Intermittent Hypoxia causes targeted disruption to NMDA receptor dependent synaptic plasticity in area CA1 of the hippocampus
Changed NMDA receptor (NMDAr) physiology is implicated with cognitive deficit resulting from conditions ranging from normal aging to neurological disease. Using intermittent hypoxia (IH) to experimentally model untreated sleep apnea, a clinical condition whose comorbidities include neurocognitive im...
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Published in | Experimental neurology Vol. 344; p. 113808 |
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Main Authors | , , , |
Format | Journal Article |
Language | English |
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Elsevier Inc
01.10.2021
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Abstract | Changed NMDA receptor (NMDAr) physiology is implicated with cognitive deficit resulting from conditions ranging from normal aging to neurological disease. Using intermittent hypoxia (IH) to experimentally model untreated sleep apnea, a clinical condition whose comorbidities include neurocognitive impairment, we recently demonstrated that IH causes a pro-oxidant condition that contributes to deficits in spatial memory and in NMDAr-dependent long-term potentiation (LTP). However, the impact of IH on additional forms of synaptic plasticity remains ill-defined. Here we show that IH prevents the induction of NMDAr-dependent LTP and long-term depression (LTD) in hippocampal brain slices from mice exposed to ten days of IH (IH10) yet spares NMDAr-independent forms of synaptic plasticity. Deficits in synaptic plasticity were accompanied by a reduction in hippocampal GluN1 expression. Acute manipulation of redox state using the reducing agent, Dithiothreitol (DTT) stimulated the NMDAr-dependent fEPSP following IH10. However, acute use of either DTT or MnTMPyP did not restore NMDAr-dependent synaptic plasticity after IH10 or prevent the IH-dependent reduction in GluN1, the obligatory subunit of the NMDAr. In contrast, MnTMPyP during IH10 (10-MnTMPyP), prevented the suppressive effects of IH on both NMDAr-dependent synaptic plasticity and GluN1 expression. These findings indicate that while the IH-dependent pro-oxidant state causes reversible oxidative neuromodulation of NMDAr activity, acute manipulation of redox state is ineffective in rescuing two key effects of IH related to the NMDAr within the hippocampus. These IH-dependent changes associated with the NMDAr may be a primary avenue by which IH enhances the vulnerability to impaired learning and memory when sleep apnea is left untreated in normal aging and in disease.
•Intermittent hypoxia (IH) impairs NMDAr-dependent synaptic plasticity yet spares other forms of synaptic plasticity.•Acute modulation of redox state after IH enhances NMDAr activity but does not restore NMDAr dependent synaptic plasticity.•IH reduces expression of GluN1 without altering the ratio of GluN2A to GluN2B expression.•While IH phenocopies the effects of aging on NMDAr-dependent synaptic plasticity, the basis differs between the phenomena. |
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AbstractList | Changed NMDA receptor (NMDAr) physiology is implicated with cognitive deficit resulting from conditions ranging from normal aging to neurological disease. Using intermittent hypoxia (IH) to experimentally model untreated sleep apnea, a clinical condition whose comorbidities include neurocognitive impairment, we recently demonstrated that IH causes a pro-oxidant condition that contributes to deficits in spatial memory and in NMDAr-dependent long-term potentiation (LTP). However, the impact of IH on additional forms of synaptic plasticity remains ill-defined. Here we show that IH prevents the induction of NMDAr-dependent LTP and long-term depression (LTD) in hippocampal brain slices from mice exposed to ten days of IH (IH
10
) yet spares NMDAr-independent forms of synaptic plasticity. Deficits in synaptic plasticity were accompanied by a reduction in hippocampal GluN1 expression. Acute manipulation of redox state using the reducing agent, Dithiothreitol (DTT) stimulated the NMDAr-dependent fEPSP following IH
10
. However, acute use of either DTT or MnTMPyP did not restore NMDAr-dependent synaptic plasticity after IH
10
or prevent the IH-dependent reduction in GluN1, the obligatory subunit of the NMDAr. In contrast, MnTMPyP during IH
10
(10-MnTMPyP), prevented the suppressive effects of IH on both NMDAr-dependent synaptic plasticity and GluN1 expression. These findings indicate that while the IH-dependent pro-oxidant state causes reversible oxidative neuromodulation of NMDAr activity, acute manipulation of redox state is ineffective in rescuing two key effects of IH related to the NMDAr within the hippocampus. These IH-dependent changes associated with the NMDAr may be a primary avenue by which IH enhances the vulnerability to impaired learning and memory when sleep apnea is left untreated in normal aging and in disease. Changed NMDA receptor (NMDAr) physiology is implicated with cognitive deficit resulting from conditions ranging from normal aging to neurological disease. Using intermittent hypoxia (IH) to experimentally model untreated sleep apnea, a clinical condition whose comorbidities include neurocognitive impairment, we recently demonstrated that IH causes a pro-oxidant condition that contributes to deficits in spatial memory and in NMDAr-dependent long-term potentiation (LTP). However, the impact of IH on additional forms of synaptic plasticity remains ill-defined. Here we show that IH prevents the induction of NMDAr-dependent LTP and long-term depression (LTD) in hippocampal brain slices from mice exposed to ten days of IH (IH10) yet spares NMDAr-independent forms of synaptic plasticity. Deficits in synaptic plasticity were accompanied by a reduction in hippocampal GluN1 expression. Acute manipulation of redox state using the reducing agent, Dithiothreitol (DTT) stimulated the NMDAr-dependent fEPSP following IH10. However, acute use of either DTT or MnTMPyP did not restore NMDAr-dependent synaptic plasticity after IH10 or prevent the IH-dependent reduction in GluN1, the obligatory subunit of the NMDAr. In contrast, MnTMPyP during IH10 (10-MnTMPyP), prevented the suppressive effects of IH on both NMDAr-dependent synaptic plasticity and GluN1 expression. These findings indicate that while the IH-dependent pro-oxidant state causes reversible oxidative neuromodulation of NMDAr activity, acute manipulation of redox state is ineffective in rescuing two key effects of IH related to the NMDAr within the hippocampus. These IH-dependent changes associated with the NMDAr may be a primary avenue by which IH enhances the vulnerability to impaired learning and memory when sleep apnea is left untreated in normal aging and in disease. •Intermittent hypoxia (IH) impairs NMDAr-dependent synaptic plasticity yet spares other forms of synaptic plasticity.•Acute modulation of redox state after IH enhances NMDAr activity but does not restore NMDAr dependent synaptic plasticity.•IH reduces expression of GluN1 without altering the ratio of GluN2A to GluN2B expression.•While IH phenocopies the effects of aging on NMDAr-dependent synaptic plasticity, the basis differs between the phenomena. Changed NMDA receptor (NMDAr) physiology is implicated with cognitive deficit resulting from conditions ranging from normal aging to neurological disease. Using intermittent hypoxia (IH) to experimentally model untreated sleep apnea, a clinical condition whose comorbidities include neurocognitive impairment, we recently demonstrated that IH causes a pro-oxidant condition that contributes to deficits in spatial memory and in NMDAr-dependent long-term potentiation (LTP). However, the impact of IH on additional forms of synaptic plasticity remains ill-defined. Here we show that IH prevents the induction of NMDAr-dependent LTP and long-term depression (LTD) in hippocampal brain slices from mice exposed to ten days of IH (IH ) yet spares NMDAr-independent forms of synaptic plasticity. Deficits in synaptic plasticity were accompanied by a reduction in hippocampal GluN1 expression. Acute manipulation of redox state using the reducing agent, Dithiothreitol (DTT) stimulated the NMDAr-dependent fEPSP following IH . However, acute use of either DTT or MnTMPyP did not restore NMDAr-dependent synaptic plasticity after IH or prevent the IH-dependent reduction in GluN1, the obligatory subunit of the NMDAr. In contrast, MnTMPyP during IH (10-MnTMPyP), prevented the suppressive effects of IH on both NMDAr-dependent synaptic plasticity and GluN1 expression. These findings indicate that while the IH-dependent pro-oxidant state causes reversible oxidative neuromodulation of NMDAr activity, acute manipulation of redox state is ineffective in rescuing two key effects of IH related to the NMDAr within the hippocampus. These IH-dependent changes associated with the NMDAr may be a primary avenue by which IH enhances the vulnerability to impaired learning and memory when sleep apnea is left untreated in normal aging and in disease. |
ArticleNumber | 113808 |
Author | Arias-Cavieres, Alejandra Castro-Rivera, Carolina I. Garcia, Alfredo J. Fonteh, Ateh |
AuthorAffiliation | b Grossman Institute for Neuroscience, Quantitative Biology & Human Behavior, The University of Chicago, USA c Department of Medicine, Section of Emergency Medicine, The University of Chicago, USA a Institute for Integrative Physiology, The University of Chicago, USA |
AuthorAffiliation_xml | – name: b Grossman Institute for Neuroscience, Quantitative Biology & Human Behavior, The University of Chicago, USA – name: a Institute for Integrative Physiology, The University of Chicago, USA – name: c Department of Medicine, Section of Emergency Medicine, The University of Chicago, USA |
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CitedBy_id | crossref_primary_10_1016_j_brainresbull_2022_09_021 crossref_primary_10_3389_fnmol_2023_1192833 crossref_primary_10_1016_j_ecoenv_2023_114828 crossref_primary_10_1152_japplphysiol_00332_2022 crossref_primary_10_3389_fphys_2022_891005 crossref_primary_10_1016_j_expneurol_2021_113951 crossref_primary_10_7554_eLife_92175 crossref_primary_10_3390_antiox12040792 crossref_primary_10_7554_eLife_92175_3 crossref_primary_10_3389_fncel_2023_1117697 |
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Keywords | Long term potentiation Oxidative stress Sleep apnea Long term depression Hippocampus |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Author contribution AAC and AJG conceived and designed experiments; AAC, AF and CICR performed experiments, AAC and AJG conducted analyses; AAC and AJG wrote and revised the first draft of the manuscript. AJG provided reagents and support. |
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SubjectTerms | Animals CA1 Region, Hippocampal - metabolism Cells, Cultured Female Hippocampus Hypoxia, Brain - metabolism Long term depression Long term potentiation Male Mice Mice, Inbred C57BL Neuronal Plasticity - physiology Oxidative stress Oxidative Stress - physiology Receptors, N-Methyl-D-Aspartate - metabolism Sleep apnea Sleep Apnea Syndromes - metabolism |
Title | Intermittent Hypoxia causes targeted disruption to NMDA receptor dependent synaptic plasticity in area CA1 of the hippocampus |
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