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Sepsis-Induced Changes in Spectral Segregation and Kinetics of Hippocampal Oscillatory States in Rats

Sepsis-associated encephalopathy (SAE) is a frequent severe complication of sepsis and the systemic inflammatory response syndrome, associated with high mortality and long-term neurologic consequences in surviving patients. One of the main clinical signs of SAE are discontinuous sleep periods that a...

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Autores principales: Kala, Annu, Leemburg, Susan, Jezek, Karel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Society for Neuroscience 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10286852/
https://www.ncbi.nlm.nih.gov/pubmed/37286344
http://dx.doi.org/10.1523/ENEURO.0002-23.2023
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author Kala, Annu
Leemburg, Susan
Jezek, Karel
author_facet Kala, Annu
Leemburg, Susan
Jezek, Karel
author_sort Kala, Annu
collection PubMed
description Sepsis-associated encephalopathy (SAE) is a frequent severe complication of sepsis and the systemic inflammatory response syndrome, associated with high mortality and long-term neurologic consequences in surviving patients. One of the main clinical signs of SAE are discontinuous sleep periods that are fragmented by frequent awakenings. Although this brain state fragmentation strongly impacts the functionality of the nervous and other systems, its underlying network mechanisms are still poorly understood. In this work, we therefore aim to characterize the properties and dynamics of brain oscillatory states in response to SAE in an acute rat model of sepsis induced by high-dose lipopolysaccharide (LPS; 10 mg/kg). To focus on intrinsically generated brain state dynamics, we used a urethane model that spares oscillatory activity in rapid eye movement (REM)-like and nonrapid eye movement (NREM)-like sleep states. Intraperitoneal LPS injection led to a robust instability of both oscillatory states resulting in several folds more state transitions. We identified opposing shifts in low-frequency oscillations (1–9 Hz) in REM and NREM-like states under influence of LPS. This resulted in increased similarity between both states. Moreover, the state-space jitter in both states increased as well, pointing to higher within-state instability. The reduction of interstate spectral distances in 2-D state space, combined with increased within-state jitter might represent a key factor in changing the energy landscape of brain oscillatory state attractors, and hence lead to altered sleep architecture. Their emergence during sepsis might point to a mechanism underlying severe sleep fragmentation as described both in sepsis patients and SAE animal models.
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spelling pubmed-102868522023-06-23 Sepsis-Induced Changes in Spectral Segregation and Kinetics of Hippocampal Oscillatory States in Rats Kala, Annu Leemburg, Susan Jezek, Karel eNeuro Research Article: New Research Sepsis-associated encephalopathy (SAE) is a frequent severe complication of sepsis and the systemic inflammatory response syndrome, associated with high mortality and long-term neurologic consequences in surviving patients. One of the main clinical signs of SAE are discontinuous sleep periods that are fragmented by frequent awakenings. Although this brain state fragmentation strongly impacts the functionality of the nervous and other systems, its underlying network mechanisms are still poorly understood. In this work, we therefore aim to characterize the properties and dynamics of brain oscillatory states in response to SAE in an acute rat model of sepsis induced by high-dose lipopolysaccharide (LPS; 10 mg/kg). To focus on intrinsically generated brain state dynamics, we used a urethane model that spares oscillatory activity in rapid eye movement (REM)-like and nonrapid eye movement (NREM)-like sleep states. Intraperitoneal LPS injection led to a robust instability of both oscillatory states resulting in several folds more state transitions. We identified opposing shifts in low-frequency oscillations (1–9 Hz) in REM and NREM-like states under influence of LPS. This resulted in increased similarity between both states. Moreover, the state-space jitter in both states increased as well, pointing to higher within-state instability. The reduction of interstate spectral distances in 2-D state space, combined with increased within-state jitter might represent a key factor in changing the energy landscape of brain oscillatory state attractors, and hence lead to altered sleep architecture. Their emergence during sepsis might point to a mechanism underlying severe sleep fragmentation as described both in sepsis patients and SAE animal models. Society for Neuroscience 2023-06-19 /pmc/articles/PMC10286852/ /pubmed/37286344 http://dx.doi.org/10.1523/ENEURO.0002-23.2023 Text en Copyright © 2023 Kala et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article: New Research
Kala, Annu
Leemburg, Susan
Jezek, Karel
Sepsis-Induced Changes in Spectral Segregation and Kinetics of Hippocampal Oscillatory States in Rats
title Sepsis-Induced Changes in Spectral Segregation and Kinetics of Hippocampal Oscillatory States in Rats
title_full Sepsis-Induced Changes in Spectral Segregation and Kinetics of Hippocampal Oscillatory States in Rats
title_fullStr Sepsis-Induced Changes in Spectral Segregation and Kinetics of Hippocampal Oscillatory States in Rats
title_full_unstemmed Sepsis-Induced Changes in Spectral Segregation and Kinetics of Hippocampal Oscillatory States in Rats
title_short Sepsis-Induced Changes in Spectral Segregation and Kinetics of Hippocampal Oscillatory States in Rats
title_sort sepsis-induced changes in spectral segregation and kinetics of hippocampal oscillatory states in rats
topic Research Article: New Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10286852/
https://www.ncbi.nlm.nih.gov/pubmed/37286344
http://dx.doi.org/10.1523/ENEURO.0002-23.2023
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