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Department of Neuroscience, Nobel Institute for Neurophysiology, Karolinska Institutet, S-171 77 Stockholm, Sweden
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ABSTRACT |
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 Abstract
 Introduction
Methods
Results
Discussion
References
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El Manira, A. and N. Bussières. Calcium channel subtypes in lamprey sensory and motor neurons. J. Neurophysiol. 78: 1334-1340, 1997. Pharmacologically distinct calcium channels have been characterized in dissociated cutaneous sensory neurons and motoneurons of the larval lamprey spinal cord. To enable cell identification, sensory dorsal cells and motoneurons were selectively labeled with fluorescein-coupled dextran amine in the intact spinal cord in vitro before dissociation. Calcium channels present in sensory dorsal cells, motoneurons, and other spinal cord neurons were characterized with the use of whole cell voltage-clamp recordings and specific calcium channel agonist and antagonists. The results show that a transient low-voltage-activated (LVA) calcium current was present in a proportion of sensory dorsal cells but not in motoneurons, whereas high-voltage-activated (HVA) calcium currents were seen in all neurons recorded. The different components of HVA current were dissected pharmacologically and similar results were obtained for both dorsal cells and motoneurons. The N-type calcium channel antagonist 
-conotoxin-GVIA(-CgTx) blocked >70% of the HVA current. A large part of the -CgTx block was reversed after washout of the toxin. The L-type calcium channel antagonist nimodipine blocked ~15% of the total HVA current. The dihydropyridine agonist (±)-BayK 8644 markedly increased the amplitude of the calcium channel current. The BayK-potentiated current was not affected by -CgTx, indicating that the reversibility of the -CgTx effect is not due to a blockade of L-type channels. Simultaneous application of -CgTx and nimodipine left ~15% of the HVA calcium channel current, a small part of which was blocked by the P/Q-type channel antagonist -agatoxin-IVA. In the presence of the three antagonists, the persistent residual current (~10%) was completely blocked by cadmium. Our results provide evidence for the existence of HVA calcium channels of the N, L, and P/Q types and other HVA calcium channels in lamprey sensory neurons and motoneurons. In addition, certain types of neurons express LVA calcium channels.
Activation of voltage-gated calcium channels controls a variety of neuronal processes, including neurotransmitter release and ion channel activation or inactivation (see Hille 1992 Retrograde labeling of spinal neurons
Larval lampreys (Petromyzon marinus) 10-14 cm long were anesthetized with tricaine methane sulfonate (100 mg/l) and eviscerated and the notochord/spinal cord was dissected out in cooled oxygenated physiological solution composed of (in mM) 138 NaCl, 2.1 KCl, 1.8 CaCl2, 1.2 MgCl2, 4 glucose, 2 N-2-hydroxyethylpiperazine-N Dissociation and culture of neurons
The dissociation was carried out in Leibovitz's L-15 culture medium (Sigma) supplemented with glutamine (2 mM), gentamicin (1 µg/ml), and penicillin-streptomycin (2 µl/ml), osmolarity adjusted to 270 mosM. The spinal cord was incubated in collagenase (2 mg/ml, 30 min, Sigma) and then in protease (2 mg/ml, 45 min, Sigma). The tissue was washed with culture medium and triturated through a sterilized pipette. The supernatant containing the dissociated cells was distributed in 35-mm poly-D-lysine-coated petri dishes (Falcon) that contained 2 ml of the culture medium. The dissociated neurons were incubated at 8°C for 1-15 days. The medium was changed every third day.
Electrophysiology
Whole cell recordings were performed on somata of spinal cord neurons with the use of an Axopatch 200A patch-clamp amplifier. Pipettes with resistances of 2-5 M Properties of calcium channel currents
Whole cell recordings were made from somata of FDA-prelabeled motoneurons (Fig. 1, A and B), skin sensory neurons (dorsal cells; Fig. 1, C and D), and unidentified spinal cord neurons. The cells were dissociated and maintained in culture for 1-15 days. Calcium currents were elicited by depolarizing voltage steps from a holding potential of
Pharmacology of calcium channel currents
To determine the types of HVA calcium channels present in lamprey spinal cord neurons, a pharmacological dissection of the total barium current was carried out. The membrane potential of the recorded neurons was held at
Types of calcium channels present in motoneurons and sensory dorsal cells
To test whether the N and L type channels were the only HVA calcium channels present in motoneurons and dorsal cells in the lamprey spinal cord or whether other types of HVA channels were also present, specific antagonists were applied simultaneously. Calcium channel currents were elicited in an FDA-prelabeled motoneuron by voltage steps to
These experiments demonstrate the presence of LVA and HVA calcium channels in lamprey spinal cord neurons (see also Matsushima et al. 1993
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
). In the lamprey locomotor network, the intracellular calcium level in spinal neurons phasically fluctuates during locomotor activity (Bacskai et al. 1995). Both low-voltage-activated (LVA) and high-voltage-activated (HVA) calcium channels are present in lamprey spinal cord neurons (Matsushima et al. 1993). These can be modulated by different transmitters, for example 
-aminobutyric acid, dopamine, and serotonin (El Manira et al. 1997; Matsushima et al. 1993; Schotland et al. 1995), resulting in changes in firing frequency and the strength of synaptic transmission (see Grillner et al. 1995). Although the modulation of calcium channels has been studied in some detail, the specific types of LVA and HVA calcium channels present in different lamprey spinal neurons and their relative responsiveness to different modulators require further study. Characterization of the types and properties of calcium channels in identified spinal cord neurons is necessary to provide insight into their specific roles and the functional significance of these channels for neuromodulation.
; Llinás et al. 1992; Mintz et al. 1992; Nowycky et al. 1985; Pearson et al. 1995; Randall and Tsien 1995). Furthermore, molecular cloning has allowed the identification of additional calcium channels that are widely distributed in the nervous system (see Birnbaumer et al. 1994; Snutch and Reiner 1992; Tsien et al. 1991). These different calcium channels contribute to various physiological functions and they can be differentially controlled by specific neuromodulators (Bean 1989; Tsien et al. 1988).
). In chick embryo dorsal root ganglion neurons and sympathetic neurons of both rat and frog, the calcium current is mediated largely through N-type channels (Boland et al. 1994; Cox and Dunlap 1992). Spinal cord neurons in the Xenopus embryo also possess -conotoxin-GVIA (-CgTx)-sensitive calcium channels, but they do not exhibit any dihydropyridine-sensitive L-type channels (Barish 1991; Wall and Dale 1994). The relative contribution of the different calcium channel subtypes to the total calcium current in spinal cord neurons thus varies between the species and the cell type studied.
). To understand the relative roles of the different calcium channels, it is necessary to define their pharmacological profile as well as their relative contribution to the total calcium current in different types of spinal neurons. This will provide information on whether the same pharmacological classification of calcium channels applies to lower vertebrates. In the present study we utilized whole cell patch-clamp techniques on identified cutaneous sensory neurons, dorsal cells, and motoneurons to determine the different types of calcium channels present. Using specific agonists and antagonists, we provide evidence for the existence of N-, L-, and P/Q-type calcium channels in motoneurons, cutaneous sensory dorsal cells, and other unidentified spinal neurons. The study of calcium channels forms the basis for the further analysis of the contribution of the different channel types in the overall activity of the spinal locomotor network.
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
-2-ethanesulfonic acid (HEPES), and 0.5 L-glutamine, pH adjusted to 7.4. The spinal cord was exposed from either the dorsal aspect, by removing overlying tissues, or from the ventral aspect by removing the notochord. Motoneurons and sensory dorsal cells were retrogradely labeled by applying fluorescein-coupled dextran amine (FDA) to the remaining muscle tissue along the entire length of the preparation. Removal of the dorsal tissue resulted in all of the dorsal roots being cut, thereby allowing the transport of the dye only through the ventral roots to label motoneurons. In contrast, removal of the notochord resulted in transection of ventral roots and dye transport only through the dorsal roots for labeling of dorsal cells. After 15 min, the preparation was thoroughly washed with physiological solution to remove the remaining FDA. The preparation was left for 48-60 h in a cold room to allow for transport of the tracer.
were pulled on a Narishige two-step puller. Cells were voltage clamped at a holding potential of 
90 mV and currents were evoked by 40- to 60-ms depolarizing voltage steps applied at 10-s intervals. Linear leak and residual capacity currents were subtracted on-line with the use of a P/4 subtraction protocol (4 steps, 1/4 of the test pulse, averaged and scaled for each test pulse). Pulse protocols, data acquisition, and analysis of recordings were performed with the use of pCLAMP software (Axon Instruments). During the recording, cells were superfused with the use of a gravity-driven system with a solution containing (in mM) 114 NaCl, 10 tetraethylammonium, 1 KCl, 1.2 MgCl2, 10 glucose, 10 HEPES, 5 CaCl2 or BaCl2, and 0.001 tetrodotoxin, pH adjusted to 7.4. For whole cell recordings, the pipettes were filled with a solution containing (in mM)110 CsCH3SO3, 10 ethylene glycol-bis(
-aminoethyl ether)-N,N,N,N-tetraacetic acid, 10 glucose, 10 HEPES, 5 MgCl2, 1 CaCl2, 2 ATP, 0.4 guanosine 5-triphosphate, and 8 phosphocreatinine, pH adjusted to 7.4 with CsOH. Drugs were added to the extracellular medium from stock solutions. Nimodipine (RBI) and (±)-BayK 8644 (BayK, RBI) were dissolved in ethanol; -CgTx (Sigma) and -agatoxin-IVA (-Aga, Peptide Institute) were dissolved in physiological solution.
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
90 mV with the use of barium as the charge carrier in the presence of blockers for sodium and potassium channels (see METHODS). Motoneurons (n = 8) showed only a sustained HVA barium current that started to be activated at voltage steps between 40 and 30 mV (Fig. 2A). This current was completely blocked by cadmium (50-200 µM; data not shown), a general blocker for HVA calcium channels. In contrast to motoneurons, some dorsal cells displayed both LVA and HVA calcium currents. The LVA current (Fig. 2B) was obtained in 17% of all dorsal cells studied (n = 63) and in 19% of unidentified spinal cord neurons(n = 64). This current was transient and typically activated at voltage steps between 60 and 50 mV. As the test potential became more depolarized (Fig. 2B), the amplitude of the total current increased and the onset became faster. The peak amplitude was reached at a test potential of ~0 mV and decreased with further depolarization (Fig. 2C). The HVA current was completely blocked with cadmium (50-200 µM), whereas the amplitude of the LVA current elicited by a test potential to 30 mV was reduced by 50%, but the LVA current was never completely blocked (Fig. 2C). In dorsal cells showing only an HVA current (not illustrated), no significant current was elicited until the test potential reached approximately 40 mV and no transient component was seen, as in the motoneuron in Fig. 2A.
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FIG. 1.
Motoneurons and sensory dorsal cells can be selectively labeled with fluorescein-coupled dextran amine (FDA). A: whole mount of spinal cord showing retrograde labeling of motoneurons after application of FDA. B: example of FDA-labeled motoneuron obtained by dissociation of spinal cord in which motoneurons were selectively labeled. C: retrogradely labeled dorsal cell in whole mount with ascending and descending axonal branches. D: isolated FDA-labeled dorsal cell with its characteristic bipolar shape. Scale bar: 25 µm.
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FIG. 2.
Properties of calcium channel currents in motoneurons and sensory dorsal cells. A: whole cell voltage-clamp recording was made from prelabeled motoneuron. Voltage steps were applied from holding potential of 90 mV. Inward barium current started to be activated at voltage steps between 40 and 30 mV, and no transient component was seen. B: inward barium current in prelabeled sensory dorsal cell. Transient barium current was elicited at voltage steps between 60 and 50 mV. Amplitude of this transient current increased with increased voltage steps. Sustained current was evoked at voltage steps between 30 and 20 mV. C: sustained current in dorsal cell was completely blocked by cadmium (100 µM), whereas large part of transient current persisted in cadmium. Vt, test potential; IBa, barium current.
90 mV and a voltage step to a test potential was applied. Application of the N-type calcium channel antagonist -CgTx (Aosaki and Kasai 1989; Boland et al. 1994; Plummer et al. 1989; Regan et al. 1991) caused a dramatic decrease of the total barium current in a dose-dependent manner (Fig. 3). At 0.2 µM, -CgTx blocked >70% of the current (Fig. 3, A and B), and the current was decreased further when the -CgTx concentration was increased to 0.5 µM. A further increase of the concentration to 1 or 2 µM had only a slight additional effect (Fig. 3, A-C). N-type channels are fully available at 90 mV and start to be activated around 25 mV (not shown). In all neurons studied (motoneurons, dorsal cells, and unidentified neurons), the -CgTx block could be reversed after the toxin was removed from the perfusing solution (Fig. 3A). Thus >70% of the total barium current was blocked by -CgTx concentrations as low as 0.2 µM and the maximum effect of the toxin was obtained at 0.5 µM (Fig. 3C). These results show that a large component of the HVA calcium channel current in lamprey spinal cord neurons is caused by activation of N-type channels.
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FIG. 3.
Effect of -conotoxin GVIA (-CgTx) on calcium channel current. A and B: inward barium current was elicited in spinal neuron by voltage step to 10 mV from holding potential (Vh) of 90 mV. Application of 0.2 µM -CgTx markedly decreased amplitude of current. Current was decreased further by 0.5 µM -CgTx, whereas increasing concentration of toxin to 1 µM had only slight additional effect. Amplitude of current partially recovered after removal of toxin from perfusing solution. C: plot of effect of different concentrations of -CgTx on calcium channels with maximum blockade obtained with 1 µM -CgTx. Plot corresponds to average values from 28 pooled experiments.
-CgTx blocked a large proportion of the total barium current, it was never able to abolish the current completely, indicating that other components, insensitive to -CgTx, are present in lamprey spinal cord neurons. The total barium current was therefore dissected further with the use of nimodipine, an antagonist for L-type calcium channels (McCarthy and TanPiengo 1992; Regan et al. 1991). Application of nimodipine decreased the amplitude of the current in a dose-dependent manner. The blocking effect of nimodipine was apparent at 0.5 µM and the maximum effect was obtained with a concentration of 2 µM (Fig. 4, A-C). Application of BayK (1-2 µM), a selective L-type channel agonist, greatly enhanced the amplitude of the calcium channel current elicited by a step potential to 30 mV (Fig. 5A). In all neurons studied, BayK increased the amplitude of the barium current by >200% (n = 9). In lamprey spinal cord neurons, L-type channels were activated at 30 mV, whereas N-type channels were activated at more positive potentials. These results thus show that lamprey spinal cord neurons possess dihydropyridine-sensitive L-type calcium channels.
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FIG. 4.
Effect of nimodipine on calcium channel current. A and B: nimodipine reduced amplitude of calcium current in dose-dependent manner. Reduction of current was obtained with 0.5 µM nimodipine. This effect was more pronounced with higher concentrations. Remainder of current was blocked by cadmium. C: plot of average effect of different concentrations of nimodipine from 29 experiments.
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FIG. 5.
(±)-BayK 8644 (BayK) increased amplitude of calcium channel current. A and B: the L-type channel agonist BayK (1 µM) markedly increased amplitude of calcium current elicited by voltage step to 30 mV from holding potential of 90 mV. Current recruited by BayK was essentially not affected by N-type antagonist -CgTx and was blocked by cadmium.
-CgTx can also block L-type calcium channels in a nonselective manner (Aosaki and Kasai 1989; Mynlieff and Beam 1992). This possibility was studied by testing the effect of -CgTx on a calcium component that had been potentiated by the dihydropyridine agonist BayK and it could thus be unambiguously identified as being mediated through opening of L-type channels (Fig. 5, A and B). The amplitude of the current recruited by BayK was unchanged after application of -CgTx (0.2 µM). A small reduction of the current amplitude, as measured at the end of the voltage step, was seen when a higher concentration of -CgTx (0.5 µM) was applied (Fig. 5, A and B). We therefore concluded that -CgTx at a concentration between 0.2 and 0.5 µM does not significantly affect L-type calcium channels.
10 mV from a holding potential of 90 mV and different calcium channel antagonists were applied (Fig. 6, A and B). Application of -CgTx (0.5 µM) blocked 74.2% (Fig. 6, A and C) of the total barium current. Addition of nimodipine (5 µM) in the presence of -CgTx blocked the current further by 14.6% (Fig. 6, A and C). In no case when both N- and L-type calcium channel antagonists were applied simultaneously was the current completely abolished, indicating that other components insensitive to -CgTx and nimodipine are present in motoneurons. The presence of P/Q-type calcium channels was therefore tested with the use of -Aga (0.2 µM). In the presence of -CgTx and nimodipine, application of -Aga blocked 4.5% (Fig. 6C) of the total barium current, but a complete block was not obtained. The remainder of the current was abolished by application of cadmium (50 µM), a general blocker for HVA calcium channels (Fig. 6, A and B).
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FIG. 6.
Calcium channel subtypes in motoneurons. A: calcium current was elicited in prelabeled motoneuron by voltage steps to 10 mV from holding potential of 90 mV. The N-type antagonist -CgTx markedly reduced amplitude of current, the L-type antagonist nimodipine decreased amplitude of current further, and P/Q-type blocker had further small effect on current. Resistant current was blocked by cadmium. B: average traces showing effect of different calcium channel antagonists. C: current mediated through N-, L-, and P/Q-type calcium channels. These traces were obtained by subtraction of current traces illustrated in B. -Aga, -agatoxin IVA.
20 mV from a holding potential of 90 mV. Application of -CgTx (0.5 µM) reduced the amplitude of the total barium current by 66.7% in this cell, and addition of nimodipine (5 µM) blocked the current further by 16.8% (Fig. 7, A-C). As in motoneurons, the HVA calcium channel current in dorsal cells also contains a component that is insensitive to -CgTx and nimodipine. Application of -Aga (0.2 µM) reduced the amplitude of the total barium current by an additional 2.8% but never blocked it completely (Fig. 7, A and B). Cadmium (50 µM) blocked the remainder of the current. These results show that both motoneurons and dorsal cells in the lamprey spinal cord possess N-, L-, and P/Q-type calcium channels as well as a residual (R) calcium current component resistant to the N-, L-, P/Q-type antagonists and blocked by cadmium (Figs. 6 and 7). In all neurons (n = 14) in which the different calcium channel antagonists were tested simultaneously, N-type, L-type, P/Q-type, and R-type channels represented68.0 ± 4.0% (mean ± SE), 12.2 ± 2.1%, 5.8 ± 1.3%, 10.0 ±1.5% of the total barium current, respectively (Fig. 8).
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FIG. 7.
High-voltage-activated (HVA) calcium channel subtypes in dorsal cells. A: whole cell recording was made from prelabeled dorsal cell and calcium current was elicited by voltage steps to 20 mV from holding potential of 90 mV. The N-type calcium channel antagonist -CgTx blocked >70% of current, the L-type blocker nimodipine reduced current amplitude by ~14%, and P/Q-type antagonist blocked current further by ~5%. In presence of 3 antagonists, there was residual current that persisted and was blocked by cadmium. B: average traces showing effect of different calcium channel antagonists. C: amount of current mediated by N-, L-, and P/Q-type channels. These traces were obtained by subtraction of current traces illustrated in B.
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FIG. 8.
Relative contribution of different calcium channels to total current in lamprey spinal cord neurons. Plot shows average effects of N-, L-, and P/Q-type calcium channel antagonists on total current as well as amount of residual current that was insensitive to combined application of the 3 antagonists.
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
). The LVA calcium channel current is characterized by a transient activation at relatively hyperpolarized potentials (Carbone and Lux 1984; Fox et al. 1987; Nowycky et al. 1985). This current was seen in 17% of sensory dorsal cells and in 19% of unidentified neurons, but was never seen in identified motoneurons. The HVA calcium channel current, on the other hand, was present in all cells recorded. This current could be divided pharmacologically into four components: N, L, P/Q, and R. In the intact spinal cord, dorsal cells have been subdivided into touch- and pressure-sensitive types depending on their sensitivity to skin stimulation (Christenson et al. 1988). Touch-sensitive dorsal cells represent ~14% of the total number of dorsal cells and possess LVA calcium channels (Christenson et al. 1993). In contrast, pressure-sensitive dorsal cells do not have LVA calcium channels. The proportion of dorsal cells that displayed an LVA calcium current in the present study thus corresponds to that reported in the intact spinal cord. Dorsal cells used in this study were not identified on the basis of their sensitivity to skin stimulation, but it is likely that dorsal cells with an LVA current are touch sensitive, whereas those with only HVA currents are sensitive to pressure.
-CgTx blocked >70% of the total barium current at the peak amplitude in skin sensory dorsal cells, motoneurons, and unidentified spinal neurons. In spinal cord neurons of larval lampreys, the largest proportion of the calcium channel current is thus carried through N-type channels. The dominance of N-type channels was also seen in cultured spinal neurons from adult (transformer) animals (unpublished data). The -CgTx block of the barium current was reversible on washout in all neurons analyzed in this study. In frog, N-type calcium channels were reversibly blocked by -CgTx and they represented the major component of the total calcium channel current (Boland et al. 1994; Wall and Dale 1993). In peripheral and central mammalian neurons, the N-type channel current has been defined as a current irreversibly blocked by -CgTx (Boland et al. 1994; Williams et al. 1992). A partial recovery of -CgTx block of mammalian N-type channels was also reported (Ellinor et al. 1994). It thus seems that N-type channels in both peripheral and central neurons of lower vertebrates are characterized by their strong blockade by -CgTx, but unlike in higher vertebrates, the block is largely reversible on washout. In chick sensory neurons and mouse motoneurons, on the other hand, -CgTx has been reported to block L-type calcium channels nonselectively and reversibly (Aosaki and Kasai 1989; Mynlieff and Beam 1992). A possible nonselective block of L-type channels is unlikely to occur in lamprey spinal cord neurons because -CgTx at concentrations sufficient to block >70% of the total barium current failed to affect an L-type current recruited by application of BayK (Fig. 4). We therefore conclude that in the lamprey spinal cord N-type channels represent a large part of the somatic calcium current and that they are characterized by a reversible block by -CgTx.
), although in the embryo of Xenopus, another lower vertebrate, spinal cord neurons do not possess dihydropyridine-sensitive calcium channels (Barish 1991; Wall and Dale 1994).
-CgTx and nimodipine never caused a complete block of the total calcium channel current. A part of the residual current was blocked by -Aga and can thus be considered as mediated through P/Q calcium channels (Llinás et al. 1992; Mintz et al. 1992; Pearson et al. 1995; Randall and Tsien 1995). No attempt, however, was made to determine the relative involvement of P- versus Q-type channels. Lamprey spinal cord neurons thus possess an additional HVA calcium component that is insensitive to specific HVA antagonists but that is blocked by cadmium. Interestingly, the proportion of this residual current is similar to what was reported for mammalian sensory and motoneurons. These results demonstrate in the lamprey the presence of N-, L-, and P/Q-type and calcium channels with pharmacological properties that are similar to those of higher vertebrates. Several cellular properties that are important for the operation of the spinal locomotor network, such as spike frequency adaptation and N-methyl-D-aspartate-induced membrane potential oscillations, are dependent on calcium entry through voltage-dependent channels.
).
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ACKNOWLEDGEMENTS |
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We thank Drs. S. Grillner, R. Hill, D. Parker, and P. Wallén for comments on the manuscript. We also thank H. Axegren and M. Bredmyr for skillful technical assistance.
This work was supported by the Swedish Medical Research Council Project 11562, J. Stiftelse, and Å. Wibergs Stiftelse.
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FOOTNOTES |
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Address reprint requests to A. El Manira.
Received 22 January 1997; accepted in final form 6 May 1997.
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REFERENCES |
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Abstract
Introduction
Methods
Results
Discussion
References
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257: 389-395, 1992.This article has been cited by other articles:
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P. Krieger, J. Hellgren-Kotaleski, P. Kettunen, and A. J. El Manira Interaction between Metabotropic and Ionotropic Glutamate Receptors Regulates Neuronal Network Activity J. Neurosci., July 15, 2000; 20(14): 5382 - 5391. [Abstract] [Full Text] [PDF]
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P. Krieger, A. Buschges, and A. el Manira Calcium Channels Involved in Synaptic Transmission From Reticulospinal Axons in Lamprey J Neurophysiol, April 1, 1999; 81(4): 1699 - 1705. [Abstract] [Full Text] [PDF]
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J. Tegner and S. Grillner Interactive Effects of the GABABergic Modulation of Calcium Channels and Calcium-Dependent Potassium Channels in Lamprey J Neurophysiol, March 1, 1999; 81(3): 1318 - 1329. [Abstract] [Full Text] [PDF]
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F. P. Elsen and J.-M. Ramirez Calcium Currents of Rhythmic Neurons Recorded in the Isolated Respiratory Network of Neonatal Mice J. Neurosci., December 15, 1998; 18(24): 10652 - 10662. [Abstract] [Full Text] [PDF]
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D. Hess and A. El Manira Characterization of a high-voltage-activated IA current with a role in spike timing and locomotor pattern generation PNAS, April 24, 2001; 98(9): 5276 - 5281. [Abstract] [Full Text] [PDF]
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