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Variability in State-Dependent Plasticity of Intrinsic Properties during Cell-Autonomous Self-Regulation of Calcium Homeostasis in Hippocampal Model Neurons(1,2,3).

Srikanth S, Narayanan R - eNeuro (2015)

Bottom Line: Although calcium homeostasis emerged efficaciously across all models in the population, disparate changes in ionic conductances that mediated this emergence resulted in variable plasticity to several intrinsic properties, also manifesting as significant differences in firing responses across models.We found that the conductance values, intrinsic properties, and firing response of neurons exhibited differential robustness to an intervening switch in the type of afferent activity.These results unveil critical dissociations between different forms of homeostasis, and call for a systematic evaluation of the impact of state-dependent switches in afferent activity on neuronal intrinsic properties during neural coding and homeostasis.

View Article: PubMed Central - HTML - PubMed

Affiliation: Cellular Neurophysiology Laboratory, Molecular Biophysics Unit, Indian Institute of Science , Bangalore 560 012, India ; Undergraduate program, Indian Institute of Science , Bangalore 560 012, India.

ABSTRACT
How do neurons reconcile the maintenance of calcium homeostasis with perpetual switches in patterns of afferent activity? Here, we assessed state-dependent evolution of calcium homeostasis in a population of hippocampal pyramidal neuron models, through an adaptation of a recent study on stomatogastric ganglion neurons. Calcium homeostasis was set to emerge through cell-autonomous updates to 12 ionic conductances, responding to different types of synaptically driven afferent activity. We first assessed the impact of theta-frequency inputs on the evolution of ionic conductances toward maintenance of calcium homeostasis. Although calcium homeostasis emerged efficaciously across all models in the population, disparate changes in ionic conductances that mediated this emergence resulted in variable plasticity to several intrinsic properties, also manifesting as significant differences in firing responses across models. Assessing the sensitivity of this form of plasticity, we noted that intrinsic neuronal properties and the firing response were sensitive to the target calcium concentration and to the strength and frequency of afferent activity. Next, we studied the evolution of calcium homeostasis when afferent activity was switched, in different temporal sequences, between two behaviorally distinct types of activity: theta-frequency inputs and sharp-wave ripples riding on largely silent periods. We found that the conductance values, intrinsic properties, and firing response of neurons exhibited differential robustness to an intervening switch in the type of afferent activity. These results unveil critical dissociations between different forms of homeostasis, and call for a systematic evaluation of the impact of state-dependent switches in afferent activity on neuronal intrinsic properties during neural coding and homeostasis.

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The frequency of afferent inputs critically regulated changes in intrinsic response properties during cell-autonomous self-regulation of calcium homeostasis. A, The steady state voltage response for 4 different sinusoidal frequencies (delta, 1 Hz, black; theta, 8 Hz, red; slow gamma, 40 Hz, green; fast gamma, 100 Hz, blue). B–H, Histograms of the steady state measurement values (f250, B; VAP, C; Rin, D; /Z/max, E; fR, F; Q, G; ΦL, H) for the 78 neurons for different sinusoidal frequencies appropriately color-coded. The dashed lines in B–H represent the lower and upper bounds for the corresponding measurement (in that order) in the GSA model validation procedure (Table 2).
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Figure 6: The frequency of afferent inputs critically regulated changes in intrinsic response properties during cell-autonomous self-regulation of calcium homeostasis. A, The steady state voltage response for 4 different sinusoidal frequencies (delta, 1 Hz, black; theta, 8 Hz, red; slow gamma, 40 Hz, green; fast gamma, 100 Hz, blue). B–H, Histograms of the steady state measurement values (f250, B; VAP, C; Rin, D; /Z/max, E; fR, F; Q, G; ΦL, H) for the 78 neurons for different sinusoidal frequencies appropriately color-coded. The dashed lines in B–H represent the lower and upper bounds for the corresponding measurement (in that order) in the GSA model validation procedure (Table 2).

Mentions: Finally, to understand the impact of afferent activity beyond the theta-frequency range on the evolution of calcium homeostasis and intrinsic properties, we picked samples from different frequency bands (delta: 1 Hz, theta: 8 Hz, slow gamma: 40 Hz, and fast gamma: 100 Hz) and repeated our simulations (until steady-state was achieved) with these afferent input frequencies. Neuronal response reflected theta-frequency band-pass structure of hippocampal pyramidal neurons, eliciting maximal firing response at the theta range with reduced response with little or no firing at other frequency bands (Fig. 6A). Although the measurements at steady state of calcium-dependent evolution did exhibit significant variability across the 78 models, their values did not have any specific dependence on the frequency of the input (Fig. 6B–H). For all further analyses, the default input frequency was 8 Hz to take into account the hippocampal theta rhythms, as mentioned above. Together, although neuronal firing pattern was heavily dependent on target calcium values and the strength/frequency of afferent inputs, intrinsic properties measured across all parametric combinations exhibited significant variability in the plasticity consequent to calcium-dependent evolution of conductances.


Variability in State-Dependent Plasticity of Intrinsic Properties during Cell-Autonomous Self-Regulation of Calcium Homeostasis in Hippocampal Model Neurons(1,2,3).

Srikanth S, Narayanan R - eNeuro (2015)

The frequency of afferent inputs critically regulated changes in intrinsic response properties during cell-autonomous self-regulation of calcium homeostasis. A, The steady state voltage response for 4 different sinusoidal frequencies (delta, 1 Hz, black; theta, 8 Hz, red; slow gamma, 40 Hz, green; fast gamma, 100 Hz, blue). B–H, Histograms of the steady state measurement values (f250, B; VAP, C; Rin, D; /Z/max, E; fR, F; Q, G; ΦL, H) for the 78 neurons for different sinusoidal frequencies appropriately color-coded. The dashed lines in B–H represent the lower and upper bounds for the corresponding measurement (in that order) in the GSA model validation procedure (Table 2).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4596012&req=5

Figure 6: The frequency of afferent inputs critically regulated changes in intrinsic response properties during cell-autonomous self-regulation of calcium homeostasis. A, The steady state voltage response for 4 different sinusoidal frequencies (delta, 1 Hz, black; theta, 8 Hz, red; slow gamma, 40 Hz, green; fast gamma, 100 Hz, blue). B–H, Histograms of the steady state measurement values (f250, B; VAP, C; Rin, D; /Z/max, E; fR, F; Q, G; ΦL, H) for the 78 neurons for different sinusoidal frequencies appropriately color-coded. The dashed lines in B–H represent the lower and upper bounds for the corresponding measurement (in that order) in the GSA model validation procedure (Table 2).
Mentions: Finally, to understand the impact of afferent activity beyond the theta-frequency range on the evolution of calcium homeostasis and intrinsic properties, we picked samples from different frequency bands (delta: 1 Hz, theta: 8 Hz, slow gamma: 40 Hz, and fast gamma: 100 Hz) and repeated our simulations (until steady-state was achieved) with these afferent input frequencies. Neuronal response reflected theta-frequency band-pass structure of hippocampal pyramidal neurons, eliciting maximal firing response at the theta range with reduced response with little or no firing at other frequency bands (Fig. 6A). Although the measurements at steady state of calcium-dependent evolution did exhibit significant variability across the 78 models, their values did not have any specific dependence on the frequency of the input (Fig. 6B–H). For all further analyses, the default input frequency was 8 Hz to take into account the hippocampal theta rhythms, as mentioned above. Together, although neuronal firing pattern was heavily dependent on target calcium values and the strength/frequency of afferent inputs, intrinsic properties measured across all parametric combinations exhibited significant variability in the plasticity consequent to calcium-dependent evolution of conductances.

Bottom Line: Although calcium homeostasis emerged efficaciously across all models in the population, disparate changes in ionic conductances that mediated this emergence resulted in variable plasticity to several intrinsic properties, also manifesting as significant differences in firing responses across models.We found that the conductance values, intrinsic properties, and firing response of neurons exhibited differential robustness to an intervening switch in the type of afferent activity.These results unveil critical dissociations between different forms of homeostasis, and call for a systematic evaluation of the impact of state-dependent switches in afferent activity on neuronal intrinsic properties during neural coding and homeostasis.

View Article: PubMed Central - HTML - PubMed

Affiliation: Cellular Neurophysiology Laboratory, Molecular Biophysics Unit, Indian Institute of Science , Bangalore 560 012, India ; Undergraduate program, Indian Institute of Science , Bangalore 560 012, India.

ABSTRACT
How do neurons reconcile the maintenance of calcium homeostasis with perpetual switches in patterns of afferent activity? Here, we assessed state-dependent evolution of calcium homeostasis in a population of hippocampal pyramidal neuron models, through an adaptation of a recent study on stomatogastric ganglion neurons. Calcium homeostasis was set to emerge through cell-autonomous updates to 12 ionic conductances, responding to different types of synaptically driven afferent activity. We first assessed the impact of theta-frequency inputs on the evolution of ionic conductances toward maintenance of calcium homeostasis. Although calcium homeostasis emerged efficaciously across all models in the population, disparate changes in ionic conductances that mediated this emergence resulted in variable plasticity to several intrinsic properties, also manifesting as significant differences in firing responses across models. Assessing the sensitivity of this form of plasticity, we noted that intrinsic neuronal properties and the firing response were sensitive to the target calcium concentration and to the strength and frequency of afferent activity. Next, we studied the evolution of calcium homeostasis when afferent activity was switched, in different temporal sequences, between two behaviorally distinct types of activity: theta-frequency inputs and sharp-wave ripples riding on largely silent periods. We found that the conductance values, intrinsic properties, and firing response of neurons exhibited differential robustness to an intervening switch in the type of afferent activity. These results unveil critical dissociations between different forms of homeostasis, and call for a systematic evaluation of the impact of state-dependent switches in afferent activity on neuronal intrinsic properties during neural coding and homeostasis.

No MeSH data available.


Related in: MedlinePlus