On temporal scale-free non-periodic stimulation and its mechanisms as an infinite improbability drive of the brain’s functional connectogram

Rationalized development of electrical stimulation (ES) therapy is of paramount importance. Not only it will foster new techniques and technologies with increased levels of safety, efficacy, and efficiency, but it will also facilitate the translation from basic research to clinical practice. For suc...

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Main Authors: Vinícius Rosa Cota, Sérgio Augusto Vieira Cançado, Márcio Flávio Dutra Moraes
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-05-01
Series:Frontiers in Neuroinformatics
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fninf.2023.1173597/full
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author Vinícius Rosa Cota
Vinícius Rosa Cota
Sérgio Augusto Vieira Cançado
Márcio Flávio Dutra Moraes
author_facet Vinícius Rosa Cota
Vinícius Rosa Cota
Sérgio Augusto Vieira Cançado
Márcio Flávio Dutra Moraes
author_sort Vinícius Rosa Cota
collection DOAJ
description Rationalized development of electrical stimulation (ES) therapy is of paramount importance. Not only it will foster new techniques and technologies with increased levels of safety, efficacy, and efficiency, but it will also facilitate the translation from basic research to clinical practice. For such endeavor, design of new technologies must dialogue with state-of-the-art neuroscientific knowledge. By its turn, neuroscience is transitioning—a movement started a couple of decades earlier—into adopting a new conceptual framework for brain architecture, in which time and thus temporal patterns plays a central role in the neuronal representation of sampled data from the world. This article discusses how neuroscience has evolved to understand the importance of brain rhythms in the overall functional architecture of the nervous system and, consequently, that neuromodulation research should embrace this new conceptual framework. Based on such support, we revisit the literature on standard (fixed-frequency pulsatile stimuli) and mostly non-standard patterns of ES to put forward our own rationale on how temporally complex stimulation schemes may impact neuromodulation strategies. We then proceed to present a low frequency, on average (thus low energy), scale-free temporally randomized ES pattern for the treatment of experimental epilepsy, devised by our group and termed NPS (Non-periodic Stimulation). The approach has been shown to have robust anticonvulsant effects in different animal models of acute and chronic seizures (displaying dysfunctional hyperexcitable tissue), while also preserving neural function. In our understanding, accumulated mechanistic evidence suggests such a beneficial mechanism of action may be due to the natural-like characteristic of a scale-free temporal pattern that may robustly compete with aberrant epileptiform activity for the recruitment of neural circuits. Delivering temporally patterned or random stimuli within specific phases of the underlying oscillations (i.e., those involved in the communication within and across brain regions) could both potentiate and disrupt the formation of neuronal assemblies with random probability. The usage of infinite improbability drive here is obviously a reference to the “The Hitchhiker’s Guide to the Galaxy” comedy science fiction classic, written by Douglas Adams. The parallel is that dynamically driving brain functional connectogram, through neuromodulation, in a manner that would not favor any specific neuronal assembly and/or circuit, could re-stabilize a system that is transitioning to fall under the control of a single attractor. We conclude by discussing future avenues of investigation and their potentially disruptive impact on neurotechnology, with a particular interest in NPS implications in neural plasticity, motor rehabilitation, and its potential for clinical translation.
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spelling doaj.art-fd156d68ae8b440981343ec67b0475162023-05-24T04:28:36ZengFrontiers Media S.A.Frontiers in Neuroinformatics1662-51962023-05-011710.3389/fninf.2023.11735971173597On temporal scale-free non-periodic stimulation and its mechanisms as an infinite improbability drive of the brain’s functional connectogramVinícius Rosa Cota0Vinícius Rosa Cota1Sérgio Augusto Vieira Cançado2Márcio Flávio Dutra Moraes3Rehab Technologies - INAIL Lab, Istituto Italiano di Tecnologia, Genoa, ItalyLaboratory of Neuroengineering and Neuroscience, Department of Electrical Engineering, Federal University of São João del-Rei, São João del Rei, BrazilNúcleo Avançado de Tratamento das Epilepsias (NATE), Felício Rocho Hospital, Fundação Felice Rosso, Belo Horizonte, BrazilDepartment of Physiology and Biophysics, Núcleo de Neurociências, Federal University of Minas Gerais, Belo Horizonte, BrazilRationalized development of electrical stimulation (ES) therapy is of paramount importance. Not only it will foster new techniques and technologies with increased levels of safety, efficacy, and efficiency, but it will also facilitate the translation from basic research to clinical practice. For such endeavor, design of new technologies must dialogue with state-of-the-art neuroscientific knowledge. By its turn, neuroscience is transitioning—a movement started a couple of decades earlier—into adopting a new conceptual framework for brain architecture, in which time and thus temporal patterns plays a central role in the neuronal representation of sampled data from the world. This article discusses how neuroscience has evolved to understand the importance of brain rhythms in the overall functional architecture of the nervous system and, consequently, that neuromodulation research should embrace this new conceptual framework. Based on such support, we revisit the literature on standard (fixed-frequency pulsatile stimuli) and mostly non-standard patterns of ES to put forward our own rationale on how temporally complex stimulation schemes may impact neuromodulation strategies. We then proceed to present a low frequency, on average (thus low energy), scale-free temporally randomized ES pattern for the treatment of experimental epilepsy, devised by our group and termed NPS (Non-periodic Stimulation). The approach has been shown to have robust anticonvulsant effects in different animal models of acute and chronic seizures (displaying dysfunctional hyperexcitable tissue), while also preserving neural function. In our understanding, accumulated mechanistic evidence suggests such a beneficial mechanism of action may be due to the natural-like characteristic of a scale-free temporal pattern that may robustly compete with aberrant epileptiform activity for the recruitment of neural circuits. Delivering temporally patterned or random stimuli within specific phases of the underlying oscillations (i.e., those involved in the communication within and across brain regions) could both potentiate and disrupt the formation of neuronal assemblies with random probability. The usage of infinite improbability drive here is obviously a reference to the “The Hitchhiker’s Guide to the Galaxy” comedy science fiction classic, written by Douglas Adams. The parallel is that dynamically driving brain functional connectogram, through neuromodulation, in a manner that would not favor any specific neuronal assembly and/or circuit, could re-stabilize a system that is transitioning to fall under the control of a single attractor. We conclude by discussing future avenues of investigation and their potentially disruptive impact on neurotechnology, with a particular interest in NPS implications in neural plasticity, motor rehabilitation, and its potential for clinical translation.https://www.frontiersin.org/articles/10.3389/fninf.2023.1173597/fullelectrical stimulationneuromodulationcoincidence-detectiontemporal patternpower-lawphase coupling
spellingShingle Vinícius Rosa Cota
Vinícius Rosa Cota
Sérgio Augusto Vieira Cançado
Márcio Flávio Dutra Moraes
On temporal scale-free non-periodic stimulation and its mechanisms as an infinite improbability drive of the brain’s functional connectogram
Frontiers in Neuroinformatics
electrical stimulation
neuromodulation
coincidence-detection
temporal pattern
power-law
phase coupling
title On temporal scale-free non-periodic stimulation and its mechanisms as an infinite improbability drive of the brain’s functional connectogram
title_full On temporal scale-free non-periodic stimulation and its mechanisms as an infinite improbability drive of the brain’s functional connectogram
title_fullStr On temporal scale-free non-periodic stimulation and its mechanisms as an infinite improbability drive of the brain’s functional connectogram
title_full_unstemmed On temporal scale-free non-periodic stimulation and its mechanisms as an infinite improbability drive of the brain’s functional connectogram
title_short On temporal scale-free non-periodic stimulation and its mechanisms as an infinite improbability drive of the brain’s functional connectogram
title_sort on temporal scale free non periodic stimulation and its mechanisms as an infinite improbability drive of the brain s functional connectogram
topic electrical stimulation
neuromodulation
coincidence-detection
temporal pattern
power-law
phase coupling
url https://www.frontiersin.org/articles/10.3389/fninf.2023.1173597/full
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