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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

Basic electrical activity in the model and biological CGCs. (A) Spontaneous tonic firing in the fitted model and the biological neuron (Data). In the absence of external or synaptic input, both fire at approximately 0.7 Hz. Dashed rectangle indicates the overlapping real and simulated spike, respectively, shown on an expanded voltage and time scale in (B). (B) Shape of the action potential in the model and biological CGCs. In both the model and biological neuron, the shape of the action potential is very similar, with the duration being approximately 17 ms (measured at −20 mV) and amplitude being approximately 115 mV. The arrow indicates the characteristic “shoulder” of the action potential during its repolarisation phase. (C) Current-frequency response in the model and the biological neuron. In both, externally injected currents in the range 0–2 nA induce spikes at frequencies up to approximately 15 Hz. To aid clarity, the frequency data shown for the biological neuron come from a single experiment where the same CGC was tested with increasing amounts of current injected into the soma through one electrode while recording spike activity through a second electrode. The same test was repeated with 4 more CGCs in different preparations. The membrane potential of all five neurons tested this way was set at −80 mV prior to each test and so the frequency responses to the same amount of current showed very little variance between the individual neurons.
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Figure 4: Basic electrical activity in the model and biological CGCs. (A) Spontaneous tonic firing in the fitted model and the biological neuron (Data). In the absence of external or synaptic input, both fire at approximately 0.7 Hz. Dashed rectangle indicates the overlapping real and simulated spike, respectively, shown on an expanded voltage and time scale in (B). (B) Shape of the action potential in the model and biological CGCs. In both the model and biological neuron, the shape of the action potential is very similar, with the duration being approximately 17 ms (measured at −20 mV) and amplitude being approximately 115 mV. The arrow indicates the characteristic “shoulder” of the action potential during its repolarisation phase. (C) Current-frequency response in the model and the biological neuron. In both, externally injected currents in the range 0–2 nA induce spikes at frequencies up to approximately 15 Hz. To aid clarity, the frequency data shown for the biological neuron come from a single experiment where the same CGC was tested with increasing amounts of current injected into the soma through one electrode while recording spike activity through a second electrode. The same test was repeated with 4 more CGCs in different preparations. The membrane potential of all five neurons tested this way was set at −80 mV prior to each test and so the frequency responses to the same amount of current showed very little variance between the individual neurons.

Mentions: An overview of the spike shape and firing activity of the fitted model is given in Figure 4. The model was compared to an intracellular current-clamp recording from axotomized cells, which demonstrated a close agreement in the spontaneous tonic firing activity (Figure 4A), spike shape (Figure 4B) and current-frequency response (Figure 4C) between the model and the biological neuron. In the absence of synaptic or experimentally applied input both the biological and the model CGCs fire at a mean frequency of ∼0.7 Hz (∼42 spikes/min; Figure 4A). Typically, an action potential starts as a gradual depolarization of the cell membrane that becomes very rapid after a threshold (∼−50 mV) is crossed (Figure 4B). The spike reaches a peak of approximately +40 mV, which is followed by a repolarization phase with a pronounced “shoulder” (indicated by an arrow in Figure 4B). At its most hyperpolarized state, immediately after the spike, the membrane potential reached a value of about −75 mV, before returning gradually to its baseline value (∼−60 mV). The spike had a total duration of ∼17 ms (measured at −20 mV). Furthermore, when injected with constant currents of increasing amplitude, the model responded with an increase in its firing frequency, which was in close agreement with the response of the biological neuron (Figure 4C).


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)

Basic electrical activity in the model and biological CGCs. (A) Spontaneous tonic firing in the fitted model and the biological neuron (Data). In the absence of external or synaptic input, both fire at approximately 0.7 Hz. Dashed rectangle indicates the overlapping real and simulated spike, respectively, shown on an expanded voltage and time scale in (B). (B) Shape of the action potential in the model and biological CGCs. In both the model and biological neuron, the shape of the action potential is very similar, with the duration being approximately 17 ms (measured at −20 mV) and amplitude being approximately 115 mV. The arrow indicates the characteristic “shoulder” of the action potential during its repolarisation phase. (C) Current-frequency response in the model and the biological neuron. In both, externally injected currents in the range 0–2 nA induce spikes at frequencies up to approximately 15 Hz. To aid clarity, the frequency data shown for the biological neuron come from a single experiment where the same CGC was tested with increasing amounts of current injected into the soma through one electrode while recording spike activity through a second electrode. The same test was repeated with 4 more CGCs in different preparations. The membrane potential of all five neurons tested this way was set at −80 mV prior to each test and so the frequency responses to the same amount of current showed very little variance between the individual neurons.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: Basic electrical activity in the model and biological CGCs. (A) Spontaneous tonic firing in the fitted model and the biological neuron (Data). In the absence of external or synaptic input, both fire at approximately 0.7 Hz. Dashed rectangle indicates the overlapping real and simulated spike, respectively, shown on an expanded voltage and time scale in (B). (B) Shape of the action potential in the model and biological CGCs. In both the model and biological neuron, the shape of the action potential is very similar, with the duration being approximately 17 ms (measured at −20 mV) and amplitude being approximately 115 mV. The arrow indicates the characteristic “shoulder” of the action potential during its repolarisation phase. (C) Current-frequency response in the model and the biological neuron. In both, externally injected currents in the range 0–2 nA induce spikes at frequencies up to approximately 15 Hz. To aid clarity, the frequency data shown for the biological neuron come from a single experiment where the same CGC was tested with increasing amounts of current injected into the soma through one electrode while recording spike activity through a second electrode. The same test was repeated with 4 more CGCs in different preparations. The membrane potential of all five neurons tested this way was set at −80 mV prior to each test and so the frequency responses to the same amount of current showed very little variance between the individual neurons.
Mentions: An overview of the spike shape and firing activity of the fitted model is given in Figure 4. The model was compared to an intracellular current-clamp recording from axotomized cells, which demonstrated a close agreement in the spontaneous tonic firing activity (Figure 4A), spike shape (Figure 4B) and current-frequency response (Figure 4C) between the model and the biological neuron. In the absence of synaptic or experimentally applied input both the biological and the model CGCs fire at a mean frequency of ∼0.7 Hz (∼42 spikes/min; Figure 4A). Typically, an action potential starts as a gradual depolarization of the cell membrane that becomes very rapid after a threshold (∼−50 mV) is crossed (Figure 4B). The spike reaches a peak of approximately +40 mV, which is followed by a repolarization phase with a pronounced “shoulder” (indicated by an arrow in Figure 4B). At its most hyperpolarized state, immediately after the spike, the membrane potential reached a value of about −75 mV, before returning gradually to its baseline value (∼−60 mV). The spike had a total duration of ∼17 ms (measured at −20 mV). Furthermore, when injected with constant currents of increasing amplitude, the model responded with an increase in its firing frequency, which was in close agreement with the response of the biological neuron (Figure 4C).

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