Realistic modeling of mesoscopic ephaptic coupling in the human brain.
Several decades of research suggest that weak electric fields may influence neural processing, including those induced by neuronal activity and proposed as a substrate for a potential new cellular communication system, i.e., ephaptic transmission. Here we aim to model mesoscopic ephaptic activity in...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2020-06-01
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| Series: | PLoS Computational Biology |
| Online Access: | https://doi.org/10.1371/journal.pcbi.1007923 |
| _version_ | 1818918560934658048 |
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| author | Giulio Ruffini Ricardo Salvador Ehsan Tadayon Roser Sanchez-Todo Alvaro Pascual-Leone Emiliano Santarnecchi |
| author_facet | Giulio Ruffini Ricardo Salvador Ehsan Tadayon Roser Sanchez-Todo Alvaro Pascual-Leone Emiliano Santarnecchi |
| author_sort | Giulio Ruffini |
| collection | DOAJ |
| description | Several decades of research suggest that weak electric fields may influence neural processing, including those induced by neuronal activity and proposed as a substrate for a potential new cellular communication system, i.e., ephaptic transmission. Here we aim to model mesoscopic ephaptic activity in the human brain and explore its trajectory during aging by characterizing the electric field generated by cortical dipoles using realistic finite element modeling. Extrapolating from electrophysiological measurements, we first observe that modeled endogenous field magnitudes are comparable to those in measurements of weak but functionally relevant self-generated fields and to those produced by noninvasive transcranial brain stimulation, and therefore possibly able to modulate neuronal activity. Then, to evaluate the role of these fields in the human cortex in large MRI databases, we adapt an interaction approximation that considers the relative orientation of neuron and field to estimate the membrane potential perturbation in pyramidal cells. We use this approximation to define a simplified metric (EMOD1) that weights dipole coupling as a function of distance and relative orientation between emitter and receiver and evaluate it in a sample of 401 realistic human brain models from healthy subjects aged 16-83. Results reveal that ephaptic coupling, in the simplified mesoscopic modeling approach used here, significantly decreases with age, with higher involvement of sensorimotor regions and medial brain structures. This study suggests that by providing the means for fast and direct interaction between neurons, ephaptic modulation may contribute to the complexity of human function for cognition and behavior, and its modification across the lifespan and in response to pathology. |
| first_indexed | 2024-12-20T00:51:55Z |
| format | Article |
| id | doaj.art-c2318a770565439a86cb6a828f4952be |
| institution | Directory Open Access Journal |
| issn | 1553-734X 1553-7358 |
| language | English |
| last_indexed | 2024-12-20T00:51:55Z |
| publishDate | 2020-06-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Computational Biology |
| spelling | doaj.art-c2318a770565439a86cb6a828f4952be2022-12-21T19:59:13ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582020-06-01166e100792310.1371/journal.pcbi.1007923Realistic modeling of mesoscopic ephaptic coupling in the human brain.Giulio RuffiniRicardo SalvadorEhsan TadayonRoser Sanchez-TodoAlvaro Pascual-LeoneEmiliano SantarnecchiSeveral decades of research suggest that weak electric fields may influence neural processing, including those induced by neuronal activity and proposed as a substrate for a potential new cellular communication system, i.e., ephaptic transmission. Here we aim to model mesoscopic ephaptic activity in the human brain and explore its trajectory during aging by characterizing the electric field generated by cortical dipoles using realistic finite element modeling. Extrapolating from electrophysiological measurements, we first observe that modeled endogenous field magnitudes are comparable to those in measurements of weak but functionally relevant self-generated fields and to those produced by noninvasive transcranial brain stimulation, and therefore possibly able to modulate neuronal activity. Then, to evaluate the role of these fields in the human cortex in large MRI databases, we adapt an interaction approximation that considers the relative orientation of neuron and field to estimate the membrane potential perturbation in pyramidal cells. We use this approximation to define a simplified metric (EMOD1) that weights dipole coupling as a function of distance and relative orientation between emitter and receiver and evaluate it in a sample of 401 realistic human brain models from healthy subjects aged 16-83. Results reveal that ephaptic coupling, in the simplified mesoscopic modeling approach used here, significantly decreases with age, with higher involvement of sensorimotor regions and medial brain structures. This study suggests that by providing the means for fast and direct interaction between neurons, ephaptic modulation may contribute to the complexity of human function for cognition and behavior, and its modification across the lifespan and in response to pathology.https://doi.org/10.1371/journal.pcbi.1007923 |
| spellingShingle | Giulio Ruffini Ricardo Salvador Ehsan Tadayon Roser Sanchez-Todo Alvaro Pascual-Leone Emiliano Santarnecchi Realistic modeling of mesoscopic ephaptic coupling in the human brain. PLoS Computational Biology |
| title | Realistic modeling of mesoscopic ephaptic coupling in the human brain. |
| title_full | Realistic modeling of mesoscopic ephaptic coupling in the human brain. |
| title_fullStr | Realistic modeling of mesoscopic ephaptic coupling in the human brain. |
| title_full_unstemmed | Realistic modeling of mesoscopic ephaptic coupling in the human brain. |
| title_short | Realistic modeling of mesoscopic ephaptic coupling in the human brain. |
| title_sort | realistic modeling of mesoscopic ephaptic coupling in the human brain |
| url | https://doi.org/10.1371/journal.pcbi.1007923 |
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