Solitonic conduction of electrotonic signals in neuronal branchlets with polarized microstructure

Poznański, Roman R.; Cacha, L. A.; Alwesabi, Yaseen; Ali, J.; Bahadoran, Mahdi; Yupapin, P.; Yunus, Jasmy

doi:10.1038/s41598-017-01849-3

Cited by 28 publications

(26 citation statements)

References 55 publications

(78 reference statements)

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“…The model presented herein constitutes a first attempt at identifying solitons as electrotonic signals propagating in neuronal branchlets with microstructure containing mitochondria. The model differs from that of Poznanski and colleagues [ 22 ] where solitonic conduction of electrotonic potentials was due to charged proteins without mitochondrial membranes.…”

Section: Discussionmentioning

confidence: 66%

“…However, the model of Poznanski [ 21 ] did not take into account polarization current due to the dispersion of bound charge held by microstructure. An instance where charge dispersal is not ignored, the voltage created by charge ‘soakage’ due to intracellular capacitive effects has been modeled through voltage-dependent capacitors [ 22 , 23 ].…”

Section: Introductionmentioning

confidence: 99%

“…This is done by treating the microstructure as a homogenized core-conductor where intracellular capacitive effects arise due to polarization effects of bound charge [ 23 ]. The microstructure included polarization-induced capacitive current of charged proteins without endoplasmic membranes [ 22 ]. An electrical model of electrolyte solution with endoplasmic membranes in the cytoplasm as a subcellular reticulum cable encased within a core-conductor developed by Shemer et al [ 27 ] did not explicitly take into consideration intracellular capacitive effects due to polarized microstructure.…”

Section: Introductionmentioning

confidence: 99%

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Induced mitochondrial membrane potential for modeling solitonic conduction of electrotonic signals

Poznański¹,

Cacha²,

Ali³

et al. 2017

PLoS ONE

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A cable model that includes polarization-induced capacitive current is derived for modeling the solitonic conduction of electrotonic potentials in neuronal branchlets with microstructure containing endoplasmic membranes. A solution of the nonlinear cable equation modified for fissured intracellular medium with a source term representing charge ‘soakage’ is used to show how intracellular capacitive effects of bound electrical charges within mitochondrial membranes can influence electrotonic signals expressed as solitary waves. The elastic collision resulting from a head-on collision of two solitary waves results in localized and non-dispersing electrical solitons created by the nonlinearity of the source term. It has been shown that solitons in neurons with mitochondrial membrane and quasi-electrostatic interactions of charges held by the microstructure (i.e., charge ‘soakage’) have a slower velocity of propagation compared with solitons in neurons with microstructure, but without endoplasmic membranes. When the equilibrium potential is a small deviation from rest, the nonohmic conductance acts as a leaky channel and the solitons are small compared when the equilibrium potential is large and the outer mitochondrial membrane acts as an amplifier, boosting the amplitude of the endogenously generated solitons. These findings demonstrate a functional role of quasi-electrostatic interactions of bound electrical charges held by microstructure for sustaining solitons with robust self-regulation in their amplitude through changes in the mitochondrial membrane equilibrium potential. The implication of our results indicate that a phenomenological description of ionic current can be successfully modeled with displacement current in Maxwell’s equations as a conduction process involving quasi-electrostatic interactions without the inclusion of diffusive current. This is the first study in which solitonic conduction of electrotonic potentials are generated by polarization-induced capacitive current in microstructure and nonohmic mitochondrial membrane current.

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Section: Discussionmentioning

confidence: 66%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Induced mitochondrial membrane potential for modeling solitonic conduction of electrotonic signals

Poznański¹,

Cacha²,

Ali³

et al. 2017

PLoS ONE

Self Cite

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“…Such non-linear filtering operations could be biologically implemented by active dendritic membrane processes that were shown to exist in VS cells 40 and by nonlinear voltage-calcium relationship 41 . In addition, two recent elegant studies have shown that nonlinear phenomena are expected in thin dendrites at the sub-micron regime (<0.5 μm) 42 , 43 . The average diameter of the branchlets in our dataset is 1.02μm (Table 1 ).…”

Section: Resultsmentioning

confidence: 99%

Non-uniform weighting of local motion inputs underlies dendritic computation in the fly visual system

Dan

Hopp

Borst

et al. 2018

Sci Rep

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The fly visual system offers a unique opportunity to explore computations performed by single neurons. Two previous studies characterized, in vivo, the receptive field (RF) of the vertical system (VS) cells of the blowfly (calliphora vicina), both intracellularly in the axon, and, independently using Ca2+ imaging, in hundreds of distal dendritic branchlets. We integrated this information into detailed passive cable and compartmental models of 3D reconstructed VS cells. Within a given VS cell type, the transfer resistance (TR) from different branchlets to the axon differs substantially, suggesting that they contribute unequally to the shaping of the axonal RF. Weighting the local RFs of all dendritic branchlets by their respective TR yielded a faithful reproduction of the axonal RF. The model also predicted that the various dendritic branchlets are electrically decoupled from each other, thus acting as independent local functional subunits. The study suggests that single neurons in the fly visual system filter dendritic noise and compute the weighted average of their inputs.

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“…In general, excitation waves from propagating graded potentials to action-potential, show an entire range of interactions; from superposition to supra-linear, to sublinear summation (57). Upon interaction, these waves can emerge unaffected (48,49) to being annihilated (58,59). Shock physics as developed for lipid monolayer now provides a general mechanism for such interactions at interfaces.…”

Section: Discussionmentioning

confidence: 99%

Shock and Detonation Waves at an Interface and the Collision of Action Potentials

Shrivastava

2020

Preprint

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Action potentials in neurons are known to annihilate each other upon collision, while there are cases where they might penetrate each other. Compression waves that travel within the plasma membrane of a neuron have previously been proposed as a thermodynamic basis for the propagation of action potentials. In this context, it was recently shown that two dimensional compressive shock waves in the model system of lipid monolayers can nearly annihilate each other upon head on collision when excited close to a phase transition. However, weaker shock waves showed penetration. In general, once the approximation of small perturbation is not valid, compression waves do not interact linearly anymore. While experiments in lipid monolayers demonstrated this principle, a mechanism remained unclear. In this article, we summarise the fundamentals of shock physics as applied to an interface and how it previously explained the observation of threshold and saturation of shockwaves in the lipid monolayer (all or none). While the theory has the same fundamental premise as the soliton model, i.e. the conservation laws and thermodynamics, we elaborate on how the two approaches make different predictions with regards to collisions and the detailed structure of the wave-front. As a case study and a new result, we show that previously unexplained annihilation of shock waves in the lipid monolayer is a direct consequence of the nature of state changes, i.e. jump conditions, within these shockwaves, and elaborate on the consequence of these results for the general understanding of the excitation waves in a thermo-fluids framework.

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Solitonic conduction of electrotonic signals in neuronal branchlets with polarized microstructure

Cited by 28 publications

References 55 publications

Induced mitochondrial membrane potential for modeling solitonic conduction of electrotonic signals

Induced mitochondrial membrane potential for modeling solitonic conduction of electrotonic signals

Non-uniform weighting of local motion inputs underlies dendritic computation in the fly visual system

Shock and Detonation Waves at an Interface and the Collision of Action Potentials

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