Biophysical Properties of the Cytoskeleton and Its Role in Neuron Function

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Background

Brain function is mediated by both excitatory and inhibitory interactions between neurons that possess their own “intrinsic electrical activity”. In the hippocampus, neuronal spiking synchronization generates theta waves propagation inducing long-term potentiation (LTP). Whilst the molecular mechanisms underlying the generation of electrical oscillations remain to be explored, the intrinsic oscillatory properties of these cells have been associated with both passive and active membrane characteristics including: ionic conductances, such as GABAA and NMDA receptors, dentritic Ca2+ currents and channels. The current paradigm does not include the neuronal cytoskeleton elements.
In both axons and dendrites, microtubules (MTs) form dense parallel arrays known as bundles, which are required for neuronal growth and maintenance of neurites. MTs are formed of highly charged αβ tubulin heterodimeric units that act as biological transistors, amplifying and axially propagating electrical signals. These may exert a functional impact on neuronal spiking capacity.
Brain MT sheets and bundles’ electrical activity was recently described using patch-clamping techniques. The examined MT structures displayed spontaneous electrical activity consistent with self-sustained oscillations in the range of 29-39 Hz, indicating that they also contribute to couple and synchronize ionic conductances in neuronal tissue. Several neuronal structures, such as dendritic spines and growth cones, are also enriched with highly dynamic actin filament networks. These are essential to experience-related plasticity and changes associated with neural stimulation. Morphological changes in actin-rich dendritic spines correlate with LTP in hippocampal tissue slices of behaving animals. However, the capacity of sustaining and propagating electrical signals as ionic waves, makes actin filaments behave like “cables” acting as transmission lines. Interestingly, recent studies indicate an effect of actin polymerization on brain MTs electrical oscillations. The regulatory role of F-actin on the oscillatory activity of brain MT is shown to be mediated by proteins able to bind both actin and tubulin, including MAP2, MAP2c and Tau. Additionally, this role of F-actin is also mediated by electrostatic phenomena on account of its polymerization on charged surfaces. These Actin-MT interactions may be essential for the gating of cytoskeleton-associated ion channels in neural compartments such as dendritic spines.

The aim of this Research Topic is to evaluate the contribution of cytoskeletal structures on the electrical oscillatory activity in the various oscillatory regimes of individual neurons and brain areas. There is the need to shed a new light on the relationship between electrical activity of cytoskeletal components, neuronal electrical activity and higher brain functions.
Potential questions to be addressed include:
1. How do cytoskeletal electrical oscillations influence higher brain functions including memory consolidation?
2. How does the neuronal cytoskeleton participate in the genesis of neural network electrical oscillatory patterns?
3. How are electrical oscillations generated by MT and actin structures (for example isolated MT, bundles, filaments…) and how do they impact the ion channel-based conductance of the neuron?
4. How do cytoskeleton electrical oscillations impact neuronal function or LTP induction, particularly in the hippocampus?

The primary goal of this collection is to receive Original Research studies, however timely Reviews, Hypotheses and Theory manuscripts are also welcome.

Keywords: Microtubules, Actin Filaments, Neurons, Cytoskeleton, Electrical Properties

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