The impact of closed-loop intracortical stimulation on neural activity in brain-injured, anesthetized animals
Abstract Background Acquired brain injuries, such as stroke, are a major cause of long-term disability worldwide. Intracortical microstimulation (ICMS) can be used successfully to assist in guiding appropriate connections to restore lost sensorimotor integration. Activity-Dependent Stimulation (ADS)...
| Main Authors: | , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2022-02-01
|
| Series: | Bioelectronic Medicine |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s42234-022-00086-y |
| _version_ | 1818919673055412224 |
|---|---|
| author | Marta Carè Alberto Averna Federico Barban Marianna Semprini Lorenzo De Michieli Randolph J. Nudo David J. Guggenmos Michela Chiappalone |
| author_facet | Marta Carè Alberto Averna Federico Barban Marianna Semprini Lorenzo De Michieli Randolph J. Nudo David J. Guggenmos Michela Chiappalone |
| author_sort | Marta Carè |
| collection | DOAJ |
| description | Abstract Background Acquired brain injuries, such as stroke, are a major cause of long-term disability worldwide. Intracortical microstimulation (ICMS) can be used successfully to assist in guiding appropriate connections to restore lost sensorimotor integration. Activity-Dependent Stimulation (ADS) is a specific type of closed-loop ICMS that aims at coupling the activity of two different brain regions by stimulating one in response to activity in the other. Recently, ADS was used to effectively promote behavioral recovery in rodent models following a unilateral traumatic brain injury in the primary motor cortex. While behavioral benefits have been described, the neurophysiological changes in spared areas in response to this type of stimulation have not been fully characterized. Here we explored how single-unit spiking activity is impacted by a focal ischemic lesion and, subsequently, by an ADS treatment. Methods Intracortical microelectrode arrays were implanted in the ipsilesional rostral forelimb area (RFA) to record spike activity and to trigger intracortical microstimulation in the primary somatosensory area (S1) of anaesthetized Long Evans rats. An ischemic injury was induced in the caudal forelimb area through microinjections of Endothelin-1. Activity from both RFA and S1 was recorded and analyzed off-line by evaluating possible changes, either induced by the lesion in the Control group or by stimulation in the ADS group. Results We found that the ischemic lesion in the motor area led to an overall increase in spike activity within RFA and a decrease in S1 with respect to the baseline condition. Subsequent treatment with ADS increased the firing rate in both RFA and S1. Post-stimulation spiking activity was significantly higher compared to pre-stimulation activity in the ADS animals versus non-stimulated controls. Moreover, stimulation promoted the generation of highly synchronized bursting patterns in both RFA and S1 only in the ADS group. Conclusions This study describes the impact on single-unit activity in ipsilesional areas immediately following a cortical infarct and demonstrates that application of ADS is effective in altering this activity. |
| first_indexed | 2024-12-20T01:09:35Z |
| format | Article |
| id | doaj.art-bc1e6a1562a947cea8e3ad509408ad02 |
| institution | Directory Open Access Journal |
| issn | 2332-8886 |
| language | English |
| last_indexed | 2024-12-20T01:09:35Z |
| publishDate | 2022-02-01 |
| publisher | BMC |
| record_format | Article |
| series | Bioelectronic Medicine |
| spelling | doaj.art-bc1e6a1562a947cea8e3ad509408ad022022-12-21T19:58:43ZengBMCBioelectronic Medicine2332-88862022-02-018111410.1186/s42234-022-00086-yThe impact of closed-loop intracortical stimulation on neural activity in brain-injured, anesthetized animalsMarta Carè0Alberto Averna1Federico Barban2Marianna Semprini3Lorenzo De Michieli4Randolph J. Nudo5David J. Guggenmos6Michela Chiappalone7Rehab Technologies, Istituto Italiano di TecnologiaRehab Technologies, Istituto Italiano di TecnologiaRehab Technologies, Istituto Italiano di TecnologiaRehab Technologies, Istituto Italiano di TecnologiaRehab Technologies, Istituto Italiano di TecnologiaDepartment of Rehabilitation Medicine, University of Kansas Medical CenterDepartment of Rehabilitation Medicine, University of Kansas Medical CenterRehab Technologies, Istituto Italiano di TecnologiaAbstract Background Acquired brain injuries, such as stroke, are a major cause of long-term disability worldwide. Intracortical microstimulation (ICMS) can be used successfully to assist in guiding appropriate connections to restore lost sensorimotor integration. Activity-Dependent Stimulation (ADS) is a specific type of closed-loop ICMS that aims at coupling the activity of two different brain regions by stimulating one in response to activity in the other. Recently, ADS was used to effectively promote behavioral recovery in rodent models following a unilateral traumatic brain injury in the primary motor cortex. While behavioral benefits have been described, the neurophysiological changes in spared areas in response to this type of stimulation have not been fully characterized. Here we explored how single-unit spiking activity is impacted by a focal ischemic lesion and, subsequently, by an ADS treatment. Methods Intracortical microelectrode arrays were implanted in the ipsilesional rostral forelimb area (RFA) to record spike activity and to trigger intracortical microstimulation in the primary somatosensory area (S1) of anaesthetized Long Evans rats. An ischemic injury was induced in the caudal forelimb area through microinjections of Endothelin-1. Activity from both RFA and S1 was recorded and analyzed off-line by evaluating possible changes, either induced by the lesion in the Control group or by stimulation in the ADS group. Results We found that the ischemic lesion in the motor area led to an overall increase in spike activity within RFA and a decrease in S1 with respect to the baseline condition. Subsequent treatment with ADS increased the firing rate in both RFA and S1. Post-stimulation spiking activity was significantly higher compared to pre-stimulation activity in the ADS animals versus non-stimulated controls. Moreover, stimulation promoted the generation of highly synchronized bursting patterns in both RFA and S1 only in the ADS group. Conclusions This study describes the impact on single-unit activity in ipsilesional areas immediately following a cortical infarct and demonstrates that application of ADS is effective in altering this activity.https://doi.org/10.1186/s42234-022-00086-yActivity-dependent stimulationFiringIn vivoMicro-electrode arraysSpikeStroke |
| spellingShingle | Marta Carè Alberto Averna Federico Barban Marianna Semprini Lorenzo De Michieli Randolph J. Nudo David J. Guggenmos Michela Chiappalone The impact of closed-loop intracortical stimulation on neural activity in brain-injured, anesthetized animals Bioelectronic Medicine Activity-dependent stimulation Firing In vivo Micro-electrode arrays Spike Stroke |
| title | The impact of closed-loop intracortical stimulation on neural activity in brain-injured, anesthetized animals |
| title_full | The impact of closed-loop intracortical stimulation on neural activity in brain-injured, anesthetized animals |
| title_fullStr | The impact of closed-loop intracortical stimulation on neural activity in brain-injured, anesthetized animals |
| title_full_unstemmed | The impact of closed-loop intracortical stimulation on neural activity in brain-injured, anesthetized animals |
| title_short | The impact of closed-loop intracortical stimulation on neural activity in brain-injured, anesthetized animals |
| title_sort | impact of closed loop intracortical stimulation on neural activity in brain injured anesthetized animals |
| topic | Activity-dependent stimulation Firing In vivo Micro-electrode arrays Spike Stroke |
| url | https://doi.org/10.1186/s42234-022-00086-y |
| work_keys_str_mv | AT martacare theimpactofclosedloopintracorticalstimulationonneuralactivityinbraininjuredanesthetizedanimals AT albertoaverna theimpactofclosedloopintracorticalstimulationonneuralactivityinbraininjuredanesthetizedanimals AT federicobarban theimpactofclosedloopintracorticalstimulationonneuralactivityinbraininjuredanesthetizedanimals AT mariannasemprini theimpactofclosedloopintracorticalstimulationonneuralactivityinbraininjuredanesthetizedanimals AT lorenzodemichieli theimpactofclosedloopintracorticalstimulationonneuralactivityinbraininjuredanesthetizedanimals AT randolphjnudo theimpactofclosedloopintracorticalstimulationonneuralactivityinbraininjuredanesthetizedanimals AT davidjguggenmos theimpactofclosedloopintracorticalstimulationonneuralactivityinbraininjuredanesthetizedanimals AT michelachiappalone theimpactofclosedloopintracorticalstimulationonneuralactivityinbraininjuredanesthetizedanimals AT martacare impactofclosedloopintracorticalstimulationonneuralactivityinbraininjuredanesthetizedanimals AT albertoaverna impactofclosedloopintracorticalstimulationonneuralactivityinbraininjuredanesthetizedanimals AT federicobarban impactofclosedloopintracorticalstimulationonneuralactivityinbraininjuredanesthetizedanimals AT mariannasemprini impactofclosedloopintracorticalstimulationonneuralactivityinbraininjuredanesthetizedanimals AT lorenzodemichieli impactofclosedloopintracorticalstimulationonneuralactivityinbraininjuredanesthetizedanimals AT randolphjnudo impactofclosedloopintracorticalstimulationonneuralactivityinbraininjuredanesthetizedanimals AT davidjguggenmos impactofclosedloopintracorticalstimulationonneuralactivityinbraininjuredanesthetizedanimals AT michelachiappalone impactofclosedloopintracorticalstimulationonneuralactivityinbraininjuredanesthetizedanimals |