Brain tissue oxygen dynamics while mimicking the functional deficiency of interneurons
The dynamic interaction between excitatory and inhibitory activity in the brain is known as excitatory-inhibitory balance (EIB). A significant shift in EIB toward excitation has been observed in numerous pathological states and diseases, such as autism or epilepsy, where interneurons may be dysfunct...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-10-01
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| Series: | Frontiers in Cellular Neuroscience |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fncel.2022.983298/full |
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| author | Daniil P. Aksenov Daniil P. Aksenov Daniil P. Aksenov Evan D. Doubovikov Natalya A. Serdyukova Natalya A. Serdyukova David A. Gascoigne Robert A. Linsenmeier Alexander Drobyshevsky Alexander Drobyshevsky |
| author_facet | Daniil P. Aksenov Daniil P. Aksenov Daniil P. Aksenov Evan D. Doubovikov Natalya A. Serdyukova Natalya A. Serdyukova David A. Gascoigne Robert A. Linsenmeier Alexander Drobyshevsky Alexander Drobyshevsky |
| author_sort | Daniil P. Aksenov |
| collection | DOAJ |
| description | The dynamic interaction between excitatory and inhibitory activity in the brain is known as excitatory-inhibitory balance (EIB). A significant shift in EIB toward excitation has been observed in numerous pathological states and diseases, such as autism or epilepsy, where interneurons may be dysfunctional. The consequences of this on neurovascular interactions remains to be elucidated. Specifically, it is not known if there is an elevated metabolic consumption of oxygen due to increased excitatory activity. To investigate this, we administered microinjections of picrotoxin, a gamma aminobutyric acid (GABA) antagonist, to the rabbit cortex in the awake state to mimic the functional deficiency of GABAergic interneurons. This caused an observable shift in EIB toward excitation without the induction of seizures. We used chronically implanted electrodes to measure both neuronal activity and brain tissue oxygen concentrations (PO2) simultaneously and in the same location. Using a high-frequency recording rate for PO2, we were able to detect two important phenomena, (1) the shift in EIB led to a change in the power spectra of PO2 fluctuations, such that higher frequencies (8–15 cycles per minute) were suppressed and (2) there were brief periods (dips with a duration of less than 100 ms associated with neuronal bursts) when PO2 dropped below 10 mmHg, which we defined as the threshold for hypoxia. The dips were followed by an overshoot, which indicates either a rapid vascular response or decrease in oxygen consumption. Our results point to the essential role of interneurons in brain tissue oxygen regulation in the resting state. |
| first_indexed | 2024-04-13T18:43:37Z |
| format | Article |
| id | doaj.art-808f561804b246f0bebad43edddaa610 |
| institution | Directory Open Access Journal |
| issn | 1662-5102 |
| language | English |
| last_indexed | 2024-04-13T18:43:37Z |
| publishDate | 2022-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Cellular Neuroscience |
| spelling | doaj.art-808f561804b246f0bebad43edddaa6102022-12-22T02:34:39ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022022-10-011610.3389/fncel.2022.983298983298Brain tissue oxygen dynamics while mimicking the functional deficiency of interneuronsDaniil P. Aksenov0Daniil P. Aksenov1Daniil P. Aksenov2Evan D. Doubovikov3Natalya A. Serdyukova4Natalya A. Serdyukova5David A. Gascoigne6Robert A. Linsenmeier7Alexander Drobyshevsky8Alexander Drobyshevsky9Department of Radiology, NorthShore University HealthSystem, Evanston, IL, United StatesDepartment of Anesthesiology, NorthShore University HealthSystem, Evanston, IL, United StatesPritzker School of Medicine, University of Chicago, Chicago, IL, United StatesDepartment of Radiology, NorthShore University HealthSystem, Evanston, IL, United StatesDepartment of Biomedical Engineering, Northwestern University, Evanston, IL, United StatesDepartment of Pediatrics, NorthShore University HealthSystem, Evanston, IL, United StatesDepartment of Radiology, NorthShore University HealthSystem, Evanston, IL, United StatesDepartment of Biomedical Engineering, Northwestern University, Evanston, IL, United StatesPritzker School of Medicine, University of Chicago, Chicago, IL, United StatesDepartment of Pediatrics, NorthShore University HealthSystem, Evanston, IL, United StatesThe dynamic interaction between excitatory and inhibitory activity in the brain is known as excitatory-inhibitory balance (EIB). A significant shift in EIB toward excitation has been observed in numerous pathological states and diseases, such as autism or epilepsy, where interneurons may be dysfunctional. The consequences of this on neurovascular interactions remains to be elucidated. Specifically, it is not known if there is an elevated metabolic consumption of oxygen due to increased excitatory activity. To investigate this, we administered microinjections of picrotoxin, a gamma aminobutyric acid (GABA) antagonist, to the rabbit cortex in the awake state to mimic the functional deficiency of GABAergic interneurons. This caused an observable shift in EIB toward excitation without the induction of seizures. We used chronically implanted electrodes to measure both neuronal activity and brain tissue oxygen concentrations (PO2) simultaneously and in the same location. Using a high-frequency recording rate for PO2, we were able to detect two important phenomena, (1) the shift in EIB led to a change in the power spectra of PO2 fluctuations, such that higher frequencies (8–15 cycles per minute) were suppressed and (2) there were brief periods (dips with a duration of less than 100 ms associated with neuronal bursts) when PO2 dropped below 10 mmHg, which we defined as the threshold for hypoxia. The dips were followed by an overshoot, which indicates either a rapid vascular response or decrease in oxygen consumption. Our results point to the essential role of interneurons in brain tissue oxygen regulation in the resting state.https://www.frontiersin.org/articles/10.3389/fncel.2022.983298/fullGABAneurovascular unitneuronal synchronizationcerebral cortexrabbitepilepsy |
| spellingShingle | Daniil P. Aksenov Daniil P. Aksenov Daniil P. Aksenov Evan D. Doubovikov Natalya A. Serdyukova Natalya A. Serdyukova David A. Gascoigne Robert A. Linsenmeier Alexander Drobyshevsky Alexander Drobyshevsky Brain tissue oxygen dynamics while mimicking the functional deficiency of interneurons Frontiers in Cellular Neuroscience GABA neurovascular unit neuronal synchronization cerebral cortex rabbit epilepsy |
| title | Brain tissue oxygen dynamics while mimicking the functional deficiency of interneurons |
| title_full | Brain tissue oxygen dynamics while mimicking the functional deficiency of interneurons |
| title_fullStr | Brain tissue oxygen dynamics while mimicking the functional deficiency of interneurons |
| title_full_unstemmed | Brain tissue oxygen dynamics while mimicking the functional deficiency of interneurons |
| title_short | Brain tissue oxygen dynamics while mimicking the functional deficiency of interneurons |
| title_sort | brain tissue oxygen dynamics while mimicking the functional deficiency of interneurons |
| topic | GABA neurovascular unit neuronal synchronization cerebral cortex rabbit epilepsy |
| url | https://www.frontiersin.org/articles/10.3389/fncel.2022.983298/full |
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