Pedunculopontine-stimulation obstructs hippocampal theta rhythm and halts movement

Abstract While the movement of rodents can be paused by optogenetic stimulation of a brainstem nucleus, the pedunculopontine nucleus (PPN), it is unknown whether this response has a functional purpose. The arrest appears conspicuously similar to fear-induced freezing behavior and could constitute a...

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Main Authors: Jaspreet Kaur, Salif A. Komi, Oksana Dmytriyeva, Grace A. Houser, Madelaine C. A. Bonfils, Rune W. Berg
Format: Article
Language:English
Published: Nature Portfolio 2025-05-01
Series:Scientific Reports
Online Access:https://doi.org/10.1038/s41598-025-01695-8
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author Jaspreet Kaur
Salif A. Komi
Oksana Dmytriyeva
Grace A. Houser
Madelaine C. A. Bonfils
Rune W. Berg
author_facet Jaspreet Kaur
Salif A. Komi
Oksana Dmytriyeva
Grace A. Houser
Madelaine C. A. Bonfils
Rune W. Berg
author_sort Jaspreet Kaur
collection DOAJ
description Abstract While the movement of rodents can be paused by optogenetic stimulation of a brainstem nucleus, the pedunculopontine nucleus (PPN), it is unknown whether this response has a functional purpose. The arrest appears conspicuously similar to fear-induced freezing behavior and could constitute a general halting mechanism for movement without an emotional component. Further, it is unclear to what extent brain activity is affected by the evoked motor arrest. Here, we investigate this phenomenon by engaging a distinct brain activity, the hippocampal theta rhythm. The theta rhythm is prominent during locomotor activity, absent under normal immobile situations, yet present under vigilant states like fear-induced freezing. Specifically, we ask whether the PPN-induced motor arrest has the same effect on the theta rhythm as if the animal would perform a volitional arrest, which results in the disappearance of the theta rhythm, or whether it would cause a continuation of the theta rhythm as would be expected by a fear-induced motor arrest. An alternative hypothesis is that the theta rhythm represents an ongoing intention to move rather than the movement itself. To distinguish between these two possibilities, we recorded the hippocampal brain rhythm before and during movement arrest induced by optogenetic stimulation of the PPN in rats. The PPN-induced motor arrest was associated with a clear obstruction of the ongoing theta activity. The timescale of movement arrest was less than 200 ms, similar to the obstruction of the theta rhythm. Since fear and behavioral freezing are associated with hippocampal theta rhythm, which we did not see during PPN stimulation, we suggest that induced motor arrest occurs without an associated emotional component. Further, our experiments reveal that the theta rhythm during motor activity does not represent an intention, but rather the ongoing sensory-motor state.
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spelling doaj-art-28d4f864d6bf40e8a223cea9a4b60ee82025-08-20T03:48:15ZengNature PortfolioScientific Reports2045-23222025-05-0115111210.1038/s41598-025-01695-8Pedunculopontine-stimulation obstructs hippocampal theta rhythm and halts movementJaspreet Kaur0Salif A. Komi1Oksana Dmytriyeva2Grace A. Houser3Madelaine C. A. Bonfils4Rune W. Berg5Department of Neuroscience, Faculty of Health and Medical Sciences, University of CopenhagenDepartment of Neuroscience, Faculty of Health and Medical Sciences, University of CopenhagenNovo Nordisk Foundation Center for Basic Metabolic Research, University of CopenhagenDepartment of Neuroscience, Faculty of Health and Medical Sciences, University of CopenhagenDepartment of Neuroscience, Faculty of Health and Medical Sciences, University of CopenhagenDepartment of Neuroscience, Faculty of Health and Medical Sciences, University of CopenhagenAbstract While the movement of rodents can be paused by optogenetic stimulation of a brainstem nucleus, the pedunculopontine nucleus (PPN), it is unknown whether this response has a functional purpose. The arrest appears conspicuously similar to fear-induced freezing behavior and could constitute a general halting mechanism for movement without an emotional component. Further, it is unclear to what extent brain activity is affected by the evoked motor arrest. Here, we investigate this phenomenon by engaging a distinct brain activity, the hippocampal theta rhythm. The theta rhythm is prominent during locomotor activity, absent under normal immobile situations, yet present under vigilant states like fear-induced freezing. Specifically, we ask whether the PPN-induced motor arrest has the same effect on the theta rhythm as if the animal would perform a volitional arrest, which results in the disappearance of the theta rhythm, or whether it would cause a continuation of the theta rhythm as would be expected by a fear-induced motor arrest. An alternative hypothesis is that the theta rhythm represents an ongoing intention to move rather than the movement itself. To distinguish between these two possibilities, we recorded the hippocampal brain rhythm before and during movement arrest induced by optogenetic stimulation of the PPN in rats. The PPN-induced motor arrest was associated with a clear obstruction of the ongoing theta activity. The timescale of movement arrest was less than 200 ms, similar to the obstruction of the theta rhythm. Since fear and behavioral freezing are associated with hippocampal theta rhythm, which we did not see during PPN stimulation, we suggest that induced motor arrest occurs without an associated emotional component. Further, our experiments reveal that the theta rhythm during motor activity does not represent an intention, but rather the ongoing sensory-motor state.https://doi.org/10.1038/s41598-025-01695-8
spellingShingle Jaspreet Kaur
Salif A. Komi
Oksana Dmytriyeva
Grace A. Houser
Madelaine C. A. Bonfils
Rune W. Berg
Pedunculopontine-stimulation obstructs hippocampal theta rhythm and halts movement
Scientific Reports
title Pedunculopontine-stimulation obstructs hippocampal theta rhythm and halts movement
title_full Pedunculopontine-stimulation obstructs hippocampal theta rhythm and halts movement
title_fullStr Pedunculopontine-stimulation obstructs hippocampal theta rhythm and halts movement
title_full_unstemmed Pedunculopontine-stimulation obstructs hippocampal theta rhythm and halts movement
title_short Pedunculopontine-stimulation obstructs hippocampal theta rhythm and halts movement
title_sort pedunculopontine stimulation obstructs hippocampal theta rhythm and halts movement
url https://doi.org/10.1038/s41598-025-01695-8
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