LFP Analysis of Brain Injured Anesthetized Animals Undergoing Closed-Loop Intracortical Stimulation

Activity dependent stimulation (ADS) is a closed loop stimulation technique whose neurophysiological effects have not been deeply investigated. Here we explored how Local field Potentials (LFP) are impacted by a focal ischemic lesion and, subsequently, by ADS treatment. Intracortical microelectrode...

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Main Authors: Alberto Averna, Federico Barban, Marta Care, Maxwell D. Murphy, Riccardo Iandolo, Lorenzo De Michieli, Randolph J. Nudo, David J. Guggenmos, Michela Chiappalone
Format: Article
Language:English
Published: IEEE 2022-01-01
Series:IEEE Transactions on Neural Systems and Rehabilitation Engineering
Subjects:
Online Access:https://ieeexplore.ieee.org/document/9780254/
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author Alberto Averna
Federico Barban
Marta Care
Maxwell D. Murphy
Riccardo Iandolo
Lorenzo De Michieli
Randolph J. Nudo
David J. Guggenmos
Michela Chiappalone
author_facet Alberto Averna
Federico Barban
Marta Care
Maxwell D. Murphy
Riccardo Iandolo
Lorenzo De Michieli
Randolph J. Nudo
David J. Guggenmos
Michela Chiappalone
author_sort Alberto Averna
collection DOAJ
description Activity dependent stimulation (ADS) is a closed loop stimulation technique whose neurophysiological effects have not been deeply investigated. Here we explored how Local field Potentials (LFP) are impacted by a focal ischemic lesion and, subsequently, by ADS treatment. Intracortical microelectrode arrays were implanted in the rostral forelimb area (RFA) and in the primary somatosensory area (S1) of anaesthetized rats. An ischemic injury was induced in the caudal forelimb area through microinjections of Endothelin-1. The lesion induced an acute depressive trend in LFP power in RFA (evaluated in 6 bands of interest: Delta (1–4Hz), Theta (4–8Hz), Alpha (8-11Hz), Beta (11–30Hz), LowGamma (30–55Hz) and HighGamma (55-80)) followed by a noticeable significant rebound in both areas. Applying ADS induced an overall decrease of power. The lesion impacted the connectivity in a frequency specific manner, resulting in widespread increase in connectivity in Delta both between and within areas. Two hours after the lesion, without stimulation, correlated activity between areas increased in Beta and Gamma. After stimulation, inter-area connectivity increased in Delta, Theta and Alpha, while considerably dropping within RFA in highGamma. By computing phase-amplitude coupling, we found that the lesion produced an incremental increase in the coupling between (Theta) Alpha phase and (lowGamma) highGamma amplitude within RFA, while S1 had a more generalized increase. Likewise, coupling between Theta phase and lowGamma/highGamma amplitudes increased between areas after lesion. ADS induced a similar increase, but greater in magnitude both within and between RFA and S1. These results have important implications on the emerging field of closed-loop adaptive stimulation promoting ADS as an innovative tool for the treatment of neurological disorders.
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spelling doaj.art-d18e73e84e0945ca9b55cff1f84d78062024-01-16T00:00:06ZengIEEEIEEE Transactions on Neural Systems and Rehabilitation Engineering1558-02102022-01-01301441145110.1109/TNSRE.2022.31772549780254LFP Analysis of Brain Injured Anesthetized Animals Undergoing Closed-Loop Intracortical StimulationAlberto Averna0https://orcid.org/0000-0001-9738-1281Federico Barban1https://orcid.org/0000-0002-5828-0282Marta Care2https://orcid.org/0000-0002-7100-1639Maxwell D. Murphy3https://orcid.org/0000-0002-8559-2361Riccardo Iandolo4Lorenzo De Michieli5https://orcid.org/0000-0001-7158-3002Randolph J. Nudo6David J. Guggenmos7Michela Chiappalone8https://orcid.org/0000-0003-1427-5147Rehab Technologies, Istituto Italiano di Tecnologia, Genoa, ItalyRehab Technologies, Istituto Italiano di Tecnologia, Genoa, ItalyRehab Technologies, Istituto Italiano di Tecnologia, Genoa, ItalyDepartment of Rehabilitation Medicine, and the Landon Center on Aging, University of Kansas Medical Center, Kansas City, KS, USARehab Technologies, Istituto Italiano di Tecnologia, Genoa, ItalyRehab Technologies, Istituto Italiano di Tecnologia, Genoa, ItalyDepartment of Rehabilitation Medicine, and the Landon Center on Aging, University of Kansas Medical Center, Kansas City, KS, USADepartment of Rehabilitation Medicine, and the Landon Center on Aging, University of Kansas Medical Center, Kansas City, KS, USARehab Technologies, Istituto Italiano di Tecnologia, Genoa, ItalyActivity dependent stimulation (ADS) is a closed loop stimulation technique whose neurophysiological effects have not been deeply investigated. Here we explored how Local field Potentials (LFP) are impacted by a focal ischemic lesion and, subsequently, by ADS treatment. Intracortical microelectrode arrays were implanted in the rostral forelimb area (RFA) and in the primary somatosensory area (S1) of anaesthetized rats. An ischemic injury was induced in the caudal forelimb area through microinjections of Endothelin-1. The lesion induced an acute depressive trend in LFP power in RFA (evaluated in 6 bands of interest: Delta (1–4Hz), Theta (4–8Hz), Alpha (8-11Hz), Beta (11–30Hz), LowGamma (30–55Hz) and HighGamma (55-80)) followed by a noticeable significant rebound in both areas. Applying ADS induced an overall decrease of power. The lesion impacted the connectivity in a frequency specific manner, resulting in widespread increase in connectivity in Delta both between and within areas. Two hours after the lesion, without stimulation, correlated activity between areas increased in Beta and Gamma. After stimulation, inter-area connectivity increased in Delta, Theta and Alpha, while considerably dropping within RFA in highGamma. By computing phase-amplitude coupling, we found that the lesion produced an incremental increase in the coupling between (Theta) Alpha phase and (lowGamma) highGamma amplitude within RFA, while S1 had a more generalized increase. Likewise, coupling between Theta phase and lowGamma/highGamma amplitudes increased between areas after lesion. ADS induced a similar increase, but greater in magnitude both within and between RFA and S1. These results have important implications on the emerging field of closed-loop adaptive stimulation promoting ADS as an innovative tool for the treatment of neurological disorders.https://ieeexplore.ieee.org/document/9780254/Activity-dependent stimulationconnectivityin vivolocal field potentialmicro-electrode arraysphase amplitude coupling
spellingShingle Alberto Averna
Federico Barban
Marta Care
Maxwell D. Murphy
Riccardo Iandolo
Lorenzo De Michieli
Randolph J. Nudo
David J. Guggenmos
Michela Chiappalone
LFP Analysis of Brain Injured Anesthetized Animals Undergoing Closed-Loop Intracortical Stimulation
IEEE Transactions on Neural Systems and Rehabilitation Engineering
Activity-dependent stimulation
connectivity
in vivo
local field potential
micro-electrode arrays
phase amplitude coupling
title LFP Analysis of Brain Injured Anesthetized Animals Undergoing Closed-Loop Intracortical Stimulation
title_full LFP Analysis of Brain Injured Anesthetized Animals Undergoing Closed-Loop Intracortical Stimulation
title_fullStr LFP Analysis of Brain Injured Anesthetized Animals Undergoing Closed-Loop Intracortical Stimulation
title_full_unstemmed LFP Analysis of Brain Injured Anesthetized Animals Undergoing Closed-Loop Intracortical Stimulation
title_short LFP Analysis of Brain Injured Anesthetized Animals Undergoing Closed-Loop Intracortical Stimulation
title_sort lfp analysis of brain injured anesthetized animals undergoing closed loop intracortical stimulation
topic Activity-dependent stimulation
connectivity
in vivo
local field potential
micro-electrode arrays
phase amplitude coupling
url https://ieeexplore.ieee.org/document/9780254/
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