JN Fuel your research with LabChart
HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS
QUICK SEARCH:   [advanced]


     

J Neurophysiol 79: 45-50, 1998;
0022-3077/98 $5.00
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Svirskis, G.
Right arrow Articles by Hounsgaard, J.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Svirskis, G.
Right arrow Articles by Hounsgaard, J.

The Journal of Neurophysiology Vol. 79 No. 1 January 1998, pp. 45-50
Copyright ©1998 by the American Physiological Society

Transmitter Regulation of Plateau Properties in Turtle Motoneurons

Gytis Svirskis and Jørn Hounsgaard

Laboratory of Neurophysiology, Biomedical Research Institute, Kaunas Medical Academy, 3000 Kaunas, Lithuania; and Department of Medical Physiology, The Panum Institute, Copenhagen University, DK-2200 Copenhagen, Denmark

    ABSTRACT
Abstract
Introduction
Methods
Results
Discussion
References

Svirskis, Gytis and Jørn Hounsgaard. Transmitter regulation of plateau properties in turtle motoneurons. J. Neurophysiol. 79: 45-50, 1998. In motoneurons, generation of plateau potentials is promoted by modulators that block potassium channels. In voltage-clamp experiments with triangular voltage ramp commands, we show that cis-(±)-1-aminocyclopentane-1,3-dicarboxylic acid (cis-ACPD) and muscarine promote the generation of plateau potentials by increasing the dihydropyridine sensitive inward current, by increasing the input resistance, and by depolarizing the resting membrane potential. Type I metabotropic glutamate receptors (mGluR I) mediate the effects of cis-ACPD. Baclofen suppresses generation of plateau potentials by decreasing the dihydropyridine sensitive inward current, by decreasing the input resistance, and by hyperpolarizing the resting membrane potential. These results suggest that membrane properties of motoneurons are continuously modulated by synaptic activity in ways that may have profound effects on synaptic integration and pattern generation.

    INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References

The nonlinear intrinsic membrane properties, provided by the particular set of voltage-sensitive ion channels in the soma-dendritic membrane in each type of neuron, are thought to be essential for brain function (Llinas 1988). Regulation of these properties by transmitters that change the voltage sensitivity or kinetics of ion channels is important for the dynamic formation and function of motor networks in invertebrates and vertebrates (Katz and Frost 1996). The flexible motor behaviors mediated by spinal cords predict regulation of motor networks to be essential. However knowledge of possible mechanisms for regulation is limited and the role of regulation of intrinsic membrane properties in vertebrate motor function is unknown. One approach to this question is to examine to what extent a specific intrinsic membrane property of a member of the spinal motor network is regulated by activation of a range of putative modulatory transmitter receptors. In this way studies on spinal motoneurons have uncovered important regulatory effects of serotonin and noradrenalin (Berger and Takahashi 1990; Elliott and Wallis 1992; Hounsgaard and Kiehn 1989; Larkman and Kelly 1992; Van Dongen et al. 1986). In the present study we have examined the regulation of plateau properties in motoneurons in transverse sections of the turtle spinal cord. In motoneurons, the best studied cell type in the spinal cord, plateau potentials are mediated by noninactivating, dihydropyridine-sensitive calcium channels (Hounsgaard and Mintz 1988) widely distributed in dendritic membranes (Hounsgaard and Kiehn 1993). The ability to generate plateau potentials is a latent property, previously shown to be facilitated by block of Ih and a range of potassium conductances (Hounsgaard and Mintz 1988). Serotonin also promotes plateau potentials in motoneurons (Hounsgaard et al. 1988; Hounsgaard and Kiehn 1989). Although the effect of serotonin was attributed to a reduction of the apamin-sensitive calcium-dependent potassium conductance underlying the slow spike afterhyperpolarization, enhancement of the calcium current was not ruled out (Hounsgaard and Kiehn 1989). Our study shows that plateau potentials are facilitated by activation of muscarine receptors and type I metabotropic glutamate receptors (mGluR) and suppressed by activation of gamma -aminobutyric acid-B (GABAB) receptors. The regulation involves several conductance changes possibly including the low voltage activated L-type calcium conductance underlying plateau potentials. The results show that several transmitter pathways of spinal and supraspinal origin can control a particular intrinsic property of a particular member of the spinal motor network.

    METHODS
Abstract
Introduction
Methods
Results
Discussion
References

Transverse sections of the lumbar spinal cord were obtained as described before from turtles (Pseudemys scripta elegans) deeply anesthetized by mebumal (at least 100 mg/kg) injected intraperitoneally (Hounsgaard et al. 1988). The bath medium contained (in mM) 120 NaCl, 5 KCl, 15 NaHCO3, 20 glucose, 2 MgCl2, and 3 CaCl2. The solution was saturated with 98% O2-2% CO2 to obtain a pH of 7.6 in the recording chamber.

For experiments a section of the cord, 1- to 2-mm thick, glued on end to a piece of filter paper, was placed in the recording chamber. The liquid level was <0.2 mm above the surface of the slice. Sharp and patch electrodes were pulled from borosilicate glass tubes with an outer diameter of 1.5 mm and an inner diameter of 0.86 mm. Sharp electrodes were filled with 1.5 M KCl and 0.5 M potassium acetate. Patch electrodes were filled with 125 mM potassium gluconate and 9 mM N-2-hydroxyethylpiperazine-N'-2-ethanesulfonic acid (HEPES), pH was adjusted to 7.4 with KOH. As in a previous study (Svirskis et al. 1997) the results obtained with the two techniques were the same including the observed range of input resistance, spiking pattern, and spike height. In some cases we also checked for the absence of an electrode-induced shunt (Svirskis et al. 1997). For these reasons, no distinctions were made between the two recording methods when analyzing the results.

Voltage clamp was performed with an Axoclamp 2A amplifier in discontinuous single-electrode voltage-clamp mode. The gain ranged from 0.7 to 3 kHz and sample rate from 6 to 9 kHz and the electrode transients were monitored to assure adequate settling before the sample point. Triangular potential ramps were generated with a homemade triangle signal generator. For slow voltage-clamp ramps the recorded currents and potentials were low-pass filtered at 0.1 kHz and digitized at 0.8 kHz. In all other cases signals were low-pass filtered at 3 kHz and digitized at 6 kHz. To reduce noise in voltage clamp recordings, 4 sweeps were averaged on a HIOKI digital oscilloscope. The data from the oscilloscope was transferred to an IBM compatible computer through a National Instruments GPIB interface for storage and later analysis. The input resistance was measured from the slope of the current-voltage relation (I-V) near the resting membrane potential.

Drugs used included tetrodotoxin (TTX, 2 µM), cis-(±)-1aminocyclopentane-1,3-dicarboxylic acid (cis-ACPD, 20 µM), (S)-3,5-dihydroxyphenylglycine (DHPG, 50 µM), (S)-a-methyl4-carboxyphenylglycine (MCPG, 1 mM), muscarine (25 µM), atropine (1 µM), baclofen (5 µM), CoCl2 (2 mM), nifedipine (10-20 µM), tetraethylammonium (TEA, 0.2-1 mM), and apamin (1 µM).

We used voltage-clamp triangle ramps lasting several seconds to monitor the activation and relative strength of the voltage sensitive inward current. In a cable structure like a neuron, voltage clamp from a point source is less than perfect (Jack et al. 1975; Jonas et al. 1993; Major et al. 1994). In light of the limited space clamp inherent with the technique, we tested the validity of our measurements for qualitative analysis. In current-clamp recordings we used field stimulation, as illustrated in Fig. 1A, to test the sensitivity of voltage-dependent currents generated in the dendrites to changes in membrane potential at the soma. The diagram illustrates the profile of the transmembrane potential calculated for a cable structure when a hyperpolarizing current is injected through the recording electrode (- - -) and when differential polarization is induced by an extracellular voltage gradient (· · ·) (Svirskis 1997). In the experiment two silver-chloride electrodes (surface area of 12 mm2, Clark Electromedical) were used to pass current delivered by an isolation unit (Isolator 11, Axon Instruments) through the tissue to establish an extracellular potential gradient (Hounsgaard and Kiehn 1993). The field was oriented in the lateral direction to obtain polarization distally in the longest dendrites (Ruigrok et al. 1985). Activation of inward current in distal dendrites was accomplished by applying the field in the soma hyperpolarizing direction (Hounsgaard and Kiehn 1993). With this procedure a delayed depolarization developed during a field pulse and fully decayed after the offset of the field (Fig. 1B, top). The delayed depolarization, reflecting activation of distal inward currents, was greatly inhibited by a <5 mV hyperpolarization at the soma, induced by current injection through the recording electrode (Fig. 1B, bottom). The hyperpolarizing current did not just prevent the propagation of the depolarization to the recording site because the delayed depolarization could be restored by increasing the strength of the applied electric field. These results suggest that inward currents in dendrites are at moderate electrotonic length from the soma and are not generating uncontrolled depolarization in distal dendrites. In agreement, the net inward current activated by a step depolarization (Fig. 1C) fully deactivated after the termination of the stimulus. Even electrotonically short cables can distort the monitored magnitude of the inward current if the voltage ramp is just suprathreshold for the activation of the slow, voltage-sensitive inward current facilitated by depolarization (Baginskas et al. 1997). Here we used ramps, which reversed much above the threshold for the activation of inward current. In this case, it is unlikely that the electrotonic delay of the voltage onset in the dendrites is important because the duration of the ramps used was two orders of magnitude slower than membrane time constant (Hounsgaard et al. 1988).


View larger version (13K):
[in this window]
[in a new window]
  		FIG. 1. Sensitivity of dendritic voltage-dependent currents to soma potential was checked by field stimulation (see METHODS). A: a cable representing a motoneuron positioned between 2 field electrodes. An extracellularpotential gradient induces differential polarization of ohmic cable (- - -)and hyperpolarization by current injection decays from stimulation site (· · ·). The resulting membrane potential is sum of two voltage changes induced if voltage-sensitive currents are not activated. Length of cable is in electrotonic units, lambda . B: when a motoneuron was stimulated by a field, initial transmembrane hyperpolarization was followed by depolarization reflecting activation of a voltage-sensitive inward current in distal dendrites (top). A small hyperpolarization by current injection in soma almost completely prevents activation of inward current (bottom). C: activation of inward current in the same neuron during voltage clamp. Potential step activates a net inward current that fully deactivates after termination of stimulus. Note slow activation and deactivation of inward current. Time scale as in B. B and C: inward current was promoted by apamin, tetraethylammonium (TEA), and (S)-3,5-dihydroxyphenylglycine (DHPG) in medium.

    RESULTS
Abstract
Introduction
Methods
Results
Discussion
References

As shown previously (Hounsgaard and Kiehn 1989; Hounsgaard and Mintz 1988), motoneurons in transverse slices of the turtle spinal cord do not generate plateau potentials in normal medium (Fig. 2A). Bistability was induced, however, when the unspecific agonist of metabotropic glutamate receptors, cis-ACPD, was applied to normal medium (n = 3; Fig. 2B). In the present study we have used triangular voltage commands (Eckert and Lux 1976) in single-electrode voltage-clamp mode to monitor changes in membrane properties induced by promoters and suppressors of plateau potentials. The experimental procedure is illustrated in Fig. 2C by the results obtained in voltage-clamp recordings from a motoneuron, in which plateau potentials were promoted by cis-ACPD. The ramps covered a voltage range of ~40 mV from just below the resting membrane potential to just above the threshold for action potentials. This range covers the voltage range of plateau potentials in current-clamp recordings (Hounsgaard and Kiehn 1989; Hounsgaard and Mintz 1988). Spike generating Na+ conductance was suppressed by TTX in the voltage-clamp experiments. The inward deviation of the current response during the triangular voltage command from the stippled linear curve is a measure of the activated inward current. Current voltage, I-V, plots showed marked clockwise hysteresis (Fig. 2C, right), which at least in part reflects the slow kinetics of the inward current or changes in gating properties (Svirskis and Hounsgaard 1997). Voltage commands with duration of ~3 s gave maximal hysteresis in the I-V plots and were therefore chosen for monitoring the voltage-sensitive inward current in most experiments. Hysteresis leveled off with faster and slower ramps but was still present with ramps lasting 8 s (Fig. 2Ca) and 0.4 s (Fig. 2Cb). The very presence of inward current generating hysteresis in response to slow ramps illustrates the necessary condition for prolonged plateau potentials in current-clamp mode. However depolarizing bias current is needed to observe sustained plateaus if hysteresis does not cross the zero current line. If the hysteresis crosses this line, as in Fig. 2C, then there are two stable potentials, i.e., the neuron is bistable. In such a neuron a sustained plateau potential can be generated in current-clamp mode by a short-lasting depolarization and terminated by a short-lasting hyperpolarization, as in Fig. 2B. In control conditions an existing inward current in motoneurons and most interneurons was too weak to cross the zero line and the cells were not bistable at rest.


View larger version (24K):
[in this window]
[in a new window]
  		FIG. 2. Plateau potentials are produced by a slow inward current causing clockwise hysteresis in I-V relation. A: in control solution motoneurons show no bistability. B: after application of cis-ACPD, the same stimulus activates a long-lasting plateau potential terminated by injection of a hyperpolarizing current. C: voltage clamp was performed in the same neuron after blockade of Na+ spikes with tetrodotoxin (TTX). Ca: - - -, hypothetical linear response to voltage clamp. Inward deviation from the linear curve indicates activation of voltage-sensitive currents. Presence of clockwise hysteresis shows that voltage ramp was too fast to obtain stationary characteristics of inward current. Cb: when ramp was even faster, the inward current was not fully activated during rising phase of triangular ramp and did not deactivate during falling phase of ramp. This resulted in a long and narrow hysteresis indicating slow current kinetics. ------, zero value for current. Inset: right-arrow, direction of potential change.

The effects of cis-ACPD and muscarine on the I-V relation were analyzed experimentally as illustrated in Fig. 3. A hysteretic I-V relation, weak or absent in normal medium (Fig. 3A), was enhanced or induced by addition of cis-ACPD to the medium (Fig. 3B). In 18 neurons (13 intracellular recordings, 5 whole cell recordings) cis-ACPD induced a slow inward current and hysteresis in 6 neurons (33%), enhanced an already existing slow inward current and hysteresis in 9 neurons (50%), and had no effect in 3 neurons (17%). Cis-ACPD increased input resistance by 31 ± (SE) 28% and the resting membrane potential (RMP) was depolarized by 6.3 ± 4 mV (Fig. 4D). The slow inward current depended on a calcium channel because it was blocked by addition of 2 mM Co2+ to the medium (n = 4; Fig. 3C). Note that the change in RMP and input resistance induced by cis-ACPD was not reversed by Co2+. As illustrated in Fig. 4A this calcium channel was dihydropyridine sensitive because the slow inward current and hysteresis were reduced or blocked by addition of nifedipine (10-20 µM; n = 6). The effects of cis-ACPD were blocked by MCPG, a nonspecific antagonist of metabotropic glutamate receptors (n = 2). The effects were mediated by type I metabotropic glutamate receptors because they were reproduced by DHPG, a selective type I mGluR agonist (n = 3) (Nicoletti et al. 1996; Riedel 1996).


View larger version (17K):
[in this window]
[in a new window]
  		FIG. 3. Hysteresis is induced or enhanced by cis-(±)-1-aminocyclopentane-1,3-dicarboxylic acid (cis-ACPD) and muscarine. A: in presence of TTX, no inward current was activated in normal medium. B: cis-ACPD induced clockwise hysteresis indicating activation of an inward current, which was blocked by Co2+ (C). D: superposition of all I-V plots from A-C shows that cis-ACPD increases input resistance of the cell and promotes opening of Ca2+ channels. up-arrow , resting membrane potential (RMP) before and after cis-ACPD. E: voltage-ramp lasting 8 s in presence of TTX; in normal medium and after addition of muscarine. Only the rising phase of ramp is shown in I-V plot. Muscarine enhanced inward current and shifted activation to hyperpolarizing potentials. Calibrations in B and C as in A.


View larger version (21K):
[in this window]
[in a new window]
  		FIG. 4. Hysteresis is mediated by nifedipine sensitive channels. A: hysteresis in I-V plot present after addition of TTX and cis-ACPD to bath was strongly reduced by nifedipine. B: in another cell, hysteresis enhanced by muscarine was reduced by nifedipine.

Plateau potentials in turtle motoneurons are promoted by TEA and apamin (Hounsgaard and Mintz 1988). In this study the slow inward current and hysteresis, promoted by TEA and apamin, was enhanced by cis-ACPD (n = 3).

In agreement with a previous study (Mintz 1987), we found that muscarine, a selective agonist of metabotropic acetylcholine receptors, induced plateau potentials and slow oscillations in turtle motoneurons. In the voltage range studied here, muscarine, had effects similar to cis-ACPD on the slow inward current (Fig. 3E) and hysteresis produced during a triangular command in voltage clamp mode (n = 17, sharp electrode recordings). The hysteresis was induced (35%, n = 6) or enhanced (47%, n = 8) or unchanged (18%, n = 3) by muscarine. Note the shift in activation of the inward current to more hyperpolarized membrane potentials on application of muscarine (Fig. 3E). The same shift was common with application of cis-ACPD. Muscarine increased the input resistance by 22 ± 22% and depolarized the RMP by 1.2 ± 4 mV. The effects of muscarine were blocked by atropine (n = 7). As illustrated in Fig. 4B, the inward current and the hysteresis induced by muscarine was reduced or blocked by nifedipine (n = 3).

The enhanced inward current and hysteresis were reduced by activation of GABAB receptors (n = 6, whole cell recordings). In motoneurons, in which weak hysteresis was present (Fig. 5A), hysteresis was further promoted by blocking potassium channels with apamin and TEA (Fig. 5B). This is in agreement with previous findings (Hounsgaard and Kiehn 1993; Hounsgaard and Mintz 1988). The slow inward current and hysteresis was reduced (n = 4;Fig. 5C) or eliminated (n = 2) when GABAB receptors were activated by adding baclofen to the medium. Baclofen also reduced the input resistance 20 ± 10% and hyperpolarized the RMP by 5.6 ± 6 mV. The effect of baclofen was reversible (Fig. 5D; n = 4) and the recovered hysteresis was blocked by nifedipine (Fig. 5E).


View larger version (17K):
[in this window]
[in a new window]
  		FIG. 5. Hysteresis is reduced by a gamma -aminobutyric acid-B (GABAB) receptor agonist, baclofen. A: in this cell a weak inward current was already activated in presence of TTX in normal medium. B: current is obscured by outward currents because application of apamin and TEA enhanced hysteresis. C: baclofen reduced inward current and washout of this drug restored hysteresis (D). E: L-type calcium channels are responsible for hysteresis because response to ramp was completely linearized by nifedipine. Scale for B and C is identical to A. Scale in E is identical to D. All experiments are from same cell.

    DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References

Modulation of plateau properties in motoneurons was studied by means of voltage ramp clamp. Clockwise hysteresis in the I-V relation is a manifestation of the ability to generate plateau potentials in current clamp. This hysteresis was shown to be induced or enhanced by agonists of metabotropic glutamate receptors and muscarinic receptors. These changes were accompanied by increased input resistance and depolarization. Activation of GABAB receptors suppressed the hysteresis, reduced the input resistance, and hyperpolarized the cells.

The involvement of calcium channels in plateau potentials and hysteresis opens the possibility that conductances sensitive to intracellular calcium concentration contribute (Partridge and Swandulla 1988) and could be possible targets for regulation. Activation of muscarine receptors (Delmas et al. 1996; Fraser and MacVicar 1996; Schwindt et al. 1988) and metabotropic glutamate receptors (Greene et al. 1994) can induce calcium-sensitive cationic currents. In some neurons, a calcium-dependent increase in input resistance was observed after application of muscarinic agonists (Sciancalepore and Constanti 1995) and agonists of mGluR (Greene et al. 1994; Sciancalepore and Constanti 1995). The modulation of calcium-sensitive potassium currents (Kume et al. 1992; Muller et al. 1992) or blockade of potassium currents (Charpak et al. 1990; Gerber et al. 1992; Guerineau et al. 1994; Jones and Baughman 1992; Selyanko and Brown 1996; Womble and Moises 1992) could also explain the enhancement or reduction of hysteresis.

However despite the presence of other calcium channels in the dendrites (Hounsgaard and Kiehn 1993) plateaus and hysteresis were eliminated by nifedipine alone, a selective antagonist of L-type calcium channels, which did not block calcium spikes (Hounsgaard and Mintz 1988). The plateaus were also observed after substitution of sodium with choline (Mintz 1987) and modulation was not reduced in the presence of TEA and apamin known to block voltage and calcium-sensitive potassium channels. It is difficult to explain both induction and full elimination of the hysteresis if modulators act without a direct action on L-type calcium channels.

However interpreting the induction or elimination of hysteresis is not straightforward because turtle motoneurons possess physically long dendrites (Ruigrok et al. 1984, 1985). Calcium channels responsible for plateau generation are located in the dendrites (see METHODS and Hounsgaard and Kiehn 1993). Therefore a change in membrane resistance and resting potential induced by receptor agonists leads to a changed activation of dendritic inward currents during a command ramp (Jack et al. 1975; Jonas et al. 1993; Major et al. 1994; Puil et al. 1994). However the estimated electrotonic length of the dendrites in motoneurons in normal medium is moderate, about ~1 lambda  (Svirskis et al. 1997). In addition the inward current responsible for the plateau was not strong enough to cause uncontrollable distal inward currents, i.e., dendritic bistability (Gutman 1991; Muller and Lux 1993; Puil et al. 1994), and was quite sensitive to changes in soma potential (see METHODS and Fig. 1).

The effect of applied drugs was variable. In some cases change in electrotonic decay of the potential cannot explain the observed phenomena. For example in three neurons after application of cis-ACPD and three neurons after muscarine, plateaus or hysteresis were induced without a noticeable change in input resistance or resting membrane potential. After cis-ACPD, hyperpolarization in RMP by 6 and 9 mV when the extracellular potassium was reduced from 5 mM to 2 and 1 mM, did not change the potential range for activation of hysteresis. In two neurons input resistance increased 25 and 30% after cis-ACPD and in two other neurons 2 mM Cs+ increased input resistance >30% after muscarine. The potential range for the activation of hysteresis remained unchanged in all cases. Furthermore, the electrotonic decay of potential in the dendrites seems not to play a role in the reduction of the hysteresis by baclofen. In four neurons baclofen reduced hysteresis without changing the potential range for activating the inward current (Fig. 4), although the RMP hyperpolarized 6-10 mV and the input resistance was reduced up to 20%. Taken together, changes in electrotonic structure cannot be the only explanation for induction and suppression of plateau potentials and hysteresis.

In conclusion we have shown that receptor-mediated regulation of the current underlying plateau potentials in turtle motoneurons is associated with multiple changes in electrophysiological cell properties. The simplest explanation for our findings is to assume that agonists of mGluR, muscarine, and GABAB receptors, in addition to their other effects, modulate L-type calcium channels. Enhanced voltage sensitivity of L-type Ca2+ channels induced by muscarine (Kamishima et al. 1992) and agonists acting on group I mGluR (Chavis et al. 1995, 1996; Riedel 1996) and suppression L-type calcium currents by agonists of GABAB receptors (Anwyl 1991) are known in other cell types. It is also clear, however, that other conductances, contributing to RMP and input resistance in motoneurons, are affected by the modulating agonists used. These may well include the conductances regulated by serotonin and noradrenalin in neonatal motoneurons (Berger and Takahashi 1990, Elliott and Wallis 1992; Larkman and Kelly 1992). More complex schemes involving modulation of Ca dependent potassium and cation channels cannot be ruled out either.

The regulation of plateau generation and bistability in motoneurons by neurotransmitters may be important for generation of motor commands because it provides a way to change the integration of synaptic potentials. When short-lasting activity in motoneurons is required, ohmic integration of the synaptic potentials may be sufficient although continuous input is needed to keep the cell firing. During long-lasting activity, bistable properties of motoneurons could be superior because they allow the minimization of needed synaptic input: the input is needed only to switch the neuron between activity and silence (Gutman 1994). Recent findings show that metabotropic regulation of plateau properties can be induced synaptically (Delgado-Lezama et al. 1997).

    ACKNOWLEDGEMENTS

  We thank A. Gutman for reading the manuscripts and critical notes.

  This work was supported by the Danish Medical Research Council, the Lundbeck Foundation, and the Novo-Nordisk Foundation.

    FOOTNOTES

  Address for reprint requests: J. Hounsgaard, Dept. of Medical Physiology, The PANUM Institute, Building 12-5-9, University of Copenhagen, Blegdamsvej 3, DK-2200 Copenhagen N, Denmark.

  Received 5 May 1997; accepted in final form 22 September 1997.

    REFERENCES
Abstract
Introduction
Methods
Results
Discussion
References
0022-3077/98 $5.00 Copyright ©1998 The American Physiological Society



This article has been cited by other articles:


Home page
 J. Neurophysiol.Home page
L. D. Ellis, R. Krahe, C. W. Bourque, R. J. Dunn, and M. J. Chacron
Muscarinic Receptors Control Frequency Tuning Through the Downregulation of an A-Type Potassium Current
J Neurophysiol, September 1, 2007; 98(3): 1526 - 1537.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurophysiol.Home page
X. Li and D. J. Bennett
Apamin-Sensitive Calcium-Activated Potassium Currents (SK) Are Activated by Persistent Calcium Currents in Rat Motoneurons
J Neurophysiol, May 1, 2007; 97(5): 3314 - 3330.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurophysiol.Home page
P. J. Harvey, X. Li, Y. Li, and D. J. Bennett
Endogenous Monoamine Receptor Activation Is Essential for Enabling Persistent Sodium Currents and Repetitive Firing in Rat Spinal Motoneurons
J Neurophysiol, September 1, 2006; 96(3): 1171 - 1186.
[Abstract] [Full Text] [PDF]

Home page
 J. Physiol.Home page
A. Nistri, K. Ostroumov, E. Sharifullina, and G. Taccola
Tuning and playing a motor rhythm: how metabotropic glutamate receptors orchestrate generation of motor patterns in the mammalian central nervous system
J. Physiol., April 15, 2006; 572(2): 323 - 334.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurosci.Home page
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]

Home page
 J. Physiol.Home page
S. M. ElBasiouny, D. J. Bennett, and V. K. Mushahwar
Simulation of Ca2+ persistent inward currents in spinal motoneurones: mode of activation and integration of synaptic inputs
J. Physiol., January 15, 2006; 570(2): 355 - 374.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurophysiol.Home page
T. V. Bui, M. Ter-Mikaelian, D. Bedrossian, and P. K. Rose
Computational Estimation of the Distribution of L-type Ca2+ Channels in Motoneurons Based on Variable Threshold of Activation of Persistent Inward Currents
J Neurophysiol, January 1, 2006; 95(1): 225 - 241.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurosci.Home page
J.-F. Perrier and R. Delgado-Lezama
Synaptic Release of Serotonin Induced by Stimulation of the Raphe Nucleus Promotes Plateau Potentials in Spinal Motoneurons of the Adult Turtle
J. Neurosci., August 31, 2005; 25(35): 7993 - 7999.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurophysiol.Home page
M. K. Floeter, P. Zhai, R. Saigal, Y. Kim, and J. Statland
Motor Neuron Firing Dysfunction in Spastic Patients With Primary Lateral Sclerosis
J Neurophysiol, August 1, 2005; 94(2): 919 - 927.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurosci.Home page
A. Alaburda, R. Russo, N. MacAulay, and J. Hounsgaard
Periodic High-Conductance States in Spinal Neurons during Scratch-Like Network Activity in Adult Turtles
J. Neurosci., July 6, 2005; 25(27): 6316 - 6321.
[Abstract] [Full Text] [PDF]

Home page
 J. Physiol.Home page
D Derjean, S Bertrand, F Nagy, and S. J Shefchyk
Plateau potentials and membrane oscillations in parasympathetic preganglionic neurones and intermediolateral neurones in the rat lumbosacral spinal cord
J. Physiol., March 1, 2005; 563(2): 583 - 596.
[Abstract] [Full Text] [PDF]

Home page
 J. Physiol.Home page
J.-F. Perrier and M. C. Tresch
Recruitment of motor neuronal persistent inward currents shapes withdrawal reflexes in the frog
J. Physiol., January 15, 2005; 562(2): 507 - 520.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurophysiol.Home page
Y. Li, X. Li, P. J. Harvey, and D. J. Bennett
Effects of Baclofen on Spinal Reflexes and Persistent Inward Currents in Motoneurons of Chronic Spinal Rats With Spasticity
J Neurophysiol, November 1, 2004; 92(5): 2694 - 2703.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurosci.Home page
C. B. Hart and S. F. Giszter
Modular Premotor Drives and Unit Bursts as Primitives for Frog Motor Behaviors
J. Neurosci., June 2, 2004; 24(22): 5269 - 5282.
[Abstract] [Full Text] [PDF]

Home page
 J. Physiol.Home page
E. A. L. Muennich and R. E. W. Fyffe
Focal aggregation of voltage-gated, Kv2.1 subunit-containing, potassium channels at synaptic sites in rat spinal motoneurones
J. Physiol., February 1, 2004; 554(3): 673 - 685.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurophysiol.Home page
R. Delgado-Lezama, J. Aguilar, and R. Cueva-Rolon
Synaptic Strength Between Motoneurons and Terminals of the Dorsolateral Funiculus Is Regulated by GABA Receptors in the Turtle Spinal Cord
J Neurophysiol, January 1, 2004; 91(1): 40 - 47.
[Abstract] [Full Text]

Home page
 J. Neurophysiol.Home page
J. J. Kuo, R. H. Lee, M. D. Johnson, H. M. Heckman, and C. J. Heckman
Active Dendritic Integration of Inhibitory Synaptic Inputs In Vivo
J Neurophysiol, December 1, 2003; 90(6): 3617 - 3624.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurosci.Home page
A. Alaburda and J. Hounsgaard
Metabotropic Modulation of Motoneurons by Scratch-Like Spinal Network Activity
J. Neurosci., September 24, 2003; 23(25): 8625 - 8629.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurophysiol.Home page
Y. Li and D. J. Bennett
Persistent Sodium and Calcium Currents Cause Plateau Potentials in Motoneurons of Chronic Spinal Rats
J Neurophysiol, August 1, 2003; 90(2): 857 - 869.
[Abstract] [Full Text] [PDF]

Home page
 J. Neurophysiol.Home page
J.-F. Perrier and J. Hounsgaard
5-HT2 Receptors Promote Plateau Potentials in Turtle Spinal Motoneurons by Faci