Interneuron‐mediated inhibition synchronizes neuronal activity during slow oscillation

Key points •  A signature of deep sleep in the EEG is large‐amplitude fluctuation of field potential, which reflects alternating periods of activity and silence in the thalamocortical network. •  Transitions between active and silent states of sleep slow oscillation are well synchronous between remo...

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Published inThe Journal of physiology Vol. 590; no. 16; pp. 3987 - 4010
Main Authors Chen, Jen‐Yung, Chauvette, Sylvain, Skorheim, Steven, Timofeev, Igor, Bazhenov, Maxim
Format Journal Article
LanguageEnglish
Published Oxford, UK Blackwell Publishing Ltd 01.08.2012
Wiley Subscription Services, Inc
Blackwell Science Inc
Subjects
Action Potentials
Animals
Biological Clocks - physiology
Cats - physiology
Cerebral Cortex - physiology
Cortical Synchronization - physiology
Interneurons - physiology
Nerve Net - physiology
Neurons - physiology
Neuroscience: Behavioural/Systems/Cognitive
Sleep
Sleep - physiology
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Abstract Key points •  A signature of deep sleep in the EEG is large‐amplitude fluctuation of field potential, which reflects alternating periods of activity and silence in the thalamocortical network. •  Transitions between active and silent states of sleep slow oscillation are well synchronous between remote populations of neurons with the onsets of silent states synchronized better than the onsets of activity. •  We found that synaptic inhibition plays a major role in terminating active cortical states; strong synaptic inhibition is necessary to synchronize onsets of silent states during normal sleep slow oscillation. •  We further show that when synaptic inhibition is significantly reduced, active state termination is mediated by intrinsic hyperpolarizing conductances. •  Our study suggests that inhibitory interaction in the cortical network actively mediates the patterns of neural activity during slow‐wave sleep and may, therefore, contribute to various brain functions developed during deep sleep.   The signature of slow‐wave sleep in the electroencephalogram (EEG) is large‐amplitude fluctuation of the field potential, which reflects synchronous alternation of activity and silence across cortical neurons. While initiation of the active cortical states during sleep slow oscillation has been intensively studied, the biological mechanisms which drive the network transition from an active state to silence remain poorly understood. In the current study, using a combination of in vivo electrophysiology and thalamocortical network simulation, we explored the impact of intrinsic and synaptic inhibition on state transition during sleep slow oscillation. We found that in normal physiological conditions, synaptic inhibition controls the duration and the synchrony of active state termination. The decline of interneuron‐mediated inhibition led to asynchronous downward transition across the cortical network and broke the regular slow oscillation pattern. Furthermore, in both in vivo experiment and computational modelling, we revealed that when the level of synaptic inhibition was reduced significantly, it led to a recovery of synchronized oscillations in the form of seizure‐like bursting activity. In this condition, the fast active state termination was mediated by intrinsic hyperpolarizing conductances. Our study highlights the significance of both intrinsic and synaptic inhibition in manipulating sleep slow rhythms.
AbstractList The signature of slow-wave sleep in the electroencephalogram (EEG) is large-amplitude fluctuation of the field potential, which reflects synchronous alternation of activity and silence across cortical neurons. While initiation of the active cortical states during sleep slow oscillation has been intensively studied, the biological mechanisms which drive the network transition from an active state to silence remain poorly understood. In the current study, using a combination of in vivo electrophysiology and thalamocortical network simulation, we explored the impact of intrinsic and synaptic inhibition on state transition during sleep slow oscillation. We found that in normal physiological conditions, synaptic inhibition controls the duration and the synchrony of active state termination. The decline of interneuron-mediated inhibition led to asynchronous downward transition across the cortical network and broke the regular slow oscillation pattern. Furthermore, in both in vivo experiment and computational modelling, we revealed that when the level of synaptic inhibition was reduced significantly, it led to a recovery of synchronized oscillations in the form of seizure-like bursting activity. In this condition, the fast active state termination was mediated by intrinsic hyperpolarizing conductances. Our study highlights the significance of both intrinsic and synaptic inhibition in manipulating sleep slow rhythms.
A signature of deep sleep in the EEG is large‐amplitude fluctuation of field potential, which reflects alternating periods of activity and silence in the thalamocortical network. Transitions between active and silent states of sleep slow oscillation are well synchronous between remote populations of neurons with the onsets of silent states synchronized better than the onsets of activity. We found that synaptic inhibition plays a major role in terminating active cortical states; strong synaptic inhibition is necessary to synchronize onsets of silent states during normal sleep slow oscillation. We further show that when synaptic inhibition is significantly reduced, active state termination is mediated by intrinsic hyperpolarizing conductances. Our study suggests that inhibitory interaction in the cortical network actively mediates the patterns of neural activity during slow‐wave sleep and may, therefore, contribute to various brain functions developed during deep sleep. Abstract  The signature of slow‐wave sleep in the electroencephalogram (EEG) is large‐amplitude fluctuation of the field potential, which reflects synchronous alternation of activity and silence across cortical neurons. While initiation of the active cortical states during sleep slow oscillation has been intensively studied, the biological mechanisms which drive the network transition from an active state to silence remain poorly understood. In the current study, using a combination of in vivo electrophysiology and thalamocortical network simulation, we explored the impact of intrinsic and synaptic inhibition on state transition during sleep slow oscillation. We found that in normal physiological conditions, synaptic inhibition controls the duration and the synchrony of active state termination. The decline of interneuron‐mediated inhibition led to asynchronous downward transition across the cortical network and broke the regular slow oscillation pattern. Furthermore, in both in vivo experiment and computational modelling, we revealed that when the level of synaptic inhibition was reduced significantly, it led to a recovery of synchronized oscillations in the form of seizure‐like bursting activity. In this condition, the fast active state termination was mediated by intrinsic hyperpolarizing conductances. Our study highlights the significance of both intrinsic and synaptic inhibition in manipulating sleep slow rhythms.
times A signature of deep sleep in the EEG is large-amplitude fluctuation of field potential, which reflects alternating periods of activity and silence in the thalamocortical network. Abstract The signature of slow-wave sleep in the electroencephalogram (EEG) is large-amplitude fluctuation of the field potential, which reflects synchronous alternation of activity and silence across cortical neurons. While initiation of the active cortical states during sleep slow oscillation has been intensively studied, the biological mechanisms which drive the network transition from an active state to silence remain poorly understood. In the current study, using a combination of in vivo electrophysiology and thalamocortical network simulation, we explored the impact of intrinsic and synaptic inhibition on state transition during sleep slow oscillation. We found that in normal physiological conditions, synaptic inhibition controls the duration and the synchrony of active state termination. The decline of interneuron-mediated inhibition led to asynchronous downward transition across the cortical network and broke the regular slow oscillation pattern. Furthermore, in both in vivo experiment and computational modelling, we revealed that when the level of synaptic inhibition was reduced significantly, it led to a recovery of synchronized oscillations in the form of seizure-like bursting activity. In this condition, the fast active state termination was mediated by intrinsic hyperpolarizing conductances. Our study highlights the significance of both intrinsic and synaptic inhibition in manipulating sleep slow rhythms.
The signature of slow-wave sleep in the electroencephalogram (EEG) is large-amplitude fluctuation of the field potential, which reflects synchronous alternation of activity and silence across cortical neurons. While initiation of the active cortical states during sleep slow oscillation has been intensively studied, the biological mechanisms which drive the network transition from an active state to silence remain poorly understood. In the current study, using a combination of in vivo electrophysiology and thalamocortical network simulation, we explored the impact of intrinsic and synaptic inhibition on state transition during sleep slow oscillation. We found that in normal physiological conditions, synaptic inhibition controls the duration and the synchrony of active state termination. The decline of interneuron-mediated inhibition led to asynchronous downward transition across the cortical network and broke the regular slow oscillation pattern. Furthermore, in both in vivo experiment and computational modelling, we revealed that when the level of synaptic inhibition was reduced significantly, it led to a recovery of synchronized oscillations in the form of seizure-like bursting activity. In this condition, the fast active state termination was mediated by intrinsic hyperpolarizing conductances. Our study highlights the significance of both intrinsic and synaptic inhibition in manipulating sleep slow rhythms.The signature of slow-wave sleep in the electroencephalogram (EEG) is large-amplitude fluctuation of the field potential, which reflects synchronous alternation of activity and silence across cortical neurons. While initiation of the active cortical states during sleep slow oscillation has been intensively studied, the biological mechanisms which drive the network transition from an active state to silence remain poorly understood. In the current study, using a combination of in vivo electrophysiology and thalamocortical network simulation, we explored the impact of intrinsic and synaptic inhibition on state transition during sleep slow oscillation. We found that in normal physiological conditions, synaptic inhibition controls the duration and the synchrony of active state termination. The decline of interneuron-mediated inhibition led to asynchronous downward transition across the cortical network and broke the regular slow oscillation pattern. Furthermore, in both in vivo experiment and computational modelling, we revealed that when the level of synaptic inhibition was reduced significantly, it led to a recovery of synchronized oscillations in the form of seizure-like bursting activity. In this condition, the fast active state termination was mediated by intrinsic hyperpolarizing conductances. Our study highlights the significance of both intrinsic and synaptic inhibition in manipulating sleep slow rhythms.
Key points •  A signature of deep sleep in the EEG is large‐amplitude fluctuation of field potential, which reflects alternating periods of activity and silence in the thalamocortical network. •  Transitions between active and silent states of sleep slow oscillation are well synchronous between remote populations of neurons with the onsets of silent states synchronized better than the onsets of activity. •  We found that synaptic inhibition plays a major role in terminating active cortical states; strong synaptic inhibition is necessary to synchronize onsets of silent states during normal sleep slow oscillation. •  We further show that when synaptic inhibition is significantly reduced, active state termination is mediated by intrinsic hyperpolarizing conductances. •  Our study suggests that inhibitory interaction in the cortical network actively mediates the patterns of neural activity during slow‐wave sleep and may, therefore, contribute to various brain functions developed during deep sleep.   The signature of slow‐wave sleep in the electroencephalogram (EEG) is large‐amplitude fluctuation of the field potential, which reflects synchronous alternation of activity and silence across cortical neurons. While initiation of the active cortical states during sleep slow oscillation has been intensively studied, the biological mechanisms which drive the network transition from an active state to silence remain poorly understood. In the current study, using a combination of in vivo electrophysiology and thalamocortical network simulation, we explored the impact of intrinsic and synaptic inhibition on state transition during sleep slow oscillation. We found that in normal physiological conditions, synaptic inhibition controls the duration and the synchrony of active state termination. The decline of interneuron‐mediated inhibition led to asynchronous downward transition across the cortical network and broke the regular slow oscillation pattern. Furthermore, in both in vivo experiment and computational modelling, we revealed that when the level of synaptic inhibition was reduced significantly, it led to a recovery of synchronized oscillations in the form of seizure‐like bursting activity. In this condition, the fast active state termination was mediated by intrinsic hyperpolarizing conductances. Our study highlights the significance of both intrinsic and synaptic inhibition in manipulating sleep slow rhythms.
Key points * A signature of deep sleep in the EEG is large-amplitude fluctuation of field potential, which reflects alternating periods of activity and silence in the thalamocortical network. * Transitions between active and silent states of sleep slow oscillation are well synchronous between remote populations of neurons with the onsets of silent states synchronized better than the onsets of activity. * We found that synaptic inhibition plays a major role in terminating active cortical states; strong synaptic inhibition is necessary to synchronize onsets of silent states during normal sleep slow oscillation. * We further show that when synaptic inhibition is significantly reduced, active state termination is mediated by intrinsic hyperpolarizing conductances. * Our study suggests that inhibitory interaction in the cortical network actively mediates the patterns of neural activity during slow-wave sleep and may, therefore, contribute to various brain functions developed during deep sleep. Abstract The signature of slow-wave sleep in the electroencephalogram (EEG) is large-amplitude fluctuation of the field potential, which reflects synchronous alternation of activity and silence across cortical neurons. While initiation of the active cortical states during sleep slow oscillation has been intensively studied, the biological mechanisms which drive the network transition from an active state to silence remain poorly understood. In the current study, using a combination of in vivo electrophysiology and thalamocortical network simulation, we explored the impact of intrinsic and synaptic inhibition on state transition during sleep slow oscillation. We found that in normal physiological conditions, synaptic inhibition controls the duration and the synchrony of active state termination. The decline of interneuron-mediated inhibition led to asynchronous downward transition across the cortical network and broke the regular slow oscillation pattern. Furthermore, in both in vivo experiment and computational modelling, we revealed that when the level of synaptic inhibition was reduced significantly, it led to a recovery of synchronized oscillations in the form of seizure-like bursting activity. In this condition, the fast active state termination was mediated by intrinsic hyperpolarizing conductances. Our study highlights the significance of both intrinsic and synaptic inhibition in manipulating sleep slow rhythms.
The signature of slow-wave sleep in the electroencephalogram (EEG) is large-amplitude fluctuation of the field potential, which reflects synchronous alternation of activity and silence across cortical neurons. While initiation of the active cortical states during sleep slow oscillation has been intensively studied, the biological mechanisms which drive the network transition from an active state to silence remain poorly understood. In the current study, using a combination of in vivo electrophysiology and thalamocortical network simulation, we explored the impact of intrinsic and synaptic inhibition on state transition during sleep slow oscillation. We found that in normal physiological conditions, synaptic inhibition controls the duration and the synchrony of active state termination. The decline of interneuron-mediated inhibition led to asynchronous downward transition across the cortical network and broke the regular slow oscillation pattern. Furthermore, in both in vivo experiment and computational modelling, we revealed that when the level of synaptic inhibition was reduced significantly, it led to a recovery of synchronized oscillations in the form of seizure-like bursting activity. In this condition, the fast active state termination was mediated by intrinsic hyperpolarizing conductances. Our study highlights the significance of both intrinsic and synaptic inhibition in manipulating sleep slow rhythms.
Author Skorheim, Steven
Chen, Jen‐Yung
Timofeev, Igor
Bazhenov, Maxim
Chauvette, Sylvain
Author_xml – sequence: 1
  givenname: Jen‐Yung
  surname: Chen
  fullname: Chen, Jen‐Yung
– sequence: 2
  givenname: Sylvain
  surname: Chauvette
  fullname: Chauvette, Sylvain
– sequence: 3
  givenname: Steven
  surname: Skorheim
  fullname: Skorheim, Steven
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  givenname: Igor
  surname: Timofeev
  fullname: Timofeev, Igor
– sequence: 5
  givenname: Maxim
  surname: Bazhenov
  fullname: Bazhenov, Maxim
BackLink https://www.ncbi.nlm.nih.gov/pubmed/22641778$$D View this record in MEDLINE/PubMed
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Snippet Key points •  A signature of deep sleep in the EEG is large‐amplitude fluctuation of field potential, which reflects alternating periods of activity and...
A signature of deep sleep in the EEG is large‐amplitude fluctuation of field potential, which reflects alternating periods of activity and silence in the...
The signature of slow-wave sleep in the electroencephalogram (EEG) is large-amplitude fluctuation of the field potential, which reflects synchronous...
Key points * A signature of deep sleep in the EEG is large-amplitude fluctuation of field potential, which reflects alternating periods of activity and silence...
times A signature of deep sleep in the EEG is large-amplitude fluctuation of field potential, which reflects alternating periods of activity and silence in the...
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SubjectTerms Action Potentials
Animals
Biological Clocks - physiology
Cats - physiology
Cerebral Cortex - physiology
Cortical Synchronization - physiology
Interneurons - physiology
Nerve Net - physiology
Neurons - physiology
Neuroscience: Behavioural/Systems/Cognitive
Sleep
Sleep - physiology
Title Interneuron‐mediated inhibition synchronizes neuronal activity during slow oscillation
URI https://onlinelibrary.wiley.com/doi/abs/10.1113%2Fjphysiol.2012.227462
https://www.ncbi.nlm.nih.gov/pubmed/22641778
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https://www.proquest.com/docview/1034517297
https://www.proquest.com/docview/1419359541
https://pubmed.ncbi.nlm.nih.gov/PMC3476644
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