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Balanced plasticity and stability of the electrical properties of a molluscan modulatory interneuron after classical conditioning: a computational study.

Vavoulis DV, Nikitin ES, Kemenes I, Marra V, Feng J, Benjamin PR, Kemenes G - Front Behav Neurosci (2010)

Bottom Line: In order to understand the ionic mechanisms of this novel combination of plasticity and stability of intrinsic electrical properties, we first constructed and validated a Hodgkin-Huxley-type model of the CGCs.Including in the model an additional increase in the conductance of a high-voltage-activated calcium current allowed the spike amplitude and spike duration also to be maintained after conditioning.We conclude therefore that a balanced increase in three identified conductances is sufficient to explain the electrophysiological changes found in the CGCs after classical conditioning.

View Article: PubMed Central - PubMed

Affiliation: Department of Computer Science, University of Warwick Coventry, UK.

ABSTRACT
The Cerebral Giant Cells (CGCs) are a pair of identified modulatory interneurons in the Central Nervous System of the pond snail Lymnaea stagnalis with an important role in the expression of both unconditioned and conditioned feeding behavior. Following single-trial food-reward classical conditioning, the membrane potential of the CGCs becomes persistently depolarized. This depolarization contributes to the conditioned response by facilitating sensory cell to command neuron synapses, which results in the activation of the feeding network by the conditioned stimulus. Despite the depolarization of the membrane potential, which enables the CGGs to play a key role in learning-induced network plasticity, there is no persistent change in the tonic firing rate or shape of the action potentials, allowing these neurons to retain their normal network function in feeding. In order to understand the ionic mechanisms of this novel combination of plasticity and stability of intrinsic electrical properties, we first constructed and validated a Hodgkin-Huxley-type model of the CGCs. We then used this model to elucidate how learning-induced changes in a somal persistent sodium and a delayed rectifier potassium current lead to a persistent depolarization of the CGCs whilst maintaining their firing rate. Including in the model an additional increase in the conductance of a high-voltage-activated calcium current allowed the spike amplitude and spike duration also to be maintained after conditioning. We conclude therefore that a balanced increase in three identified conductances is sufficient to explain the electrophysiological changes found in the CGCs after classical conditioning.

No MeSH data available.


Related in: MedlinePlus

Contribution of identified ionic currents to the electrical properties of the CGCs. (A) Contribution of the total sodium current. When washing the preparation into sodium-free saline, CGCs from the intact nervous system cease to fire and the membrane potential is significantly hyperpolarized (Ai; also see Staras et al., 2002). In the model, washing into sodium-free saline was simulated by gradually setting the maximal persistent and transient sodium conductances (gNaP and gNaT, respectively) to zero over a time interval of 60 s (Aii). This is equivalent to completely removing the transient and persistent sodium currents from the model, inducing the cell to stop firing and the membrane potential to settle at a very negative value (∼−90 mV), similarly to the biological neuron. (B) Contribution of the delayed rectifier potassium current to spike shape. When blocking ID by washing the preparation in 50 mM TEA (tetraethylammonium chloride), the duration of the action potentials recorded from CGCs in the intact nervous system increased significantly (Bi; also see Staras et al., 2002). Also, the after-hyperpolarization following each spike was reduced in amplitude. In the model, this situation was simulated by blocking the maximal conductance of the delayed rectifier, gD, by 30% (Bii). This resulted in spikes of longer duration by ∼17 ms and a smaller spike after-hyperpolarization by ∼12 mV, similarly to washing the biological neuron into saline containing TEA. (C) Contribution of the high-voltage-activated calcium current to spike shape. When blocking IHVA by washing the preparation into 100-μM CdCl2, the spikes recorded from CGCs in the intact nervous system became shorter and narrower and the spike after-hyperpolarization was reduced in amplitude (Ci; Staras et al., 2002). In the model, blocking IHVA by CdCl2 was simulated by setting gHVA, the maximal conductance of the high-voltage-activated calcium current, equal to zero (Cii). This resulted in spikes losing their characteristic “shoulder” and becoming narrower and shorter by ∼6 ms and ∼17 mV respectively, similarly to recordings from the biological neuron after the application of CdCl2.
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Figure 5: Contribution of identified ionic currents to the electrical properties of the CGCs. (A) Contribution of the total sodium current. When washing the preparation into sodium-free saline, CGCs from the intact nervous system cease to fire and the membrane potential is significantly hyperpolarized (Ai; also see Staras et al., 2002). In the model, washing into sodium-free saline was simulated by gradually setting the maximal persistent and transient sodium conductances (gNaP and gNaT, respectively) to zero over a time interval of 60 s (Aii). This is equivalent to completely removing the transient and persistent sodium currents from the model, inducing the cell to stop firing and the membrane potential to settle at a very negative value (∼−90 mV), similarly to the biological neuron. (B) Contribution of the delayed rectifier potassium current to spike shape. When blocking ID by washing the preparation in 50 mM TEA (tetraethylammonium chloride), the duration of the action potentials recorded from CGCs in the intact nervous system increased significantly (Bi; also see Staras et al., 2002). Also, the after-hyperpolarization following each spike was reduced in amplitude. In the model, this situation was simulated by blocking the maximal conductance of the delayed rectifier, gD, by 30% (Bii). This resulted in spikes of longer duration by ∼17 ms and a smaller spike after-hyperpolarization by ∼12 mV, similarly to washing the biological neuron into saline containing TEA. (C) Contribution of the high-voltage-activated calcium current to spike shape. When blocking IHVA by washing the preparation into 100-μM CdCl2, the spikes recorded from CGCs in the intact nervous system became shorter and narrower and the spike after-hyperpolarization was reduced in amplitude (Ci; Staras et al., 2002). In the model, blocking IHVA by CdCl2 was simulated by setting gHVA, the maximal conductance of the high-voltage-activated calcium current, equal to zero (Cii). This resulted in spikes losing their characteristic “shoulder” and becoming narrower and shorter by ∼6 ms and ∼17 mV respectively, similarly to recordings from the biological neuron after the application of CdCl2.

Mentions: As a first example, we examined the effect of removing the persistent and transient sodium currents from the model. In the intact nervous system, bathing the preparation in zero-Na+ saline caused the CGCs to stop firing and hyperpolarize to a very negative potential (Figure 5Ai; also see Staras et al., 2002; Nikitin et al., 2008). Artificially repolarizing the cell above the firing threshold failed to evoke action potentials, but washing back into normal saline caused the CGCs to start firing again, with no apparent change in the spike shape (Staras et al., 2002).


Balanced plasticity and stability of the electrical properties of a molluscan modulatory interneuron after classical conditioning: a computational study.

Vavoulis DV, Nikitin ES, Kemenes I, Marra V, Feng J, Benjamin PR, Kemenes G - Front Behav Neurosci (2010)

Contribution of identified ionic currents to the electrical properties of the CGCs. (A) Contribution of the total sodium current. When washing the preparation into sodium-free saline, CGCs from the intact nervous system cease to fire and the membrane potential is significantly hyperpolarized (Ai; also see Staras et al., 2002). In the model, washing into sodium-free saline was simulated by gradually setting the maximal persistent and transient sodium conductances (gNaP and gNaT, respectively) to zero over a time interval of 60 s (Aii). This is equivalent to completely removing the transient and persistent sodium currents from the model, inducing the cell to stop firing and the membrane potential to settle at a very negative value (∼−90 mV), similarly to the biological neuron. (B) Contribution of the delayed rectifier potassium current to spike shape. When blocking ID by washing the preparation in 50 mM TEA (tetraethylammonium chloride), the duration of the action potentials recorded from CGCs in the intact nervous system increased significantly (Bi; also see Staras et al., 2002). Also, the after-hyperpolarization following each spike was reduced in amplitude. In the model, this situation was simulated by blocking the maximal conductance of the delayed rectifier, gD, by 30% (Bii). This resulted in spikes of longer duration by ∼17 ms and a smaller spike after-hyperpolarization by ∼12 mV, similarly to washing the biological neuron into saline containing TEA. (C) Contribution of the high-voltage-activated calcium current to spike shape. When blocking IHVA by washing the preparation into 100-μM CdCl2, the spikes recorded from CGCs in the intact nervous system became shorter and narrower and the spike after-hyperpolarization was reduced in amplitude (Ci; Staras et al., 2002). In the model, blocking IHVA by CdCl2 was simulated by setting gHVA, the maximal conductance of the high-voltage-activated calcium current, equal to zero (Cii). This resulted in spikes losing their characteristic “shoulder” and becoming narrower and shorter by ∼6 ms and ∼17 mV respectively, similarly to recordings from the biological neuron after the application of CdCl2.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2871690&req=5

Figure 5: Contribution of identified ionic currents to the electrical properties of the CGCs. (A) Contribution of the total sodium current. When washing the preparation into sodium-free saline, CGCs from the intact nervous system cease to fire and the membrane potential is significantly hyperpolarized (Ai; also see Staras et al., 2002). In the model, washing into sodium-free saline was simulated by gradually setting the maximal persistent and transient sodium conductances (gNaP and gNaT, respectively) to zero over a time interval of 60 s (Aii). This is equivalent to completely removing the transient and persistent sodium currents from the model, inducing the cell to stop firing and the membrane potential to settle at a very negative value (∼−90 mV), similarly to the biological neuron. (B) Contribution of the delayed rectifier potassium current to spike shape. When blocking ID by washing the preparation in 50 mM TEA (tetraethylammonium chloride), the duration of the action potentials recorded from CGCs in the intact nervous system increased significantly (Bi; also see Staras et al., 2002). Also, the after-hyperpolarization following each spike was reduced in amplitude. In the model, this situation was simulated by blocking the maximal conductance of the delayed rectifier, gD, by 30% (Bii). This resulted in spikes of longer duration by ∼17 ms and a smaller spike after-hyperpolarization by ∼12 mV, similarly to washing the biological neuron into saline containing TEA. (C) Contribution of the high-voltage-activated calcium current to spike shape. When blocking IHVA by washing the preparation into 100-μM CdCl2, the spikes recorded from CGCs in the intact nervous system became shorter and narrower and the spike after-hyperpolarization was reduced in amplitude (Ci; Staras et al., 2002). In the model, blocking IHVA by CdCl2 was simulated by setting gHVA, the maximal conductance of the high-voltage-activated calcium current, equal to zero (Cii). This resulted in spikes losing their characteristic “shoulder” and becoming narrower and shorter by ∼6 ms and ∼17 mV respectively, similarly to recordings from the biological neuron after the application of CdCl2.
Mentions: As a first example, we examined the effect of removing the persistent and transient sodium currents from the model. In the intact nervous system, bathing the preparation in zero-Na+ saline caused the CGCs to stop firing and hyperpolarize to a very negative potential (Figure 5Ai; also see Staras et al., 2002; Nikitin et al., 2008). Artificially repolarizing the cell above the firing threshold failed to evoke action potentials, but washing back into normal saline caused the CGCs to start firing again, with no apparent change in the spike shape (Staras et al., 2002).

Bottom Line: In order to understand the ionic mechanisms of this novel combination of plasticity and stability of intrinsic electrical properties, we first constructed and validated a Hodgkin-Huxley-type model of the CGCs.Including in the model an additional increase in the conductance of a high-voltage-activated calcium current allowed the spike amplitude and spike duration also to be maintained after conditioning.We conclude therefore that a balanced increase in three identified conductances is sufficient to explain the electrophysiological changes found in the CGCs after classical conditioning.

View Article: PubMed Central - PubMed

Affiliation: Department of Computer Science, University of Warwick Coventry, UK.

ABSTRACT
The Cerebral Giant Cells (CGCs) are a pair of identified modulatory interneurons in the Central Nervous System of the pond snail Lymnaea stagnalis with an important role in the expression of both unconditioned and conditioned feeding behavior. Following single-trial food-reward classical conditioning, the membrane potential of the CGCs becomes persistently depolarized. This depolarization contributes to the conditioned response by facilitating sensory cell to command neuron synapses, which results in the activation of the feeding network by the conditioned stimulus. Despite the depolarization of the membrane potential, which enables the CGGs to play a key role in learning-induced network plasticity, there is no persistent change in the tonic firing rate or shape of the action potentials, allowing these neurons to retain their normal network function in feeding. In order to understand the ionic mechanisms of this novel combination of plasticity and stability of intrinsic electrical properties, we first constructed and validated a Hodgkin-Huxley-type model of the CGCs. We then used this model to elucidate how learning-induced changes in a somal persistent sodium and a delayed rectifier potassium current lead to a persistent depolarization of the CGCs whilst maintaining their firing rate. Including in the model an additional increase in the conductance of a high-voltage-activated calcium current allowed the spike amplitude and spike duration also to be maintained after conditioning. We conclude therefore that a balanced increase in three identified conductances is sufficient to explain the electrophysiological changes found in the CGCs after classical conditioning.

No MeSH data available.


Related in: MedlinePlus