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.
Highlights
Afferent activity patterns to hippocampal pyramidal neurons manifest well established distinctions that reflect the behavioral state of the animal (Anderson et al, 2007)
As the 78 models were valid models for hippocampal pyramidal neuron physiology, we used these for our analysis on state-dependence of intrinsic properties in regulating calcium homeostasis
The key conclusion of this study is that neuronal ionic conductances and intrinsic properties could undergo significant plasticity in the process of maintaining calcium homeostasis through a regime of behavioral state-dependent eNeuro.sfn.org changes in afferent activity
Summary
Afferent activity patterns to hippocampal pyramidal neurons manifest well established distinctions that reflect the behavioral state of the animal (Anderson et al, 2007). How do neurons reconcile the maintenance of calcium homeostasis with perpetual state-dependent switches in afferent activity patterns? Existing literature has explored switches in afferent activity from the perspective of firing rate modulation, synaptic normalization and plasticity, especially during sleep—(Tononi and Cirelli, 2006; Chauvette et al, 2012; Grosmark et al, 2012; Barnes and Wilson, 2014)—and from the perspective of how dendritic nonlinearities endow hippocampal neurons with the ability to adapt to changes in afferent activity (Gasparini and Magee, 2006). The question of how neurons implementing calcium homeostasis through changes in ionic conductances react to state-dependent switches in afferent activity has not been addressed. Under a selfregulating, cell-autonomous schema for calcium homeostasis, are there changes in neuronal firing, conductance values, and intrinsic properties that are consequent to switches in afferent activity?
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