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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.


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Electrophysiological effects of conditioning in the biological and model CGCs. (A) Effects of conditioning in the biological CGCs. Recordings from CGCs in animals trained using a single-trial classical appetitive conditioning protocol do not show any significant differences in the frequency of the spontaneous firing activity of the cell, when compared to recordings from cells in non-conditioned animals (Example traces shown in Ai, also see Kemenes et al., 2006). However, the membrane potential of CGCs from conditioned animals (measured midway between consecutive spikes and averaged for the whole trace shown) was depolarized, when compared to CGC recordings from non-conditioned control animals (section of Ai in dashed rectangle shown in Aii). (B) Effects of conditioning in the model CGCs. Conditioning in the model was simulated by a balanced increase in gNaP and gD, the maximal conductances of the persistent sodium and delayed rectifier potassium currents respectively. For example, when gNaP was increased by 50%, increasing gD by approximately the same proportion stabilized the spontaneous firing frequency in the model cell at the value it had before increasing the two conductances, i.e., ∼0.7 Hz (Bi). A closer inspection of the model CGCs revealed that the membrane potential after the increase was depolarized by 3.1 mV (section of Bi in dashed rectangle shown in Bii). This increase is comparable to the values measured from the biological cells after conditioning (example in Aii).
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Figure 6: Electrophysiological effects of conditioning in the biological and model CGCs. (A) Effects of conditioning in the biological CGCs. Recordings from CGCs in animals trained using a single-trial classical appetitive conditioning protocol do not show any significant differences in the frequency of the spontaneous firing activity of the cell, when compared to recordings from cells in non-conditioned animals (Example traces shown in Ai, also see Kemenes et al., 2006). However, the membrane potential of CGCs from conditioned animals (measured midway between consecutive spikes and averaged for the whole trace shown) was depolarized, when compared to CGC recordings from non-conditioned control animals (section of Ai in dashed rectangle shown in Aii). (B) Effects of conditioning in the model CGCs. Conditioning in the model was simulated by a balanced increase in gNaP and gD, the maximal conductances of the persistent sodium and delayed rectifier potassium currents respectively. For example, when gNaP was increased by 50%, increasing gD by approximately the same proportion stabilized the spontaneous firing frequency in the model cell at the value it had before increasing the two conductances, i.e., ∼0.7 Hz (Bi). A closer inspection of the model CGCs revealed that the membrane potential after the increase was depolarized by 3.1 mV (section of Bi in dashed rectangle shown in Bii). This increase is comparable to the values measured from the biological cells after conditioning (example in Aii).

Mentions: During appetitive classical conditioning using a single-trial protocol (Alexander et al., 1984), the resting membrane potential of the CGC soma in trained animals is significantly depolarized at 24 h after conditioning (mean membrane potential increase, 2.5 mV; merged data from left and right CGCs), when compared to measurements taken from unpaired or naïve controls (Figures 6Ai,ii; see Nikitin et al., 2008 for more details). However, no significant differences were found in the firing frequency of spontaneously generated CGC spikes between trained and control animals (Figure 6Ai). Other spike parameters, such as duration, amplitude and after-hyperpolarization also remained unchanged after conditioning (Kemenes et al., 2006; Nikitin et al., 2008).


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)

Electrophysiological effects of conditioning in the biological and model CGCs. (A) Effects of conditioning in the biological CGCs. Recordings from CGCs in animals trained using a single-trial classical appetitive conditioning protocol do not show any significant differences in the frequency of the spontaneous firing activity of the cell, when compared to recordings from cells in non-conditioned animals (Example traces shown in Ai, also see Kemenes et al., 2006). However, the membrane potential of CGCs from conditioned animals (measured midway between consecutive spikes and averaged for the whole trace shown) was depolarized, when compared to CGC recordings from non-conditioned control animals (section of Ai in dashed rectangle shown in Aii). (B) Effects of conditioning in the model CGCs. Conditioning in the model was simulated by a balanced increase in gNaP and gD, the maximal conductances of the persistent sodium and delayed rectifier potassium currents respectively. For example, when gNaP was increased by 50%, increasing gD by approximately the same proportion stabilized the spontaneous firing frequency in the model cell at the value it had before increasing the two conductances, i.e., ∼0.7 Hz (Bi). A closer inspection of the model CGCs revealed that the membrane potential after the increase was depolarized by 3.1 mV (section of Bi in dashed rectangle shown in Bii). This increase is comparable to the values measured from the biological cells after conditioning (example in Aii).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 6: Electrophysiological effects of conditioning in the biological and model CGCs. (A) Effects of conditioning in the biological CGCs. Recordings from CGCs in animals trained using a single-trial classical appetitive conditioning protocol do not show any significant differences in the frequency of the spontaneous firing activity of the cell, when compared to recordings from cells in non-conditioned animals (Example traces shown in Ai, also see Kemenes et al., 2006). However, the membrane potential of CGCs from conditioned animals (measured midway between consecutive spikes and averaged for the whole trace shown) was depolarized, when compared to CGC recordings from non-conditioned control animals (section of Ai in dashed rectangle shown in Aii). (B) Effects of conditioning in the model CGCs. Conditioning in the model was simulated by a balanced increase in gNaP and gD, the maximal conductances of the persistent sodium and delayed rectifier potassium currents respectively. For example, when gNaP was increased by 50%, increasing gD by approximately the same proportion stabilized the spontaneous firing frequency in the model cell at the value it had before increasing the two conductances, i.e., ∼0.7 Hz (Bi). A closer inspection of the model CGCs revealed that the membrane potential after the increase was depolarized by 3.1 mV (section of Bi in dashed rectangle shown in Bii). This increase is comparable to the values measured from the biological cells after conditioning (example in Aii).
Mentions: During appetitive classical conditioning using a single-trial protocol (Alexander et al., 1984), the resting membrane potential of the CGC soma in trained animals is significantly depolarized at 24 h after conditioning (mean membrane potential increase, 2.5 mV; merged data from left and right CGCs), when compared to measurements taken from unpaired or naïve controls (Figures 6Ai,ii; see Nikitin et al., 2008 for more details). However, no significant differences were found in the firing frequency of spontaneously generated CGC spikes between trained and control animals (Figure 6Ai). Other spike parameters, such as duration, amplitude and after-hyperpolarization also remained unchanged after conditioning (Kemenes et al., 2006; Nikitin et al., 2008).

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