Dynamic Metabolic Changes in the Human Thalamus at the Transition From Waking to Sleep - Insights From Simultaneous Functional MR Spectroscopy and Polysomnography
An important contribution of the thalamus to the transition from wakefulness to sleep is a consistent finding in animal studies. In humans, only little is currently known about the specific role of the thalamus in regulating wake-sleep transitions. Although changes in thalamic blood flow and activit...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2019-10-01
|
| Series: | Frontiers in Neuroscience |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/article/10.3389/fnins.2019.01158/full |
| _version_ | 1819135973825445888 |
|---|---|
| author | Mick Lehmann Mick Lehmann Mick Lehmann Andreas Hock Andreas Hock Niklaus Zoelch Niklaus Zoelch Niklaus Zoelch Hans-Peter Landolt Hans-Peter Landolt Erich Seifritz Erich Seifritz |
| author_facet | Mick Lehmann Mick Lehmann Mick Lehmann Andreas Hock Andreas Hock Niklaus Zoelch Niklaus Zoelch Niklaus Zoelch Hans-Peter Landolt Hans-Peter Landolt Erich Seifritz Erich Seifritz |
| author_sort | Mick Lehmann |
| collection | DOAJ |
| description | An important contribution of the thalamus to the transition from wakefulness to sleep is a consistent finding in animal studies. In humans, only little is currently known about the specific role of the thalamus in regulating wake-sleep transitions. Although changes in thalamic blood flow and activity have been reported, the underlying molecular mechanisms have not been investigated. Knowledge about neurotransmitter changes at the wake-to-sleep transition would be indispensable for a better translation of basic animal research findings to humans. Here, we start to fill this important scientific gap. More specifically, we benefit from recent advances in magnetic resonance (MR) spectroscopy, which allow for the non-invasive, local-specific and high-quality detection of naturally occurring metabolite changes in the human brain. We demonstrate in nine young adults able to produce consolidated sleep in the MR spectroscopy scanner, a specific decrease in thalamic glutamate concentration from wakefulness to stage N2 sleep. The magnitude of this decrease was highly correlated with individual N2 sleep duration. When five participants of the original experiment were kept awake in a separate control condition, no decrease in thalamic glutamate levels occurred. The study highlights for the first time in humans that dynamic changes in distinct brain metabolites can be reliably detected at the transition from waking to sleep. The reported methodology to simultaneously acquire functional MR spectroscopy data and neurophysiological signals offers great potential for investigating the molecular mechanisms underlying the transition between and the maintenance of sleep and wake states in humans. |
| first_indexed | 2024-12-22T10:27:36Z |
| format | Article |
| id | doaj.art-a2972df622bf48678a9aae061cd4bc5c |
| institution | Directory Open Access Journal |
| issn | 1662-453X |
| language | English |
| last_indexed | 2024-12-22T10:27:36Z |
| publishDate | 2019-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Neuroscience |
| spelling | doaj.art-a2972df622bf48678a9aae061cd4bc5c2022-12-21T18:29:25ZengFrontiers Media S.A.Frontiers in Neuroscience1662-453X2019-10-011310.3389/fnins.2019.01158491574Dynamic Metabolic Changes in the Human Thalamus at the Transition From Waking to Sleep - Insights From Simultaneous Functional MR Spectroscopy and PolysomnographyMick Lehmann0Mick Lehmann1Mick Lehmann2Andreas Hock3Andreas Hock4Niklaus Zoelch5Niklaus Zoelch6Niklaus Zoelch7Hans-Peter Landolt8Hans-Peter Landolt9Erich Seifritz10Erich Seifritz11Institute of Pharmacology and Toxicology, University of Zurich, Zurich, SwitzerlandSleep & Health Zurich, University of Zurich, Zurich, SwitzerlandDepartment of Psychiatry, Psychotherapy and Psychosomatics, Hospital of Psychiatry, University of Zurich, Zurich, SwitzerlandDepartment of Psychiatry, Psychotherapy and Psychosomatics, Hospital of Psychiatry, University of Zurich, Zurich, SwitzerlandInstitute for Biomedical Engineering, ETH Zurich and University of Zurich, Zurich, SwitzerlandDepartment of Psychiatry, Psychotherapy and Psychosomatics, Hospital of Psychiatry, University of Zurich, Zurich, SwitzerlandInstitute for Biomedical Engineering, ETH Zurich and University of Zurich, Zurich, SwitzerlandDepartment of Forensic Medicine and Imaging, Institute of Forensic Medicine, University of Zurich, Zurich, SwitzerlandInstitute of Pharmacology and Toxicology, University of Zurich, Zurich, SwitzerlandSleep & Health Zurich, University of Zurich, Zurich, SwitzerlandSleep & Health Zurich, University of Zurich, Zurich, SwitzerlandDepartment of Psychiatry, Psychotherapy and Psychosomatics, Hospital of Psychiatry, University of Zurich, Zurich, SwitzerlandAn important contribution of the thalamus to the transition from wakefulness to sleep is a consistent finding in animal studies. In humans, only little is currently known about the specific role of the thalamus in regulating wake-sleep transitions. Although changes in thalamic blood flow and activity have been reported, the underlying molecular mechanisms have not been investigated. Knowledge about neurotransmitter changes at the wake-to-sleep transition would be indispensable for a better translation of basic animal research findings to humans. Here, we start to fill this important scientific gap. More specifically, we benefit from recent advances in magnetic resonance (MR) spectroscopy, which allow for the non-invasive, local-specific and high-quality detection of naturally occurring metabolite changes in the human brain. We demonstrate in nine young adults able to produce consolidated sleep in the MR spectroscopy scanner, a specific decrease in thalamic glutamate concentration from wakefulness to stage N2 sleep. The magnitude of this decrease was highly correlated with individual N2 sleep duration. When five participants of the original experiment were kept awake in a separate control condition, no decrease in thalamic glutamate levels occurred. The study highlights for the first time in humans that dynamic changes in distinct brain metabolites can be reliably detected at the transition from waking to sleep. The reported methodology to simultaneously acquire functional MR spectroscopy data and neurophysiological signals offers great potential for investigating the molecular mechanisms underlying the transition between and the maintenance of sleep and wake states in humans.https://www.frontiersin.org/article/10.3389/fnins.2019.01158/fullglutamateelectroencephalography (EEG)metabolite cyclingexcitabilitythalamic reticular nucleus |
| spellingShingle | Mick Lehmann Mick Lehmann Mick Lehmann Andreas Hock Andreas Hock Niklaus Zoelch Niklaus Zoelch Niklaus Zoelch Hans-Peter Landolt Hans-Peter Landolt Erich Seifritz Erich Seifritz Dynamic Metabolic Changes in the Human Thalamus at the Transition From Waking to Sleep - Insights From Simultaneous Functional MR Spectroscopy and Polysomnography Frontiers in Neuroscience glutamate electroencephalography (EEG) metabolite cycling excitability thalamic reticular nucleus |
| title | Dynamic Metabolic Changes in the Human Thalamus at the Transition From Waking to Sleep - Insights From Simultaneous Functional MR Spectroscopy and Polysomnography |
| title_full | Dynamic Metabolic Changes in the Human Thalamus at the Transition From Waking to Sleep - Insights From Simultaneous Functional MR Spectroscopy and Polysomnography |
| title_fullStr | Dynamic Metabolic Changes in the Human Thalamus at the Transition From Waking to Sleep - Insights From Simultaneous Functional MR Spectroscopy and Polysomnography |
| title_full_unstemmed | Dynamic Metabolic Changes in the Human Thalamus at the Transition From Waking to Sleep - Insights From Simultaneous Functional MR Spectroscopy and Polysomnography |
| title_short | Dynamic Metabolic Changes in the Human Thalamus at the Transition From Waking to Sleep - Insights From Simultaneous Functional MR Spectroscopy and Polysomnography |
| title_sort | dynamic metabolic changes in the human thalamus at the transition from waking to sleep insights from simultaneous functional mr spectroscopy and polysomnography |
| topic | glutamate electroencephalography (EEG) metabolite cycling excitability thalamic reticular nucleus |
| url | https://www.frontiersin.org/article/10.3389/fnins.2019.01158/full |
| work_keys_str_mv | AT micklehmann dynamicmetabolicchangesinthehumanthalamusatthetransitionfromwakingtosleepinsightsfromsimultaneousfunctionalmrspectroscopyandpolysomnography AT micklehmann dynamicmetabolicchangesinthehumanthalamusatthetransitionfromwakingtosleepinsightsfromsimultaneousfunctionalmrspectroscopyandpolysomnography AT micklehmann dynamicmetabolicchangesinthehumanthalamusatthetransitionfromwakingtosleepinsightsfromsimultaneousfunctionalmrspectroscopyandpolysomnography AT andreashock dynamicmetabolicchangesinthehumanthalamusatthetransitionfromwakingtosleepinsightsfromsimultaneousfunctionalmrspectroscopyandpolysomnography AT andreashock dynamicmetabolicchangesinthehumanthalamusatthetransitionfromwakingtosleepinsightsfromsimultaneousfunctionalmrspectroscopyandpolysomnography AT niklauszoelch dynamicmetabolicchangesinthehumanthalamusatthetransitionfromwakingtosleepinsightsfromsimultaneousfunctionalmrspectroscopyandpolysomnography AT niklauszoelch dynamicmetabolicchangesinthehumanthalamusatthetransitionfromwakingtosleepinsightsfromsimultaneousfunctionalmrspectroscopyandpolysomnography AT niklauszoelch dynamicmetabolicchangesinthehumanthalamusatthetransitionfromwakingtosleepinsightsfromsimultaneousfunctionalmrspectroscopyandpolysomnography AT hanspeterlandolt dynamicmetabolicchangesinthehumanthalamusatthetransitionfromwakingtosleepinsightsfromsimultaneousfunctionalmrspectroscopyandpolysomnography AT hanspeterlandolt dynamicmetabolicchangesinthehumanthalamusatthetransitionfromwakingtosleepinsightsfromsimultaneousfunctionalmrspectroscopyandpolysomnography AT erichseifritz dynamicmetabolicchangesinthehumanthalamusatthetransitionfromwakingtosleepinsightsfromsimultaneousfunctionalmrspectroscopyandpolysomnography AT erichseifritz dynamicmetabolicchangesinthehumanthalamusatthetransitionfromwakingtosleepinsightsfromsimultaneousfunctionalmrspectroscopyandpolysomnography |