Abstract
Neurons often receive massive concurrent bombardment of synaptic inhibition and excitation during functional network activity. This increases membrane conductance and causes fluctuations in membrane potential (Vm) and spike timing. The conductance increase is commonly attributed to synaptic conductance, but also includes the intrinsic conductances recruited during network activity. These two sources of conductance have contrasting dynamic properties at sub-threshold membrane potentials. Synaptic transmitter gated conductance changes abruptly and briefly with each presynaptic action potential. If the spikes arrive at random times the changes in synaptic conductance are therefore stochastic and rapid during intense network activity. In comparison, sub-threshold intrinsic conductances vary smoothly in time. In the present study this discrepancy is investigated using two conductance-based models: a (1) compartment model and a (2) compartment with realistic slow intrinsic conductances. We examine the effects of varying the relative contributions of non-fluctuating intrinsic conductance with fluctuating concurrent inhibitory and excitatory synaptic conductance. For given levels of correlation in the synaptic input we find that the magnitude of the membrane fluctuations uniquely determines the relative contribution of synaptic and intrinsic conductance. We also quantify how Vm-fluctuations vary with synaptic correlations for fixed ratios of synaptic and intrinsic conductance. Interestingly, the levels of Vm -fluctuations and conductance observed experimentally during functional network activity leave little room for intrinsic conductance to contribute. Even without intrinsic conductances the variance in Vm -fluctuations can only be explained by a high degree of correlated firing among presynaptic neurons.
Highlights
Changes in membrane potential in active neurons are caused by synaptic current generators activated by neurotransmitters and by voltage-activated intrinsic current generators
The relative contribution of synaptic and intrinsic current generators determines whether individual neurons during network activity, at one extreme, are weakly coupled autonomous oscillators (Toledo-Rodriguez et al, 2005; Grillner, 2006; Smith and Perrier, 2006) or in the other extreme driven by strong synaptic input
We explore the effect of synaptic correlations on the Vm-fluctuations the membrane potential (Vm)-fluctuations at different levels of intrinsic conductance and compare with data from turtle motoneurons during functional network activity
Summary
Changes in membrane potential in active neurons are caused by synaptic current generators activated by neurotransmitters and by voltage-activated intrinsic current generators. The relative contribution of synaptic and intrinsic current generators determines whether individual neurons during network activity, at one extreme, are weakly coupled autonomous oscillators (Toledo-Rodriguez et al, 2005; Grillner, 2006; Smith and Perrier, 2006) or in the other extreme driven by strong synaptic input. For neurons in active networks the synaptic input can be so intense that the mean synaptic conductance is comparable to or larger than the input conductance of the neuron in absence of synaptic input In this condition, the synaptic input itself severely distorts the electrotonic structure (Bernander et al, 1991; Korogod et al, 2000) and reduces the integration time up to ten-fold (Rapp et al, 1992; Koch et al, 1996; Berg et al, 2008). Whereas the intrinsic conductances may not always contribute detectably to spike patterns during network activity (Berg et al, 2008) they will certainly contribute to the total conductance and affect the synaptically induced Vm-fluctuations
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