Abstract
Synaptic inputs to neurons are processed in a frequency-dependent manner, with either low-pass or resonant response characteristics. These types of filtering play a key role in the frequency-specific information flow in neuronal networks. While the generation of resonance by specific ionic conductances is well investigated, less attention has been paid to the spatial distribution of the resonance-generating conductances across a neuron. In pyramidal neurons – one of the major excitatory cell-types in the mammalian brain – a steep gradient of resonance-generating h-conductances with a 60-fold increase towards distal dendrites has been demonstrated experimentally. Because the dendritic trees of these cells are large, spatial compartmentalization of resonant properties can be expected. Here, we use mathematical descriptions of spatially extended neurons to investigate the consequences of such a distal, dendritic localization of h-conductances for signal processing. While neurons with short dendrites do not exhibit a pronounced compartmentalization of resonance, i.e. the filter properties of dendrites and soma are similar, we find that neurons with longer dendrites ( space constant) can show distinct filtering of dendritic and somatic inputs due to electrotonic segregation. Moreover, we show that for such neurons, experimental classification as resonant versus nonresonant can be misleading when based on somatic recordings, because for these morphologies a dendritic resonance could easily be undetectable when using somatic input. Nevertheless, noise-driven membrane-potential oscillations caused by dendritic resonance can propagate to the soma where they can be recorded, hence contrasting with the low-pass filtering at the soma. We conclude that non-uniform distributions of active conductances can underlie differential filtering of synaptic input in neurons with spatially extended dendrites, like pyramidal neurons, bearing relevance for the localization-dependent targeting of synaptic input pathways to these cells.
Highlights
IntroductionIn the subthreshold membrane potential range such filtering can have low-pass or resonant characteristics – i.e., a cell either shows the largest amplitude responses to low input frequencies, or it responds maximally to input in a particular frequency band (see [1] and references therein)
Responses to synaptic input are shaped by a neuron’s membrane properties
Using an analytically tractable neuron model, we show that a predominant expression of resonance-generating channels in distal dendrites can be responsible for a strong dendritic resonance that shapes the somatic response to dendritic input, without affecting the response to somatic input
Summary
In the subthreshold membrane potential range such filtering can have low-pass or resonant characteristics – i.e., a cell either shows the largest amplitude responses to low input frequencies, or it responds maximally to input in a particular frequency band (see [1] and references therein). Such resonant properties of neuronal membranes are thought to play an essential role in the generation of brain rhythms associated with various behavioral and perceptual states [2]. In the hippocampus it is thought to play a central role in the generation of local-field theta oscillations (4–12 Hz range; [10,11])
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