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2. Massive perturbation of sound representations by anesthesia in the auditory brainstem.

Author

Gosselin, Etienne, Bagur, Sophie, and Bathellier, Brice

Subjects
*AUDITORY pathways, *SENSORIMOTOR integration, *BRAIN stem, *WAKEFULNESS, *ANESTHESIA, *COCHLEAR nucleus
Abstract

Anesthesia modifies sensory representations in the thalamo-cortical circuit but is considered to have a milder impact on peripheral sensory processing. Here, tracking the same neurons across wakefulness and isoflurane or ketamine medetomidine anesthesia, we show that the amplitude and sign of single neuron responses to sounds are massively modified by anesthesia in the cochlear nucleus of the brainstem, the first relay of the auditory system. The reorganization of activity is so profound that decoding of sound representation under anesthesia is not possible based on awake activity. However, population-level parameters, such as average tuning strength and population decoding accuracy, are weakly affected by anesthesia, explaining why its effect has previously gone unnoticed when comparing independently sampled neurons. Together, our results indicate that the functional organization of the auditory brainstem largely depends on the network state and is ill-defined under anesthesia. This demonstrates a remarkable sensitivity of an early sensory stage to anesthesia, which is bound to disrupt downstream processing. [ABSTRACT FROM AUTHOR]

Published
2024
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8. A Spatial Code for Temporal Information is Necessary for Sensory Learning

Author

Bagur, Sophie, primary, Bourg, Jacques, additional, Kempf, Alexandre, additional, Tarpin, Thibault, additional, Bergaoui, Khalil, additional, Guo, Yin, additional, Ceballo, Sebastian, additional, Schwenkgrub, Joanna, additional, Verdier, Antonin, additional, Puel, Jean-Luc, additional, Bourien, Jérôme, additional, and Bathellier, Brice, additional

Published
2023
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10. A spatial code for temporal cues is necessary for sensory learning

Author

Bagur, Sophie, primary, Bourg, Jacques, additional, Kempf, Alexandre, additional, Tarpin, Thibault, additional, Bergaoui, Khalil, additional, Guo, Yin, additional, Ceballo, Sebastian, additional, Schwenkgrub, Joanna, additional, Verdier, Antonin, additional, Puel, Jean Luc, additional, Bourien, Jérôme, additional, and Bathellier, Brice, additional

Published
2022
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15. Harnessing olfactory bulb oscillations to perform fully brain-based sleep-scoring and real-time monitoring of anaesthesia depth

Author

Bagur, Sophie, Lacroix, Marie Masako, De Lavilléon, Gaetan, Lefort, Julie, Geoffroy, Hélène, Benchenane, Karim, Physiopathologie des Maladies du Système Nerveux Central, Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Neuroscience Paris Seine (NPS), Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut de Biologie Paris Seine (IBPS), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Laboratoire de mécanique des solides (LMS), École polytechnique (X)-MINES ParisTech - École nationale supérieure des mines de Paris-Centre National de la Recherche Scientifique (CNRS), Laboratoire de Physiologie de la Perception et de l'Action (LPPA), Collège de France (CdF)-Centre National de la Recherche Scientifique (CNRS), Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Pierre et Marie Curie - Paris 6 (UPMC), Neurosciences Paris Seine (NPS), École polytechnique (X)-MINES ParisTech - École nationale supérieure des mines de Paris, Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Centre National de la Recherche Scientifique (CNRS), and Collège de France (CdF (institution))-Centre National de la Recherche Scientifique (CNRS)

Subjects
Male, QH301-705.5, Physiology, Imaging Techniques, Cardiology, Sleep, REM, Neurophysiology, Neuroimaging, Research and Analysis Methods, Hippocampus, Gamma Spectrometry, Mice, Spectrum Analysis Techniques, Drug Therapy, Anesthesiology, Heart Rate, Medicine and Health Sciences, Animals, Anesthesia, Biology (General), Wakefulness, ComputingMilieux_MISCELLANEOUS, Clinical Neurophysiology, Brain Mapping, Electromyography, Pharmaceutics, [SCCO.NEUR]Cognitive science/Neuroscience, Electrophysiological Techniques, Methods and Resources, Brain, Biology and Life Sciences, Electroencephalography, Olfactory Bulb, Mice, Inbred C57BL, Electrophysiology, Bioassays and Physiological Analysis, Brain Electrophysiology, Vigilance (Psychology), Sleep Stages, Clinical Medicine, Anatomy, Sleep, Physiological Processes, Algorithms, Muscle Electrophysiology, Neuroscience
Abstract

Real-time tracking of vigilance states related to both sleep or anaesthesia has been a goal for over a century. However, sleep scoring cannot currently be performed with brain signals alone, despite the deep neuromodulatory transformations that accompany sleep state changes. Therefore, at heart, the operational distinction between sleep and wake is that of immobility and movement, despite numerous situations in which this one-to-one mapping fails. Here we demonstrate, using local field potential (LFP) recordings in freely moving mice, that gamma (50–70 Hz) power in the olfactory bulb (OB) allows for clear classification of sleep and wake, thus providing a brain-based criterion to distinguish these two vigilance states without relying on motor activity. Coupled with hippocampal theta activity, it allows the elaboration of a sleep scoring algorithm that relies on brain activity alone. This method reaches over 90% homology with classical methods based on muscular activity (electromyography [EMG]) and video tracking. Moreover, contrary to EMG, OB gamma power allows correct discrimination between sleep and immobility in ambiguous situations such as fear-related freezing. We use the instantaneous power of hippocampal theta oscillation and OB gamma oscillation to construct a 2D phase space that is highly robust throughout time, across individual mice and mouse strains, and under classical drug treatment. Dynamic analysis of trajectories within this space yields a novel characterisation of sleep/wake transitions: whereas waking up is a fast and direct transition that can be modelled by a ballistic trajectory, falling asleep is best described as a stochastic and gradual state change. Finally, we demonstrate that OB oscillations also allow us to track other vigilance states. Non-REM (NREM) and rapid eye movement (REM) sleep can be distinguished with high accuracy based on beta (10–15 Hz) power. More importantly, we show that depth of anaesthesia can be tracked in real time using OB gamma power. Indeed, the gamma power predicts and anticipates the motor response to stimulation both in the steady state under constant anaesthetic and dynamically during the recovery period. Altogether, this methodology opens the avenue for multi-timescale characterisation of brain states and provides an unprecedented window onto levels of vigilance., Author summary Real-time tracking of vigilance states related to wake, sleep, and anaesthesia has been a goal for over a century. However identification of wakefulness and different sleep states cannot currently be performed routinely with brain signals and instead relies on motor activity. Here we demonstrate that 50–70 Hz electrical oscillations in the olfactory bulb (OB) of mice are a reliable indicator for global brain states. Recording this activity with an implanted electrode allows for clear classification of sleep and wake, without the need for motor activity monitoring. We construct a fully automatic sleep scoring algorithm that relies on brain activity alone and is robust throughout time, between animals, and after drug administration. Our method also tracks in real time the depth of anaesthesia both in the steady state under constant anaesthetic and dynamically during the recovery period from anaesthesia. Furthermore, this index predicts responsiveness to noxious stimulation under anaesthesia. Altogether, this methodology opens the avenue for characterisation of vigilance states based on OB recordings.

Published
2018

16. Improved sleep scoring in mice reveals human-like stages

Author

Lacroix, Marie Masako, primary, de Lavilléon, Gaetan, additional, Lefort, Julie, additional, El Kanbi, Karim, additional, Bagur, Sophie, additional, Laventure, Samuel, additional, Dauvilliers, Yves, additional, Peyron, Christelle, additional, and Benchenane, Karim, additional

Published
2018
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25. Harnessing olfactory bulb oscillations to perform fully brain-based sleep-scoring and real-time monitoring of anaesthesia depth.

Author

Bagur S, Lacroix MM, de Lavilléon G, Lefort JM, Geoffroy H, and Benchenane K

Subjects
Algorithms, Anesthesia methods, Animals, Brain physiology, Electroencephalography methods, Electromyography, Hippocampus physiology, Male, Mice, Mice, Inbred C57BL, Olfactory Bulb metabolism, Sleep drug effects, Sleep Stages physiology, Sleep, REM physiology, Olfactory Bulb physiology, Sleep physiology, Wakefulness physiology
Abstract

Real-time tracking of vigilance states related to both sleep or anaesthesia has been a goal for over a century. However, sleep scoring cannot currently be performed with brain signals alone, despite the deep neuromodulatory transformations that accompany sleep state changes. Therefore, at heart, the operational distinction between sleep and wake is that of immobility and movement, despite numerous situations in which this one-to-one mapping fails. Here we demonstrate, using local field potential (LFP) recordings in freely moving mice, that gamma (50-70 Hz) power in the olfactory bulb (OB) allows for clear classification of sleep and wake, thus providing a brain-based criterion to distinguish these two vigilance states without relying on motor activity. Coupled with hippocampal theta activity, it allows the elaboration of a sleep scoring algorithm that relies on brain activity alone. This method reaches over 90% homology with classical methods based on muscular activity (electromyography [EMG]) and video tracking. Moreover, contrary to EMG, OB gamma power allows correct discrimination between sleep and immobility in ambiguous situations such as fear-related freezing. We use the instantaneous power of hippocampal theta oscillation and OB gamma oscillation to construct a 2D phase space that is highly robust throughout time, across individual mice and mouse strains, and under classical drug treatment. Dynamic analysis of trajectories within this space yields a novel characterisation of sleep/wake transitions: whereas waking up is a fast and direct transition that can be modelled by a ballistic trajectory, falling asleep is best described as a stochastic and gradual state change. Finally, we demonstrate that OB oscillations also allow us to track other vigilance states. Non-REM (NREM) and rapid eye movement (REM) sleep can be distinguished with high accuracy based on beta (10-15 Hz) power. More importantly, we show that depth of anaesthesia can be tracked in real time using OB gamma power. Indeed, the gamma power predicts and anticipates the motor response to stimulation both in the steady state under constant anaesthetic and dynamically during the recovery period. Altogether, this methodology opens the avenue for multi-timescale characterisation of brain states and provides an unprecedented window onto levels of vigilance., Competing Interests: The authors have declared that no competing interests exist.

Published
2018
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