© 2004 by The Society for Integrative and Comparative Biology
Cellular Mechanisms Underlying Swim Acceleration in the Pteropod Mollusk Clione limacina1
1 Abilene Christian University, Biology Department, Abilene, Texas 79699-7868
2 Arizona State University, Biology Department, Tempe, Arizona 85287-1501
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The pteropod mollusk Clione limacina swims by dorsal-ventral flapping movements of its wing-like parapodia. Two basic swim speeds are observed—slow and fast. Serotonin enhances swimming speed by increasing the frequency of wing movements. It does this by modulating intrinsic properties of swim interneurons comprising the swim central pattern generator (CPG). Here we examine some of the ionic currents that mediate changes in the intrinsic properties of swim interneurons to increase swimming speed in Clione. Serotonin influences three intrinsic properties of swim interneurons during the transition from slow to fast swimming: baseline depolarization, postinhibitory rebound (PIR), and spike narrowing. Current clamp experiments suggest that neither Ih nor IA exclusively accounts for the serotonin-induced baseline depolarization. However, Ih and IA both have a strong influence on the timing of PIR—blocking Ih increases the latency to PIR while blocking IA decreases the latency to PIR. Finally, apamin a blocker of IK(Ca) reverses serotonin-induced spike narrowing. These results suggest that serotonin may simultaneously enhance Ih and IK(Ca) and suppress IA to contribute to increases in locomotor speed.
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INTRODUCTION |
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Typically, Clione swim nearly continuously to maintain a stable position in the water column and avoid sinking due to negative buoyancy. Satterlie and Norekian (2001)
described the general mechanisms of locomotor speed change in Clione limacina. Clione swim by dorsal-ventral flapping movements of their wing-like parapodia. Two groups of antagonistic interneurons (six interneurons in the dorsal group and seven interneurons in the ventral group) comprise the Clione swim central pattern generator (CPG) that produces the basic slow swim rhythm (Arshavsky et al., 1985b). The two groups of interneurons reciprocally inhibit each other and exhibit postinhibitory rebound (PIR; Arshavsky et al., 1985c; Satterlie, 1985).
Initiation of swim acceleration occurs in response to prey during feeding and as an escape response to tactile stimuli applied to the wings, body, or tail (Arshavsky et al., 1985a). The Clione swim system uses many of the general mechanisms underlying locomotor speed changes including: 1) increases in limb cycle frequency, 2) increases in force of limb muscle contraction, and 3) changes in biomechanical properties of the locomotor system (Sillar et al., 1997). In Clione, serotonin mediates many of these changes in swim speed, both in whole animals and reduced preparations. Bath application of serotonin or endogenous release of serotonin through identified serotonergic modulatory neurons causes increases in swim speed by means of enhancement of both cycle frequency and contractile force (Satterlie and Norekian, 1995; Satterlie, 1995). A compartmental serotonergic modulatory system alters swim speed through the activity of subsets of serotonergic neurons and is potentially capable of modifying cycle frequency and contractile force independently (Satterlie and Norekian, 1996).
Neuromodulation involves several changes at the network, synaptic and cellular levels including enhanced synaptic efficacy, recruitment of previously inactive neurons, and modification of the voltage-dependent and time-dependent properties of ion channels (Kaczmarek and Levitan, 1987; Levitan, 1988; Getting, 1989; Harris-Warrick and Marder, 1991; Calabrese, 1998; Grillner, 1999; El Manira and Wallén, 2000). Two groups of serotonergic cells in the cerebral ganglia of Clione (Cr-SA and Cr-SP neurons) modify swimming speed by modulating CPG interneurons and by recruiting additional interneurons and motoneurons into activity (Satterlie and Norekian, 1995).
Cr-S neurons recruit two groups of neurons that affect Clione locomotor speed. First, Cr-S neurons recruit two pairs of large motoneurons (GEMNs) that innervate both slow-twitch and fast-twitch swim muscles throughout their ipsilateral wings. Recruitment of the GEMNs during fast swimming in turn activates the fast-twitch musculature to enhance the intensity of wing contractions. Second, a pair of pleural interneurons (type-12 interneurons) are also recruited during fast swimming by the Cr-S neurons (Satterlie and Norekian, 1996). The type-12 interneurons reconfigure the swim CPG by providing early excitation of the dorsal-phase swim interneurons and early inhibition of ventral-phase swim interneurons to shorten the cycle period of the swim rhythm (Arshavsky et al., 1985d).
Cr-S neuron activation also enhances the activity of a group of pedal serotonergic cells, the Pd-SW neurons. The axons of Pd-SW neurons extend from the pedal ganglia and innervate the slow-twitch swim musculature of the ipsilateral wing. Pd-SW neurons contribute to increased swim speed by enhancing contractility of the slow-twitch musculature, thus, modulating the force of muscle contraction. Pd-SW neurons can act independently of changes that occur centrally with regard to reconfiguration of the swim CPG and thereby can enhance locomotor performance within both slow and fast swimming modes (Satterlie, 1995; Satterlie and Norekian, 1996).
Bath application of serotonin or release of endogenous serotonin via direct Cr-S neuron stimulation induces three critical changes in swim interneurons of the basic CPG. First, serotonin depolarizes swim interneurons. Second, it enhances PIR amplitude and decreases in latency between the termination of hyperpolarization to peak PIR of swim interneurons. Third, serotonin decreases the spike duration of swim interneurons (Satterlie, 1991; Satterlie et al., 2000). Tonic depolarization increases excitability of swim interneurons by bringing them closer to spike threshold. Modifying the trajectory of PIR decreases the time between subsequent swim interneuron spikes and provides an additional temporary increase in excitability. Finally, the decrease in spike duration acts permissively to allow high cycle frequencies by preventing the long duration spikes from exceeding their half cycle duration.
Here we provide data on the ionic mechanisms that may underlie many of the changes in CPG interneurons that occur at the cellular level during the transition between slow and fast swimming behavior in Clione. We have used both intracellular and single electrode voltage clamp (SEVC) recording techniques to describe ionic mechanisms of swim acceleration that result from serotonergic modulation.
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Clione limacina were collected from the breakwater at Friday Harbor Laboratories, Friday Harbor, WA. Specimens were maintained in gallon jars and either partially submerged in flowing seawater tables at 10°C or placed in a refrigerator at 4°C. Animals were pinned on SYLGARD®-lined Petri dishes (3 cm diameter) using cactus spines (Opuntia sp.) prior to dissection. The dissected preparation consisted of the central ganglia and wings. To facilitate penetration of intracellular microelectrodes through the ganglionic sheath, the ganglia were bathed in protease (Sigma type XIV) for 3 to 5 min. at 1 mg/ml concentration then thoroughly washed in natural seawater. A similar proteolytic treatment using collagenase (Sigma blend collagenase) for 3–5 min. at a concentration of 1 mg/ml was used to help physical removal of the ganglionic sheath with fine forceps. Removing the ganglionic sheath was necessary to isolate swim interneurons for single electrode voltage clamp experiments due to electrical coupling in in situ preparations. Swim interneuron isolation was done according to methods previously described by Arshavsky et al. (1986)
and Satterlie et al. (2000), by pulling the cell out of the ganglia using the recording microelectrode. During the entire dissection and throughout the ensuing experiments, the preparation was submerged in a natural seawater bath. The temperature of the bath was kept constant at 10–12°C using a peltier device (Dagan Instruments, Inc.). The bath volume was kept constant at 3 ml, and drugs were administered by pipetting the appropriate volume of an isotonic stock solution of the drug directly to the bath to give the desired end concentration. All the drugs were soluble in sea water. A gravity fed perfusion system in combination with a peristaltic pump was used to exchange larger solution volumes (i.e., during high magnesium-high calcium saline administration and during wash in normal seawater). All drugs and chemicals used were obtained from SIGMA, Inc., (St. Louis MO) except apamin, which was purchased from Alomone Laboratories, Inc. (Israel). High magnesium-High calcium seawater (HI-DI) was made by adding 18.8 ml of 1 M MgCl2, 3.8 ml CaCl2, 0.8 ml 1 M KCl, and 51.6 ml of distilled water to 125 ml of natural seawater.
All electrophysiological recordings were made using Axon Instruments, Inc. AxoClamp 2B amplifier, Digidata 1321, and pCLAMP software. Electrodes were filled with 2M potassium acetate, and electrode resistances used for single electrode voltage clamp ranged from 5–10 M
while electrode resistances used for intracellular recording ranged from 10–30 M.
All averaged data are reported as mean ± SE. Paired sample t-tests were used to show significant differences between mean values measured under different conditions. An ANOVA with post hoc multiple comparison analysis was used to test for significant differences between multiple means.
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Ionic currents of swim interneurons
Preliminary single electrode voltage clamp experiments on physically isolated Clione swim interneurons suggest the presence of at least six different ionic currents. These include a sodium current (INa), a low-voltage-activated calcium current (LVA-ICa), a delayed rectifier potassium current (IK), an inactivating, transient potassium current (IA), a calcium-activated potassium current (IK(Ca)), and an hyperpolarization-activated cation current (Ih). Five of these are shown in Figure 1. The sixth, IK(Ca) is not directly shown, but is instead represented by the characteristic ‘N-shaped’ current-voltage relationship (Fig. 1F).
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The immediate goal is to find ionic currents that are serotonin-sensitive since applied serotonin, or activation of serotonergic cerebral neurons, triggers a distinct acceleration of swimming speed in Clione. However, we have thus far not been able to demonstrate direct serotonergic modulation of the ionic currents mediating swim acceleration. Our initial experiments presented here focus on the three subthreshold currents Ih, IA, and IK(Ca). By pharmacologically blocking these subtrheshold currents in separate current clamp experiments, we examine the function that they may play in the modulation of swimming speed with respect to the three characteristic changes that occur in CPG interneurons during swim accelerations—baseline depolarization, changes in PIR latency, and spike narrowing.
Role of Ih and IA in mediating baseline depolarization
Antagonists to Ih and IA, ZD7288 and 4-aminopyridine respectively, were used to test the hypothesis that Ih and IA mediate changes in baseline depolarization. In other systems, Ih is activated at hyperpolarizing voltages below resting membrane potential, and does not exhibit inactivation. Ih conducts both Na+ and K+ and has a reversal potential around –30 mV (Pape, 1996; Lüthi and McCormick, 1998). Furthermore, Ih is sensitive to selective block by two antagonists—CsCl and ZD7288 (Pape, 1996; Satoh and Yamada, 2000).
Both CsCl and ZD7288 were observed to hyperpolarize the membrane potential of Clione swim interneurons (Fig. 2). In this experiment, a 1:1 mixture of isotonic (0.333M) MgCl2 and seawater were initially applied to decrease excitability in the swim interneurons. Following addition of MgCl2/seatwater, the Ih antagonist ZD7288 (200 µM) hyperpolarized the membrane potential by 1.95 mV (Fig. 2A, B). Application of serotonin (1 µM) induced a large depolarization in membrane potential in the presence of ZD7288 suggesting that Ih does not appreciably contribute to membrane depolarization.
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The role of IA in mediating baseline depolarization was tested in a similar manner using 4-Aminopyridine (4-AP) to block IA. Activation of IA is known to hyperpolarize the membrane potential and increase the time between action potentials of neurons in other preparations (Hille, 1992
). To test the possibility that IA contributes to baseline depolarization, 4-AP (4 mM) was applied following addition of 1:1 MgCl2 as previously described. Blocking IA initially depolarized the swim interneuron and resulted in spike activity in this cell (Fig. 3), however, 4-AP application did not cause the sustained depolarization as observed in the presence of serotonin. Therefore, it is unlikely that either Ih or IA, acting alone, produce the baseline depolarization.
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Role of Ih and IA in changing the trajectory of PIR
To test the hypothesis that a serotonin-induced decrease in IA of Clione swim interneurons contributes to enhanced locomotory speed we applied 4-AP to reduced preparations. The serotonin antagonist, mianserin (10 µM) was added to the preparation to preclude any serotonin effects. Administration of 4-AP (4 mM) in the presence of minaserin significantly increased the swim cycle frequency (39%) from 1.41 ± 0.194 s–1 to 1.960 ± 0.205 s–1 (n = 50, average of ten consecutive cycles from five preparations, paired sample t-test, P < 0.05, Fig. 4).
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To examine PIR of Clione swim interneurons it was necessary to synaptically isolate the swim interneurons by applying high-magnesium-high-calcium seawater (HIDI), by applying tetrodotoxin (TTX, 10 µM), or by applying a combination of TTX, the cholinergic antagonist, atropine (1 mM), and the glutaminergic antagonist, CNQX (10 µM). By suppressing the synaptic activity in the preparation it was possible to clearly examine the effects of IA and Ih channel antagonists on PIR. The effect of 4-AP (4 mM) on the timing of PIR is shown in Figure 5A–C. 4-AP increases the duration range of hyperpolarizing current pulses that produce PIR and also significantly reduces the latency to PIR in Clione swim interneurons (from 202.3 ± 23.7 ms to 89.2 ± 15.5 ms). In these experiments, we normalized the latency data by dividing the latency in the presence of 4-AP (the experimental value) by the corresponding latency in normal saline (the control value). This was done to eliminate variability between preparations; a paired sample t-test was used to determine significance (n = 5, P < 0.05).
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The Ih antagonist, CsCl, has the opposite effect on the latency to PIR (Fig. 6). Application of CsCl (5 mM) significantly increases the latency to PIR (from 54.5 ± 8.80 ms to 105.4 ± 20.6 ms, n = 6, paired sample t-test, P < 0.05). In current clamp recordings, Ih activity is represented by a sag potential, a steady depolarization of the membrane potential that lasts the duration of hyperpolarizating current injection. The sag of Clione swim interneurons is blocked by CsCl, a blocker of Ih. A Cs-sensitive depolarizing sag that occurs during hyperpolarizing input is characteristic of Ih other preparations (Pape, 1996
; Robinson, 2003). The Ih antagonist, ZD7288 (200 mM) had similar effects on the latency and sag potential (data not shown).
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Role of IK(Ca) in mediating spike narrowing
Spike narrowing is involved in serotonin-induced swim acceleration in Clione, but only as a permissive change (Satterlie et al., 2000
). Serotonergic-induced spike narrowing is sensitive to TEA suggesting that activation or modulation of a potassium current mediates this response. Spike narrowing is affected by apamin, an antagonist of the small conductance calcium-activated potassium current (IK(Ca)), and this blocker significantly affects swim speed. Figure 7 illustrates the effects of serotonin and apamin on swim frequency and spike duration. Initially, addition of serotonin causes a significant increase in swim frequency accompanied by a decrease in spike duration. Serotonin significantly increased the mean cycle from 3.07 ± 0.103 s–1 to 4.65 ± 0.332 s–1 (51%, n = 30, ten consecutive cycles from three preparations, one-way ANOVA with post hoc multiple comparison test, F = 25.25, P < 0.05), and the decreased spike duration from 87.7 ± 9.55 ms to 55.9 ± 12.6 ms (36%, n = 30, ten consecutive spikes from three preparations, one-way ANOVA with post hoc multiple comparison test, F = 36.177, P < 0.05). Addition of apamin reverses the effects of serotonin, causing a significant reduction in mean swim frequency from 4.65 ± 0.332 s–1 to 2.44 ± 0.179 s–1 (48%, n = 30, ten consecutive cycles from three preparations, one-way ANOVA with post hoc multiple comparison test, F = 25.25, P < 0.05, Fig. 7) and a significant increase in mean spike duration 55.9 ± 12.6 ms to 79.1 ± 20.5 ms (42%, n = 30, ten consecutive spikes from three preparations, one-way ANOVA with post hoc multiple comparison test, F = 36.177, P < 0.05) in comparison to values for serotonin.
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Three subthreshold ionic currents are potential targets for serotonergic modulation of CPG interneurons and may contribute to altered swim speed in Clione limacina. IA and Ih affect the timing of the PIR response, and IK(Ca) affects spike narrowing. Neither IA nor Ih alone can account for the type of sustained depolarization observed when serotonin is applied. IA and Ih may contribute to baseline depolarization, but only in concert with each other or other currents. This contrasts with work done in other systems. Using a model LP neuron of the stomatogastric system, Golowasch et al. (1992) demonstrate that a decrease in the IK(Ca) conductance causes the model cell to depolarize by 5 mV. Current clamp experiments with Clione suggest that serotonin enhances IK(Ca) thus ruling out the possibility that this ionic current plays a similar role in baseline depolarization. A specific neuromodulator may modulate multiple ionic currents in a single neuron. For example, SCPb modulates multiple ion channels in identified neurons of Hermissenda to enhance excitability. SCPb reduces IA and IK but enhances IK(Ca), ICa, and INa with the net effect of causing depolarization (Acosta-Urquidi, 1988). On the other hand, Kiehn et al. (2000)
found that modulation of a single ionic current, Ih, influences the motor output in the mammalian spinal cord by tonic depolarization. Their data suggests that Ih enhancement acts as a leak conductance that depolarizes the membrane potential thereby increasing the rate of action potential production in neonatal rat spinal motoneurons.
The main property of Clione swim interneurons that is affected by Ih and IA is the timing of PIR. Blocking IA using 4-AP resulted in a shortening of the latency to PIR, while blocking Ih using CsCl resulted in a lengthening of the latency to PIR (Figs. 5–6). Serotonin had previously been shown to decrease the latency to PIR in Clione swim interneurons (Satterlie et al., 2000). Data presented here suggests that serotonin simultaneously inhibits IA and enhances Ih to shorten the latency to peak PIR. Reduction of IA and enhancement of Ih have not been directly demonstrated in voltage clamp experiments. Nonetheless, the changes in latency to PIR revealed in current clamp experiments when IA and Ih specific antagonists are applied suggest their role as modulation targets. Modulation of PIR latency brings the membrane potential of the swim interneurons to threshold more quickly, thereby speeding the onset of spike production in these cells increasing locomotor speed. Similar effects have been observed in the stomatogastric preparation of the lobster. Harris-Warrick et al. (1995) have shown that dopaminergic modulation reduces IA and enhances Ih to affect timing in the stomatogastric rhythm by shortening the latency to PIR in the isolated LP neuron. Furthermore, Kloppenburg et al. (1999) have shown that the opposite occurs in isolated PD neurons of the stomatogastric system. Here, enhancement of IA in isolated PD neurons leads to an increase in the latency to PIR in these cells. Thus, it appears that dopamine differentially modulates IA in different cells of the stomatogastric system to affect the timing of PIR in opposite ways.
Increases in swim speed are accompanied by spike narrowing in Clione swim interneurons. This was previously attributed to an enhancement of an unidentified potassium conductance (Satterlie et al., 2000) since application of the potassium channel blocker, tetraethylammonium (TEA, 10 mM), blocks serotonin-induced spike narrowing. Apamin, a blocker of the small conductance calcium activated potassium current (IK(Ca)), reverses serotonin-induced spike narrowing and causes a decrease in swim speed. Thus, serotonergic enhancement of an IK(Ca) contributes to both spike narrowing and increased swim speed in Clione. There could be other potassium currents that contribute to spike narrowing since TEA is a relatively nonspecific blocker of outward potassium currents in other molluscan preparations. However, the concentration range for TEA to block an appreciable amount of IK(Ca) in other mollusks can be considerably high—100 mM to block 20% of IK(Ca) in Tritonia (Thompson, 1982). While it is likely that the 10 mM concentration used in experiments by Satterlie et al. (2000) had only a slight effect on IK(Ca), we cannot rule out the possibility that TEA has a larger affect on IK(Ca). IK(Ca) of different neurons within a given species respond differently to TEA administration. For example, in some cells of Helix high concentrations of TEA (greater than about 100 mM) are necessary to block IK(Ca) while in other Helix neurons lower concentrations of TEA (less than about 1 mM) block IK(Ca) (Hermann and Hartung, 1983). Because apamin is a highly specific blocker of IK(Ca), it appears that serotonergic enhancement of this current plays a role in mediating swim speed changes.
IK(Ca) activates within a large range of both positive and negative membrane potentials, and thus participates in many neurophysiological processes. IK(Ca) may contribute to the resting membrane potential, to spike frequency adaptation, and to pacemaking (Hermann and Hartung, 1983). Hyperpolarization caused by IPSPs or activity of outward currents including IK(Ca) may result in activation of Ih (Lüthi and McCormick, 1998). Modulation of this type of interaction between Ih and IK(Ca) affects the oscillatory frequency of vertebrate inferior olive neurons (Bal and McCormick, 1997). Modulation of IK(Ca) also affects the output of neurons in motor systems. In the lamprey, application of N-methyl-d-aspartic acid (NMDA) increases the frequency of plateau potential oscillations characteristic of motoneurons and interneurons. This increase in frequency is inhibited by subsequent application of apamin (El Manira et al., 1994; Tegner et al., 1998). Addition of apamin also increases the duration of the plateau potential and lengthens the duration of hyperpolarization between plateau potentials. This suggests a role for IK(Ca) in mediating output frequency, at least in the low frequency range. IK(Ca) shortens the duration of the plateau potential, and by doing so increases the frequency of plateau potential oscillation (El Manira et al., 1994). Similar mechanisms may be involved in mediating speed changes in Clione. However, we do not know if serotonin directly affects IK(Ca). Serotonin could enhance calcium entry into the cell and this could have an indirect modulatory effect on IK(Ca).
Differential modulation of outward currents in Clione swim interneurons contribute to increased locomotor speed—inhibition of IA and enhancement of IK(Ca) and possibly IK. Furthermore, serotonin differentially modulates two currents, IA and Ih, to affect the latency to PIR. Finally, serotonin may directly or indirectly modulate IK(Ca) to enhance swim speed by contributing to spike narrowing, and enhancement of IK(Ca) may lead to an enhancement of Ih to circuitously contribute to increases in swim speed. It is obvious that serotonin targets multiple ionic conductances to trigger an increase in firing frequency in these cells. Most important, individual variables at the current clamp level—baseline depolarization, decreased PIR latency, and spike narrowing—are each altered through a collaborative modulation of more than a single ionic conductance.
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ACKNOWLEDGMENTS |
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We thank Dr. A. O. Dennis Willows and the staff of Friday Harbor Laboratories for their assistance and support of this research. The work was supported by NSF grant IBN-9904424 and NIH grant RO1 N539302 to R.A.S. and NSF IGERT grant DGE-9987619.
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1 From the Symposium Recent Developments in Neurobiology presented at the Annual meeting of the Society for Integrative and Comparative Biology, 4–8 January 2003 at Toronto, Canada.
2 E-mail: Thomas.Pirtle{at}acu.edu
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