholine Receptors Enhances the Release of Endogenous Cannabinoids in the Hippocampus
J. Neurosci., December 1, 2002; 22(23): 10182 - 10191.
[Abstract] [Full Text] [PDF]
B. J Hall and K. R Delaney
Contribution of a calcium-activated non-specific conductance to NMDA receptor-mediated synaptic potentials in granule cells of the frog olfactory bulb
J. Physiol., September 15, 2002; 543(3): 819 - 834.
[Abstract] [Full Text] [PDF]
T. G. Hornby, J. C. McDonagh, R. M. Reinking, and D. G. Stuart
Effects of Excitatory Modulation on Intrinsic Properties of Turtle Motoneurons
J Neurophysiol, July 1, 2002; 88(1): 86 - 97.
[Abstract] [Full Text] [PDF]
S. Schuchmann, H. Meierkord, K. Stenkamp, J. Breustedt, O. Windmuller, U. Heinemann, and K. Buchheim
Synaptic and Nonsynaptic Ictogenesis Occurs at Different Temperatures in Submerged and Interface Rat Brain Slices
J Neurophysiol, June 1, 2002; 87(6): 2929 - 2935.
[Abstract] [Full Text] [PDF]
J. B. Kuzmiski and B. A. MacVicar
Cyclic Nucleotide-Gated Channels Contribute to the Cholinergic Plateau Potential in Hippocampal CA1 Pyramidal Neurons
J. Neurosci., November 15, 2001; 21(22): 8707 - 8714.
[Abstract] [Full Text] [PDF]
R. A Morton, N. A Manuel, D. O Bulters, S. R Cobb, and C. H Davies
Regulation of muscarinic acetylcholine receptor-mediated synaptic responses by GABAB receptors in the rat hippocampus
J. Physiol., September 15, 2001; 535(3): 757 - 766.
[Abstract] [Full Text] [PDF]
M. D'Antuono, H. Kawasaki, C. Palmieri, and M. Avoli
Network and Intrinsic Contributions to Carbachol-Induced Oscillations in the Rat Subiculum
J Neurophysiol, September 1, 2001; 86(3): 1164 - 1178.
[Abstract] [Full Text] [PDF]
G. G. Somjen
Mechanisms of Spreading Depression and Hypoxic Spreading Depression-Like Depolarization
Physiol Rev, July 1, 2001; 81(3): 1065 - 1096.
[Abstract] [Full Text] [PDF]
D. F. Collins, D. Burke, and S. C. Gandevia
Large Involuntary Forces Consistent with Plateau-Like Behavior of Human Motoneurons
J. Neurosci., June 1, 2001; 21(11): 4059 - 4065.
[Abstract] [Full Text] [PDF]
D. D. Fraser, D. Doll, and B. A. MacVicar
Serine/Threonine Protein Phosphatases and Synaptic Inhibition Regulate the Expression of Cholinergic-Dependent Plateau Potentials
J Neurophysiol, March 1, 2001; 85(3): 1197 - 1205.
[Abstract] [Full Text] [PDF]
D. Saar, Y. Grossman, and E. Barkai
Long-Lasting Cholinergic Modulation Underlies Rule Learning in Rats
J. Neurosci., February 15, 2001; 21(4): 1385 - 1392.
[Abstract] [Full Text] [PDF]
S. Royer, M. Martina, and D. Pare
Bistable Behavior of Inhibitory Neurons Controlling Impulse Traffic through the Amygdala: Role of a Slowly Deinactivating K+ Current
J. Neurosci., December 15, 2000; 20(24): 9034 - 9039.
[Abstract] [Full Text] [PDF]
D. L S Washburn, J. W Anderson, and A. V Ferguson
A subthreshold persistent sodium current mediates bursting in rat subfornical organ neurones
J. Physiol., December 1, 2000; 529(2): 359 - 371.
[Abstract] [Full Text] [PDF]
G. V. Di Prisco, E. Pearlstein, D. Le Ray, R. Robitaille, and R. Dubuc
A Cellular Mechanism for the Transformation of a Sensory Input into a Motor Command
J. Neurosci., November 1, 2000; 20(21): 8169 - 8176.
[Abstract] [Full Text] [PDF]
H. Kager, W. J. Wadman, and G. G. Somjen
Simulated Seizures and Spreading Depression in a Neuron Model Incorporating Interstitial Space and Ion Concentrations
J Neurophysiol, July 1, 2000; 84(1): 495 - 512.
[Abstract] [Full Text] [PDF]
S. M Beier and M. E Barish
Cholinergic stimulation enhances cytosolic calcium ion accumulation in mouse hippocampal CA1 pyramidal neurones during short action potential trains
J. Physiol., July 1, 2000; 526(1): 129 - 142.
[Abstract] [Full Text] [PDF]
X. M. Shao and J. L. Feldman
Acetylcholine Modulates Respiratory Pattern: Effects Mediated by M3-Like Receptors in PreBotzinger Complex Inspiratory Neurons
J Neurophysiol, March 1, 2000; 83(3): 1243 - 1252.
[Abstract] [Full Text] [PDF]
H. Yoshimura and N. Kato
Diverse roles of intracellular cAMP in early synaptic modifications in the rat visual cortex
J. Physiol., February 1, 2000; 522(3): 417 - 426.
[Abstract] [Full Text] [PDF]
H. Kawasaki, C. Palmieri, and M. Avoli
Muscarinic Receptor Activation Induces Depolarizing Plateau Potentials in Bursting Neurons of the Rat Subiculum
J Neurophysiol, November 1, 1999; 82(5): 2590 - 2601.
[Abstract] [Full Text] [PDF]
V. Morisset and F. Nagy
Ionic Basis for Plateau Potentials in Deep Dorsal Horn Neurons of the Rat Spinal Cord
J. Neurosci., September 1, 1999; 19(17): 7309 - 7316.
[Abstract] [Full Text] [PDF]
A. R. McQuiston and D. V. Madison
Muscarinic Receptor Activity Induces an Afterdepolarization in a Subpopulation of Hippocampal CA1 Interneurons
J. Neurosci., July 15, 1999; 19(14): 5703 - 5710.
[Abstract] [Full Text] [PDF]
S. R Cobb, D. O Bulters, S. Suchak, G. Riedel, R. G M Morris, and C. H Davies
Activation of nicotinic acetylcholine receptors patterns network activity in the rodent hippocampus
J. Physiol., July 1, 1999; 518(1): 131 - 140.
[Abstract] [Full Text] [PDF]
B. Carette
Characterization of Carbachol-Induced Rhythmic Bursting Discharges in Neurons From Guinea Pig Lateral Septum Slices
J Neurophysiol, September 1, 1998; 80(3): 1042 - 1055.
[Abstract] [Full Text] [PDF]
S. Haj-Dahmane and R. Andrade
Ionic Mechanism of the Slow Afterdepolarization Induced by Muscarinic Receptor Activation in Rat Prefrontal Cortex
J Neurophysiol, September 1, 1998; 80(3): 1197 - 1210.
[Abstract] [Full Text] [PDF]
P. A. Rutecki and Y. Yang
Ictal Epileptiform Activity in the CA3 Region of Hippocampal Slices Produced by Pilocarpine
J Neurophysiol, June 1, 1998; 79(6): 3019 - 3029.
[Abstract] [Full Text] [PDF]
G. Svirskis and J. Hounsgaard
Transmitter Regulation of Plateau Properties in Turtle Motoneurons
J Neurophysiol, January 1, 1998; 79(1): 45 - 50.
[Abstract] [Full Text] [PDF]
J. C. Rekling and J. L. Feldman
Calcium-Dependent Plateau Potentials in Rostral Ambiguus Neurons in the Newborn Mouse Brain Stem In Vitro
J Neurophysiol, November 1, 1997; 78(5): 2483 - 2492.
[Abstract] [Full Text] [PDF]
H. Tsubokawa and W. N. Ross
Muscarinic Modulation of Spike Backpropagation in the Apical Dendrites of Hippocampal CA1 Pyramidal Neurons
J. Neurosci., August 1, 1997; 17(15): 5782 - 5791.
[Abstract] [Full Text] [PDF]
P. Congar, X. Leinekugel, Y. Ben-Ari, and V. Crepel
A Long-Lasting Calcium-Activated Nonselective Cationic Current Is Generated by Synaptic Stimulation or Exogenous Activation of Group I Metabotropic Glutamate Receptors in CA1 Pyramidal Neurons
J. Neurosci., July 15, 1997; 17(14): 5366 - 5379.
[Abstract] [Full Text] [PDF]
H. S. Lukatch and M. B. Maciver
Physiology, Pharmacology, and Topography of Cholinergic Neocortical Oscillations In Vitro
J Neurophysiol, May 1, 1997; 77(5): 2427 - 2445.
[Abstract] [Full Text] [PDF]
R. Klink and A. Alonso
Ionic Mechanisms of Muscarinic Depolarization in Entorhinal Cortex Layer II Neurons
J Neurophysiol, April 1, 1997; 77(4): 1829 - 1843.
[Abstract] [Full Text] [PDF]
This Article Abstract 
Full Text (PDF) Submit an eLetter Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in Web of Science Similar articles in PubMed Alert me to new issues of the journal Download to citation manager 
Citing Articles Citing Articles via HighWire Citing Articles via Web of Science (95) Citing Articles via Google Scholar Google Scholar Articles by Fraser, D. D. Articles by MacVicar, B. A. Search for Related Content PubMed PubMed Citation Articles by Fraser, D. D. Articles by MacVicar, B. A.
ABSTRACT
|
|
|
|
 |
|