Cargando…

The aperiodic exponent of subthalamic field potentials reflects excitation/inhibition balance in Parkinsonism

Periodic features of neural time-series data, such as local field potentials (LFPs), are often quantified using power spectra. While the aperiodic exponent of spectra is typically disregarded, it is nevertheless modulated in a physiologically relevant manner and was recently hypothesised to reflect...

Descripción completa

Detalles Bibliográficos
Autores principales: Wiest, Christoph, Torrecillos, Flavie, Pogosyan, Alek, Bange, Manuel, Muthuraman, Muthuraman, Groppa, Sergiu, Hulse, Natasha, Hasegawa, Harutomo, Ashkan, Keyoumars, Baig, Fahd, Morgante, Francesca, Pereira, Erlick A, Mallet, Nicolas, Magill, Peter J, Brown, Peter, Sharott, Andrew, Tan, Huiling
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10005762/
https://www.ncbi.nlm.nih.gov/pubmed/36810199
http://dx.doi.org/10.7554/eLife.82467
_version_ 1784905161162883072
author Wiest, Christoph
Torrecillos, Flavie
Pogosyan, Alek
Bange, Manuel
Muthuraman, Muthuraman
Groppa, Sergiu
Hulse, Natasha
Hasegawa, Harutomo
Ashkan, Keyoumars
Baig, Fahd
Morgante, Francesca
Pereira, Erlick A
Mallet, Nicolas
Magill, Peter J
Brown, Peter
Sharott, Andrew
Tan, Huiling
author_facet Wiest, Christoph
Torrecillos, Flavie
Pogosyan, Alek
Bange, Manuel
Muthuraman, Muthuraman
Groppa, Sergiu
Hulse, Natasha
Hasegawa, Harutomo
Ashkan, Keyoumars
Baig, Fahd
Morgante, Francesca
Pereira, Erlick A
Mallet, Nicolas
Magill, Peter J
Brown, Peter
Sharott, Andrew
Tan, Huiling
author_sort Wiest, Christoph
collection PubMed
description Periodic features of neural time-series data, such as local field potentials (LFPs), are often quantified using power spectra. While the aperiodic exponent of spectra is typically disregarded, it is nevertheless modulated in a physiologically relevant manner and was recently hypothesised to reflect excitation/inhibition (E/I) balance in neuronal populations. Here, we used a cross-species in vivo electrophysiological approach to test the E/I hypothesis in the context of experimental and idiopathic Parkinsonism. We demonstrate in dopamine-depleted rats that aperiodic exponents and power at 30–100 Hz in subthalamic nucleus (STN) LFPs reflect defined changes in basal ganglia network activity; higher aperiodic exponents tally with lower levels of STN neuron firing and a balance tipped towards inhibition. Using STN-LFPs recorded from awake Parkinson’s patients, we show that higher exponents accompany dopaminergic medication and deep brain stimulation (DBS) of STN, consistent with untreated Parkinson’s manifesting as reduced inhibition and hyperactivity of STN. These results suggest that the aperiodic exponent of STN-LFPs in Parkinsonism reflects E/I balance and might be a candidate biomarker for adaptive DBS.
format Online
Article
Text
id pubmed-10005762
institution National Center for Biotechnology Information
language English
publishDate 2023
publisher eLife Sciences Publications, Ltd
record_format MEDLINE/PubMed
spelling pubmed-100057622023-03-11 The aperiodic exponent of subthalamic field potentials reflects excitation/inhibition balance in Parkinsonism Wiest, Christoph Torrecillos, Flavie Pogosyan, Alek Bange, Manuel Muthuraman, Muthuraman Groppa, Sergiu Hulse, Natasha Hasegawa, Harutomo Ashkan, Keyoumars Baig, Fahd Morgante, Francesca Pereira, Erlick A Mallet, Nicolas Magill, Peter J Brown, Peter Sharott, Andrew Tan, Huiling eLife Neuroscience Periodic features of neural time-series data, such as local field potentials (LFPs), are often quantified using power spectra. While the aperiodic exponent of spectra is typically disregarded, it is nevertheless modulated in a physiologically relevant manner and was recently hypothesised to reflect excitation/inhibition (E/I) balance in neuronal populations. Here, we used a cross-species in vivo electrophysiological approach to test the E/I hypothesis in the context of experimental and idiopathic Parkinsonism. We demonstrate in dopamine-depleted rats that aperiodic exponents and power at 30–100 Hz in subthalamic nucleus (STN) LFPs reflect defined changes in basal ganglia network activity; higher aperiodic exponents tally with lower levels of STN neuron firing and a balance tipped towards inhibition. Using STN-LFPs recorded from awake Parkinson’s patients, we show that higher exponents accompany dopaminergic medication and deep brain stimulation (DBS) of STN, consistent with untreated Parkinson’s manifesting as reduced inhibition and hyperactivity of STN. These results suggest that the aperiodic exponent of STN-LFPs in Parkinsonism reflects E/I balance and might be a candidate biomarker for adaptive DBS. eLife Sciences Publications, Ltd 2023-02-22 /pmc/articles/PMC10005762/ /pubmed/36810199 http://dx.doi.org/10.7554/eLife.82467 Text en © 2023, Wiest et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Neuroscience
Wiest, Christoph
Torrecillos, Flavie
Pogosyan, Alek
Bange, Manuel
Muthuraman, Muthuraman
Groppa, Sergiu
Hulse, Natasha
Hasegawa, Harutomo
Ashkan, Keyoumars
Baig, Fahd
Morgante, Francesca
Pereira, Erlick A
Mallet, Nicolas
Magill, Peter J
Brown, Peter
Sharott, Andrew
Tan, Huiling
The aperiodic exponent of subthalamic field potentials reflects excitation/inhibition balance in Parkinsonism
title The aperiodic exponent of subthalamic field potentials reflects excitation/inhibition balance in Parkinsonism
title_full The aperiodic exponent of subthalamic field potentials reflects excitation/inhibition balance in Parkinsonism
title_fullStr The aperiodic exponent of subthalamic field potentials reflects excitation/inhibition balance in Parkinsonism
title_full_unstemmed The aperiodic exponent of subthalamic field potentials reflects excitation/inhibition balance in Parkinsonism
title_short The aperiodic exponent of subthalamic field potentials reflects excitation/inhibition balance in Parkinsonism
title_sort aperiodic exponent of subthalamic field potentials reflects excitation/inhibition balance in parkinsonism
topic Neuroscience
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10005762/
https://www.ncbi.nlm.nih.gov/pubmed/36810199
http://dx.doi.org/10.7554/eLife.82467
work_keys_str_mv AT wiestchristoph theaperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT torrecillosflavie theaperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT pogosyanalek theaperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT bangemanuel theaperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT muthuramanmuthuraman theaperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT groppasergiu theaperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT hulsenatasha theaperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT hasegawaharutomo theaperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT ashkankeyoumars theaperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT baigfahd theaperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT morgantefrancesca theaperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT pereiraerlicka theaperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT malletnicolas theaperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT magillpeterj theaperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT brownpeter theaperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT sharottandrew theaperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT tanhuiling theaperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT wiestchristoph aperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT torrecillosflavie aperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT pogosyanalek aperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT bangemanuel aperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT muthuramanmuthuraman aperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT groppasergiu aperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT hulsenatasha aperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT hasegawaharutomo aperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT ashkankeyoumars aperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT baigfahd aperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT morgantefrancesca aperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT pereiraerlicka aperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT malletnicolas aperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT magillpeterj aperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT brownpeter aperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT sharottandrew aperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism
AT tanhuiling aperiodicexponentofsubthalamicfieldpotentialsreflectsexcitationinhibitionbalanceinparkinsonism