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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.

No MeSH data available.


Related in: MedlinePlus

The strength of afferent theta inputs critically regulated changes in intrinsic response properties during cell-autonomous self-regulation of calcium homeostasis. A, The steady state voltage response after theta-dependent evolution, for four different amplitudes of the 8 Hz input sinusoid (peak-to-peak value of sinusoidal permeability: black, 100 nm/s; red, 200 nm/s; green, 300 nm/s; blue, 400 nm/s). Note that at high values of sinusoidal amplitudes (e.g., 400 nm/s) the deflections are large along the hyperpolarized direction because of the large driving force for AMPA/NMDA receptors that mediate the sinusoidal oscillations. Along the depolarized direction, an action potential was elicited once the membrane potential crossed threshold, and the amplitude of the action potential did not cross the sodium reversal potential of +55 mV. 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 valid models, obtained after theta-dependent evolution with different sinusoidal amplitudes. 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 5: The strength of afferent theta inputs critically regulated changes in intrinsic response properties during cell-autonomous self-regulation of calcium homeostasis. A, The steady state voltage response after theta-dependent evolution, for four different amplitudes of the 8 Hz input sinusoid (peak-to-peak value of sinusoidal permeability: black, 100 nm/s; red, 200 nm/s; green, 300 nm/s; blue, 400 nm/s). Note that at high values of sinusoidal amplitudes (e.g., 400 nm/s) the deflections are large along the hyperpolarized direction because of the large driving force for AMPA/NMDA receptors that mediate the sinusoidal oscillations. Along the depolarized direction, an action potential was elicited once the membrane potential crossed threshold, and the amplitude of the action potential did not cross the sodium reversal potential of +55 mV. 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 valid models, obtained after theta-dependent evolution with different sinusoidal amplitudes. 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: We next assessed the impact of afferent activity strength on θ-dependent evolution by altering the peak-to-peak amplitude of the sinusoidal modulation in receptor permeability, with the sinusoidal frequency fixed at 8 Hz (Fig. 5). Whereas the neuron did not fire action potentials for lower strengths of afferent input (Fig. 5A; permeability value P1), at very high values of input permeability neurons entered into depolarization-induced block with average membrane potential around –30 mV (Fig. 5A; permeability value P4). In the mid-range between these two extremes, the number of action potentials fired per cycle increased with increase in afferent input strength. Assessing steady-state values of intrinsic properties after θ-dependent evolution, we noted that variable plasticity in all seven intrinsic measurements was observed across all tested values of input strength, with no qualitative differences observed in the measurement variability with different values of the sinusoidal peak-to-peak amplitude (Fig. 5B–H).


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 strength of afferent theta inputs critically regulated changes in intrinsic response properties during cell-autonomous self-regulation of calcium homeostasis. A, The steady state voltage response after theta-dependent evolution, for four different amplitudes of the 8 Hz input sinusoid (peak-to-peak value of sinusoidal permeability: black, 100 nm/s; red, 200 nm/s; green, 300 nm/s; blue, 400 nm/s). Note that at high values of sinusoidal amplitudes (e.g., 400 nm/s) the deflections are large along the hyperpolarized direction because of the large driving force for AMPA/NMDA receptors that mediate the sinusoidal oscillations. Along the depolarized direction, an action potential was elicited once the membrane potential crossed threshold, and the amplitude of the action potential did not cross the sodium reversal potential of +55 mV. 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 valid models, obtained after theta-dependent evolution with different sinusoidal amplitudes. 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 5: The strength of afferent theta inputs critically regulated changes in intrinsic response properties during cell-autonomous self-regulation of calcium homeostasis. A, The steady state voltage response after theta-dependent evolution, for four different amplitudes of the 8 Hz input sinusoid (peak-to-peak value of sinusoidal permeability: black, 100 nm/s; red, 200 nm/s; green, 300 nm/s; blue, 400 nm/s). Note that at high values of sinusoidal amplitudes (e.g., 400 nm/s) the deflections are large along the hyperpolarized direction because of the large driving force for AMPA/NMDA receptors that mediate the sinusoidal oscillations. Along the depolarized direction, an action potential was elicited once the membrane potential crossed threshold, and the amplitude of the action potential did not cross the sodium reversal potential of +55 mV. 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 valid models, obtained after theta-dependent evolution with different sinusoidal amplitudes. 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: We next assessed the impact of afferent activity strength on θ-dependent evolution by altering the peak-to-peak amplitude of the sinusoidal modulation in receptor permeability, with the sinusoidal frequency fixed at 8 Hz (Fig. 5). Whereas the neuron did not fire action potentials for lower strengths of afferent input (Fig. 5A; permeability value P1), at very high values of input permeability neurons entered into depolarization-induced block with average membrane potential around –30 mV (Fig. 5A; permeability value P4). In the mid-range between these two extremes, the number of action potentials fired per cycle increased with increase in afferent input strength. Assessing steady-state values of intrinsic properties after θ-dependent evolution, we noted that variable plasticity in all seven intrinsic measurements was observed across all tested values of input strength, with no qualitative differences observed in the measurement variability with different values of the sinusoidal peak-to-peak amplitude (Fig. 5B–H).

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