HOME HELP FEEDBACK SUBSCRIPTIONS ARCHIVE SEARCH TABLE OF CONTENTS		QUICK SEARCH:   [advanced] Author: Keyword(s): Year:  Vol:  Page:

This Article Abstract Full Text (PDF) All Versions of this Article: 96/2/931    most recent 00309.2006v1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal 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 ISI Web of Science (5) Citing Articles via Google Scholar Google Scholar Articles by Biró, Z. Articles by Grillner, S. Search for Related Content PubMed PubMed Citation Articles by Biró, Z. Articles by Grillner, S.

REPORT

5-HT Modulation of Identified Segmental Premotor Interneurons in the Lamprey Spinal Cord

Department of Neuroscience, the Nobel Institute for Neurophysiology, Karolinska Institutet, Stockholm, Sweden

Submitted 22 March 2006; accepted in final form 8 May 2006

	ABSTRACT

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION GRANTS ACKNOWLEDGMENTS REFERENCES

 
Ipsilaterally projecting spinal excitatory interneurons (EINs) generate the hemisegmental rhythmic locomotor activity in lamprey, while the commissural interneurons ensure proper left-right alternation. 5-HT is a potent modulator of the locomotor rhythm and is endogenously released from the spinal cord during fictive locomotion. The effect of 5-HT was investigated for three segmental premotor interneuron types: EINs, commissural excitatory and commissural inhibitory interneurons. All three types of interneurons produced chemical postsynaptic potentials in motoneurons, but only those from EINs had an electrical component. The effect of 5-HT was studied on the slow afterhyperpolarization, involved in spike frequency regulation, and on the segmental synaptic transmission to motoneurons. 5-HT induced a reduction in the slow afterhyperpolarization and a depression of synaptic transmission in all three types of segmental interneurons. Thus 5-HT is a very potent modulator of membrane properties and synaptic transmission of last-order segmental premotor interneurons. Such modulation of locomotor network interneurons can partially account for the observed effects of 5-HT on the swimming pattern in lamprey.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION GRANTS ACKNOWLEDGMENTS REFERENCES

 
Serotonin (5-HT) is a powerful modulator of the locomotor network in all vertebrates studied (Schmidt and Jordan 2000). In lamprey, 5-HT slows down the locomotor frequency, increases burst intensity and burst duration, and makes the locomotor rhythm more regular (Harris-Warrick and Cohen 1985; Wallén et al. 1989; Zhang and Grillner 2000). Spinal 5-HT is supplied from descending fibers, dorsal root ganglia and from cells below the central canal throughout the length of the spinal cord, forming a plexus, into which interneurons (INs) and motoneurons (MNs) extend their dendrites (Christenson et al. 1991). 5-HT is endogenously released during fictive locomotion (Christenson et al. 1989; Kemnitz et al. 1995; Zhang and Grillner 2000).

5-HT decreases the slow postspike afterhyperpolarization (sAHP) in motoneurons, crossed caudal (CCINs), and lateral interneurons (Wallén et al. 1989). The sAHP is mainly due to apamin-sensitive calcium-activated potassium channels of the SK type (El Manira et al. 1994; Hill et al. 1992). These channels are activated by Ca²⁺ entry via N-type channels (Wikström and El Manira 1998), which in turn are depressed via 5-HT_1A receptors in lamprey spinal neurons (Hill et al. 2003). 5-HT also depresses excitatory chemical synaptic transmission between excitatory interneurons (EINs) and motoneurons (Parker and Grillner 1999).

EINs play a key role in generating the locomotor activity, and the sAHP plays an important role in the regulating neuronal firing frequency (Grillner 2003). The effect of 5-HT on the sAHP of EINs had not been investigated and was one of the main aims of this project, as was exploration of the effects on the sAHP of the segmental commissural interneurons. A further aim was to determine whether these interneurons are modulated by 5-HT similarly to EINs with respect to synaptic transmission. Because of the paucity of information available, an electrophysiological profile of these interneuron types is also reported.

	METHODS

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION GRANTS ACKNOWLEDGMENTS REFERENCES

 
Electrophysiology

All experimental procedures were carried out in accordance with institutional guidelines and the regulations of the local ethical committee (Stockholms norra djurförsöksetiska nämnd). Thirty-eight adult river lampreys (Lampetra fluviatilis) were included in this study. The general experimental arrangement is illustrated in Fig. 1A. 5-HT (10 µM; Sigma, St. Louis, MO) was dissolved in physiological solution and administered by chilled perfusion for 3–10 min.

View larger version (24K): [in this window] [in a new window]   FIG. 1. A schematic of the experimental preparation and the electrophysiological profile of last-order segmental premotor interneurons. A: spinal cord was isolated and mounted ventral side up in a recording chamber. Interneurons (IN) were stimulated and recorded intracellularly using microelectrodes to measure the fast AHP, slow AHP presynaptically (presyn.) and the chemical (chem.) and electrical (elec.) postsynaptic (postsyn.) potentials were recorded in motoneurons (MN). B: mean sAHP amplitudes: EIN 1.81 ± 0.34 mV; CEIN 1.23 ± 0.20 mV; CIIN 0.95 ± 0.22 mV. C: mean fAHP amplitudes: EIN 4.70 ± 1.0 mV; CEIN 2.36 ± 0.54 mV; CIIN 4.55 ± 0.83 mV. D: membrane potential ranges at which measurements were made in the same population of the respective IN type. E: chemical PSP responses in MNs. Mean amplitudes: EIN 0.55 ± 0.15 mV; CEIN 0.57 ± 0.09 mV; CIIN 0.38 ± 0.07 mV. F: electrical PSPs. Only EINs had an electrical component. G: mean resting membrane potentials of MNs corresponding to the same population of the respective IN type.

Identification of motoneurons (MNs), and, for interneurons, the presence of an intersegmental commissural caudally projecting axon (a defining characteristic of CCINs) was established by previously described methods (Buchanan 1982). A monosynaptic PSP in a MN and a spike at the cut caudal end of the spinal cord were taken as evidence for an intersegmental axon collateral. Except for identification purposes, the experiments were carried out with low-frequency intracellular stimulation (1 Hz) of the interneuron.

The amplitudes of the slow and fast AHPs (fAHPs) and PSPs were measured with respect to the average membrane potential for 10 ms preceding the action potential (baseline). The amplitude of the sAHP was measured from a depolarization level where the peak of the afterdepolarization, which immediately follows the fAHP, was aligned to the baseline (Cangiano et al. 2002). Usually this alignment required DC current injection.

Statistical analysis

Statistical comparisons were performed with paired Student's t-test, or repeated measures ANOVA. Data are reported as means ± SE. Twenty or more traces were averaged for calculating the mean. With regard to the 5-HT effects, no difference was observed between rostrally and caudally projecting interneurons (in relation to the postsynaptic motoneuron), including those with axon collaterals exceeding five segments. The results were therefore pooled in the analysis. N-values refer to the number of IN-MN pairs. Quantitative data are presented in the figures.

Histochemistry and visualization

For labeling, neurons were injected with biocytin (2 mg/ml), fixed in paraformaldehyde and incubated in carbocyanine 3-conjugated streptavidin (2 µg/ml; Jackson Immuno Research, West Grove, PA) in Triton-X 100 for 16 h, dehydrated, and mounted. The tissue was scanned using a Sarastro Phoibos 1000 confocal microscope (Molecular Dynamics, Sunnyvale, CA).

	RESULTS

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION GRANTS ACKNOWLEDGMENTS REFERENCES

 
Electrophysiological profile of segmentally projecting premotor interneurons

All 55 last-order premotor interneurons that were included in the analysis for an electrophysiological profile had sAHPs (Fig. 1, A and B), fAHPs (Fig. 1, A and C) and produced small amplitude monosynaptic PSPs in motoneurons (Fig. 1, A and E). These properties and the average membrane potentials at which each parameter were measured (Fig. 1, D and G), were similar for all three types of interneuron. An early electric, presumably gap junction-mediated, component was present in a majority of the EINs (Fig. 1, A and F), as previously reported (Parker 2003). It is interesting to note that none of the commissural excitatory (CEIN) or inhibitory (CIIN) interneurons had an electrical component (n = 39). The mean synaptic latency was between 5 and 6.6 ms for EINs (n = 16), CEINs (n = 22), and CIINs (n = 17). In addition to the segmental synapse, two of eight CIINs tested (four from the 5-HT results, see following text) had a long-projecting axon collateral (>5 segments; Ohta et al. 1991), whereas there was no evidence for this in two CEINs tested.

We investigated the effect of 5-HT on the sAHP in EINs and on the synaptic transmission between EINs and motoneurons. In all cases (n = 6), brief application of 5-HT (10 µM) resulted in a depression of the sAHP amplitude, with a mean depression to 38% of control, returning to control levels after washout (Fig. 2A, B). This depression was accompanied by a reduction of the EPSP in motoneurons (Fig. 2A) to 47% of control (Fig. 2B).

View larger version (23K): [in this window] [in a new window]   FIG. 2. The effect of 5-HT on EIN membrane properties and synaptic transmission. A: 5-HT reversibly reduces the sAHP in EINs (top). This reduction is accompanied by a depression of the EPSP amplitude of the EIN-to-MN synapse (bottom). The mean membrane potential for the MN traces shown in the left panel were –79.3 mV and –78.2 mV for control and 5-HT, respectively. The fAHP amplitude increased by a mean of 34% in 4/6 EINs (6.0 ± 1.8 mV to 8.0 ± 2.4 mV), while in 2/6 EINs it decreased by 13% (6.6 ± 0.22 to 5.71 ± 0.93) during 5-HT application. Scale bars: 2 mV (EIN, MN), 50 ms. B: the effect of 5-HT on EIN sAHP amplitude (1.70 ± 0.35 mV reduced to 0.64 ± 0.16 mV, P = 0.007) and synaptic transmission (0.68 ± 0.46 mV depressed to 0.32 ± 0.29 mV, at –69.4 ± 4.8 mV and –65.4 ± 8.0 mV, respectively, P = 0.038). Filled bars represent all the interneuron-MN pairs where 5-HT was applied, whereas unfilled bars represent the subset of these recordings where the pair was held long enough to also obtain a washout. (* = P < 0.05, ** = P < 0.01).

5-HT reduced both the sAHP of CEINs and the segmental synaptic transmission to motoneurons (as shown for two CEINs in Fig. 3, A and B). The mean sAHP amplitude was 61% of control following 5-HT application (Fig. 3C, top panel). Mean reduction for the EPSPs in motoneurons was to 37% of control (Fig. 3C, bottom panel). Neither of the two CEINs tested had long-projecting axon collaterals. Figure 3A shows an intracellular recording (left) from a biocytin-filled CEIN-MN pair (right).

View larger version (52K): [in this window] [in a new window]   FIG. 3. 5-HT effects on CEIN and CIIN membrane properties and synaptic transmission. A: left panel shows trace averages for a CEIN-MN pair that was labeled and scanned using a confocal microscope (right panel). Both the sAHP and the CEIN-to-MN EPSP is depressed during 5-HT application. Mean MN membrane potentials were –84.4 mV and –86.8 mV for control and 5-HT, respectively. This CEIN lacked a long caudally projecting axon collateral (>5 segments). Scale bars: 1 mV (CEIN), 0.5 mV (MN), 50 ms. The fAHP amplitude increased during 5-HT application in 6/7 CEINs with a mean increase of 66% (2.4 ± 0.9 mV to 4.0 ± 1.1 mV), while in one CEIN it decreased by 30% (5.3 mV to 3.7 mV). B: another CEIN where washout was obtained showing similar effects. The mean MN membrane potentials were –72.5 mV, –74.8 mV, and –74.5 mV for control, 5-HT, and washout, respectively. Scale bars: 2 mV (CEIN), 1 mV (MN), 50 ms. C: effect of 5-HT on CEIN sAHP amplitude (1.68 ± 0.39 mV reduced to 1.04 ± 0.41 mV, P = 0.028) and synaptic transmission (0.90 ± 0.25 mV depressed to 0.33 ± 0.22 mV, P = 0.035, at a mean motoneuron membrane potential of –75.8 ± 6.0 mV and –76.6 ± 6.6 mV, respectively). Filled and unfilled bars as in Fig. 2B. (*, P < 0.05) D: trace averages (left) showing the effect of 5-HT on an intracellularly labeled CIIN and its target motoneuron, and a confocal image of this pair is depicted on the right. A depression of the sAHP is accompanied by an increase in the fAHP amplitude. Also the CIIN-to-MN IPSP is reduced. The mean MN membrane potential is –87.3 mV for control, and –88.1 mV for 5-HT. This CIIN did not have a caudally projecting axon collateral (>5 segments). Scale bars: 0.5 mV (CIIN), 0.1 mV (MN), 50 ms. In 4/6 cases, reduction of the sAHP was accompanied by an increase of the mean fAHP amplitude by 64% (from 4.7 ± 1.5 mV to 7.7 ± 0.9 mV), whereas in two CIINs the mean decrease was 6% (7.7 ± 2.1 mV to 7.1 ± 2.3 mV). E: a CIIN-MN pair, where a washout was obtained, shows a significant and reversible depression of both the sAHP and synaptic transmission following 5-HT application. MN membrane potentials (in mV): –69.5, –71.3, –72.0 for control, 5-HT, and washout, respectively. Scale bars: 2 mV (CIIN), 1 mV (MN), 50 ms. F: The effect of 5-HT on CIIN sAHP amplitude (1.39 ± 0.29 mV reduced to 0.97 ± 0.21 mV, P = 0.011) and CIIN-to-MN synaptic transmission (0.49 ± 0.15 mV depressed to 0.17 ± 0.04 mV, P = 0.046, at a mean motoneuron membrane potential of –72.9 ± 3.4 mV and –74.6 ± 3.0 mV, respectively). Filled and unfilled bars as in Fig. 2B. (*, P < 0.05) cc, central canal; lm, lateral margin.

A brief application of 5-HT also reduced the sAHP of CIINs (as shown for two CIIN-MN pairs in Fig. 3, D and E) to 70% of control (Fig. 3F). Low frequency–evoked IPSPs to motoneurons were depressed to 35% of control following 5-HT application (Fig. 3, D–F). Two of four CIINs tested produced a fixed-latency extracellular response at the cut end of the spinal cord, five and eight segments caudal to the CIIN recording site. The right panel of Fig. 3D shows a confocal image of the CIIN and MN pair from which the intracellular recordings depicted on the left panel was obtained.

	DISCUSSION

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION GRANTS ACKNOWLEDGMENTS REFERENCES

 
Hemisegmental networks of EINs can alone generate rhythmic motor output, whereas glycinergic commissural interneurons provide reciprocal inhibition to ensure proper left-right alternation during swimming by the lamprey (Cangiano and Grillner 2003; Cohen and Harris-Warrick 1984). Interconnected EINs constitute the hemisegmental oscillators (Cangiano and Grillner 2005), and here we provide evidence that 5-HT decreases the sAHP of EINs.

The depression of the sAHP amplitude was typically accompanied by an increase in the fAHP amplitude (see Figs. 2A and 3, A–E). This may be due to the reduction of N-type Ca²⁺-currents by 5-HT (Hill et al. 2003), which would unmask the fast outward K⁺-current following the action potential, and due to an increase in the net driving force toward the K⁺ equilibrium potential as a result of the reduced sAHP.

We also found that the synaptic transmission to motoneurons is similarly depressed by 5-HT in all three types of segmental interneurons. This differs from the results in a previous study (Parker and Grillner 1999), where inhibitory CCIN synaptic transmission to MNs remained unchanged following 5-HT application.

In eight of ten interneurons in the present study, there was no evidence for a long-projecting axon collateral, and they therefore probably belong to the class of small commissural interneurons that may constitute 50% of the neurons in a segment (Buchanan and Grillner 1988; Ohta et al. 1991). These interneurons have elsewhere been reported to have mean PSP amplitudes of approximately twice those observed in the present study (Parker and Grillner 2000). The reasons for these discrepancies remain unclear.

Two CIINs had caudally projecting axon collaterals exceeding five segments in length (characteristic for CCINs; Buchanan 1982). Thus, a subpopulation of the inhibitory CCINs has segmental synapses to MNs, and 5-HT had the same effect on these as on the other interneurons.

As in a previous study (Parker 2003), we observed an electrical component in the EIN-evoked EPSPs in MNs; however, we found no electrical component in the motoneuron EPSPs from CEINs. This may reflect a difference in the synaptic organization between ipsi- and contralaterally projecting interneurons.

The overall effect of 5-HT at the network level is to reduce burst rate (Harris-Warrick and Cohen 1985) and also affect the intersegmental coordination (Matsushima and Grillner 1992). The reduction of the slow AHP will reduce the spike frequency adaptation and thereby contribute to prolongation of the burst activity (El Manira et al. 1994).

In summary, 5-HT produces the same types of effects on these three subtypes of segmental interneurons with regard to the sAHP as described elsewhere for MNs, CCINs, and lateral interneurons. Similarly, 5-HT reduces synaptic efficacy in all types of interneurons. This could not be assumed, because some modulators (e.g., substance P) exert different effects in different classes of interneurons (Parker and Grillner 1999). Such modulation of the sAHP and synaptic transmission in locomotor network interneurons would clearly contribute to the observed effects of 5-HT on the locomotor pattern.

	GRANTS

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION GRANTS ACKNOWLEDGMENTS REFERENCES

 
This study was supported by the Swedish Research Council, the Wallenberg Foundation, the European Commission, the Christopher Reeve Foundation, and Karolinska Institutet.

	ACKNOWLEDGMENTS

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION GRANTS ACKNOWLEDGMENTS REFERENCES

 
We thank O. Kiehn, T. Harkany, E. Nanou, and A.-C. Westerdahl for invaluable contributions.

	FOOTNOTES

 
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Address for reprint requests and other correspondence: S. Grillner, Department of Neuroscience, the Nobel Institute for Neurophysiology, Karolinska Institutet, SE 171 77 Stockholm, Sweden (E-mail: sten.grillner{at}ki.se)

	REFERENCES

TOP ABSTRACT INTRODUCTION METHODS RESULTS DISCUSSION GRANTS ACKNOWLEDGMENTS REFERENCES

 
Buchanan JT. Identification of interneurons with contralateral, caudal axons in the lamprey spinal cord: synaptic interactions and morphology. J Neurophysiol 47: 961–975, 1982.[Abstract/Free Full Text]

Buchanan JT and Grillner S. A new class of small inhibitory interneurones in the lamprey spinal cord. Brain Res 438: 404–407, 1988.[CrossRef][ISI][Medline]

Buchanan JT and Grillner S. Newly identified "glutamate interneurons" and their role in locomotion in the lamprey spinal cord. Science 236: 312–314, 1987.[Abstract/Free Full Text]

Cangiano L and Grillner S. Fast and slow locomotor burst generation in the hemispinal cord of the lamprey. J Neurophysiol 89: 2931–2942, 2003.[Abstract/Free Full Text]

Cangiano L and Grillner S. Mechanisms of rhythm generation in a spinal locomotor network deprived of crossed connections: the lamprey hemicord. J Neurosci 25: 923–935, 2005.[Abstract/Free Full Text]

Cangiano L, Wallén P, and Grillner S. Role of apamin-sensitive KCa channels for reticulospinal synaptic transmission to motoneuron and for the afterhyperpolarization. J Neurophysiol 88: 289–299, 2002.[Abstract/Free Full Text]

Christenson J, Franck J, and Grillner S. Increase in endogenous 5-hydroxytryptamine levels modulates the central network underlying locomotion in the lamprey spinal cord. Neurosci Lett 100: 188–192, 1989.[CrossRef][ISI][Medline]

Christenson J, Wallén P, Brodin L, and Grillner S. 5-HT systems in a lower vertebrate model: Ultrastructure, distribution, and synaptic and cellular mechanisms. In: Volume Transmission in the Brain: Novel Mechanisms for Neural Transmission, edited by Fuxe K and Aganati L. New York: Raven Press, 1991, p. 159–170.

Cohen AH and Harris-Warrick RM. Strychnine eliminates alternating motor output during fictive locomotion in the lamprey. Brain Res 293: 164–167, 1984.[CrossRef][ISI][Medline]

El Manira A, Tegnér J, and Grillner S. Calcium-dependent potassium channels play a critical role for burst termination in the locomotor network in lamprey. J Neurophysiol 72: 1852–1861, 1994.[Abstract/Free Full Text]

Grillner S. The motor infrastructure: from ion channels to neuronal networks. Nat Rev Neurosci 4: 573–586, 2003.[ISI][Medline]

Harris-Warrick RM, and Cohen AH. Serotonin modulates the central pattern for locomotion in the isolated lamprey spinal cord. J Exp Biol 116: 27–46, 1985.[Abstract/Free Full Text]

Hill R, Matsushima T, Schotland J, and Grillner S. Apamin blocks the slow AHP in lamprey and delays termination of locomotor bursts. Neuroreport 3: 943–945, 1992.[ISI][Medline]

Hill RH, Svensson E, Dewael Y, and Grillner S. 5-HT inhibits N-type but not the L-type Ca²⁺ channels via 5-HT1A receptors in lamprey spinal cord. Eur J Neurosci 18: 2919–2924, 2003.[CrossRef][ISI][Medline]

Kemnitz CP, Strauss TR, Hosford DM, and Buchanan JT. Modulation of swimming in the lamprey, Petromyzon marinus, by serotonergic and dopaminergic drugs. Neurosci Lett 201: 115–118, 1995.[CrossRef][ISI][Medline]

Matsushima T and Grillner S. Local serotonergic modulation of calcium-dependent potassium channels controls intersegmental coordination in the lamprey spinal cord. J Neurophysiol 67: 1683–1690, 1992.[Abstract/Free Full Text]

Ohta Y, Dubuc R, and Grillner S. A new population of neurons with crossed axons in the lamprey spinal cord. Brain Res 564: 143–148, 1991.[CrossRef][ISI][Medline]

Parker D. Variable Properties in a Single Class of Excitatory Spinal Synapse. J Neurosci 23: 3154–3163, 2003.[Abstract/Free Full Text]

Parker D and Grillner S. Activity-dependent metaplasticity of inhibitory and excitatory synaptic transmission in the lamprey spinal cord locomotor network. J Neurosci 19: 1647–1656, 1999.[Abstract/Free Full Text]

Parker D and Grillner S. The activity-dependent plasticity of segmental and intersegmental synaptic connections in the lamprey spinal cord. Eur J Neurosci 12: 2135–2146, 2000.[CrossRef][ISI][Medline]

Schmidt BJ and Jordan LM. The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord. Brain Res Bull 53: 689–710, 2000.[CrossRef][ISI][Medline]

Wallén P, Buchanan JT, Grillner S, Hill RH, Christenson J, and Hökfelt T. Effects of 5-hydroxytryptamine on the afterhyperpolarization, spike frequency regulation, and oscillatory properties in lamprey spinal cord neurons. J Neurophysiol 61: 759–768, 1989.[Abstract/Free Full Text]

Wikström MA, and El Manira A. Calcium influx through N- and P/Q-type channels activate apamin-sensitive calcium-dependent potassium channels generating the late afterhyperpolarization in lamprey spinal neurons. Eur J Neurosci 10: 1528–1532, 1998.[CrossRef][ISI][Medline]

Zhang W and Grillner S. The spinal 5-HT system contributes to the generation of fictive locomotion in lamprey. Brain Res 879: 188–192, 2000.[CrossRef][ISI][Medline]

This article has been cited by other articles:

				J. C. Petruska, R. M. Ichiyama, D. L. Jindrich, E. D. Crown, K. E. Tansey, R. R. Roy, V. R. Edgerton, and L. M. Mendell Changes in Motoneuron Properties and Synaptic Inputs Related to Step Training after Spinal Cord Transection in Rats J. Neurosci., April 18, 2007; 27(16): 4460 - 4471. [Abstract] [Full Text] [PDF]

				M. Huss, A. Lansner, P. Wallen, A. El Manira, S. Grillner, and J. H. Kotaleski Roles of Ionic Currents in Lamprey CPG Neurons: A Modeling Study J Neurophysiol, April 1, 2007; 97(4): 2696 - 2711. [Abstract] [Full Text] [PDF]

This Article Abstract Full Text (PDF) All Versions of this Article: 96/2/931    most recent 00309.2006v1 Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal 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 ISI Web of Science (5) Citing Articles via Google Scholar Google Scholar Articles by Biró, Z. Articles by Grillner, S. Search for Related Content PubMed PubMed Citation Articles by Biró, Z. Articles by Grillner, S.