Coupling of hippocampal theta and ripples with pontogeniculooccipital waves
The hippocampus has a major role in encoding and consolidating long-term memories, and undergoes plastic changes during sleep 1 . These changes require precise homeostatic control by subcortical neuromodulatory structures 2 . The underlying mechanisms of this phenomenon, however, remain unknown. Her...
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| Veröffentlicht in: | Nature (London) 2021-01, Vol.589 (7840), p.96-102 |
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| creator | Ramirez-Villegas, Juan F. Besserve, Michel Murayama, Yusuke Evrard, Henry C. Oeltermann, Axel Logothetis, Nikos K. |
| description | The hippocampus has a major role in encoding and consolidating long-term memories, and undergoes plastic changes during sleep
1
. These changes require precise homeostatic control by subcortical neuromodulatory structures
2
. The underlying mechanisms of this phenomenon, however, remain unknown. Here, using multi-structure recordings in macaque monkeys, we show that the brainstem transiently modulates hippocampal network events through phasic pontine waves known as pontogeniculooccipital waves (PGO waves). Two physiologically distinct types of PGO wave appear to occur sequentially, selectively influencing high-frequency ripples and low-frequency theta events, respectively. The two types of PGO wave are associated with opposite hippocampal spike-field coupling, prompting periods of high neural synchrony of neural populations during periods of ripple and theta instances. The coupling between PGO waves and ripples, classically associated with distinct sleep stages, supports the notion that a global coordination mechanism of hippocampal sleep dynamics by cholinergic pontine transients may promote systems and synaptic memory consolidation as well as synaptic homeostasis.
Studies using multi-structure recordings in macaque monkeys show that distinct phasic pontogeniculooccipital waves modulate hippocampal network events similar to those that underlie the learning and formation of memories during sleep. |
| doi_str_mv | 10.1038/s41586-020-2914-4 |
| format | Article |
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1
. These changes require precise homeostatic control by subcortical neuromodulatory structures
2
. The underlying mechanisms of this phenomenon, however, remain unknown. Here, using multi-structure recordings in macaque monkeys, we show that the brainstem transiently modulates hippocampal network events through phasic pontine waves known as pontogeniculooccipital waves (PGO waves). Two physiologically distinct types of PGO wave appear to occur sequentially, selectively influencing high-frequency ripples and low-frequency theta events, respectively. The two types of PGO wave are associated with opposite hippocampal spike-field coupling, prompting periods of high neural synchrony of neural populations during periods of ripple and theta instances. The coupling between PGO waves and ripples, classically associated with distinct sleep stages, supports the notion that a global coordination mechanism of hippocampal sleep dynamics by cholinergic pontine transients may promote systems and synaptic memory consolidation as well as synaptic homeostasis.
Studies using multi-structure recordings in macaque monkeys show that distinct phasic pontogeniculooccipital waves modulate hippocampal network events similar to those that underlie the learning and formation of memories during sleep.</description><identifier>ISSN: 0028-0836</identifier><identifier>EISSN: 1476-4687</identifier><identifier>DOI: 10.1038/s41586-020-2914-4</identifier><identifier>PMID: 33208951</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>631/378 ; 631/378/2649 ; 692/698 ; 9/30 ; 96/63 ; Animals ; Brain stem ; Cholinergics ; Chromosome Pairing - physiology ; Coupling ; Experiments ; Female ; Geniculate Bodies - physiology ; Hippocampus ; Hippocampus - physiology ; Homeostasis ; Humanities and Social Sciences ; Macaca - physiology ; Memory ; Memory Consolidation - physiology ; Monkeys ; multidisciplinary ; Neuronal Plasticity ; Occipital Lobe - physiology ; Plasticity ; Pons - physiology ; Ripples ; Science ; Science (multidisciplinary) ; Sleep ; Sleep - physiology ; Sleep Stages - physiology ; Theta Rhythm - physiology ; Theta rhythms</subject><ispartof>Nature (London), 2021-01, Vol.589 (7840), p.96-102</ispartof><rights>The Author(s), under exclusive licence to Springer Nature Limited 2020</rights><rights>Copyright Nature Publishing Group Jan 7, 2021</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c372t-8bdbd8982efad7f7cada8860a5af3ed7b9342acd1328fe05ac281fbc4a12033c3</citedby><cites>FETCH-LOGICAL-c372t-8bdbd8982efad7f7cada8860a5af3ed7b9342acd1328fe05ac281fbc4a12033c3</cites><orcidid>0000-0001-7728-4118 ; 0000-0003-0025-2323</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/s41586-020-2914-4$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/s41586-020-2914-4$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,776,780,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33208951$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ramirez-Villegas, Juan F.</creatorcontrib><creatorcontrib>Besserve, Michel</creatorcontrib><creatorcontrib>Murayama, Yusuke</creatorcontrib><creatorcontrib>Evrard, Henry C.</creatorcontrib><creatorcontrib>Oeltermann, Axel</creatorcontrib><creatorcontrib>Logothetis, Nikos K.</creatorcontrib><title>Coupling of hippocampal theta and ripples with pontogeniculooccipital waves</title><title>Nature (London)</title><addtitle>Nature</addtitle><addtitle>Nature</addtitle><description>The hippocampus has a major role in encoding and consolidating long-term memories, and undergoes plastic changes during sleep
1
. These changes require precise homeostatic control by subcortical neuromodulatory structures
2
. The underlying mechanisms of this phenomenon, however, remain unknown. Here, using multi-structure recordings in macaque monkeys, we show that the brainstem transiently modulates hippocampal network events through phasic pontine waves known as pontogeniculooccipital waves (PGO waves). Two physiologically distinct types of PGO wave appear to occur sequentially, selectively influencing high-frequency ripples and low-frequency theta events, respectively. The two types of PGO wave are associated with opposite hippocampal spike-field coupling, prompting periods of high neural synchrony of neural populations during periods of ripple and theta instances. The coupling between PGO waves and ripples, classically associated with distinct sleep stages, supports the notion that a global coordination mechanism of hippocampal sleep dynamics by cholinergic pontine transients may promote systems and synaptic memory consolidation as well as synaptic homeostasis.
Studies using multi-structure recordings in macaque monkeys show that distinct phasic pontogeniculooccipital waves modulate hippocampal network events similar to those that underlie the learning and formation of memories during sleep.</description><subject>631/378</subject><subject>631/378/2649</subject><subject>692/698</subject><subject>9/30</subject><subject>96/63</subject><subject>Animals</subject><subject>Brain stem</subject><subject>Cholinergics</subject><subject>Chromosome Pairing - physiology</subject><subject>Coupling</subject><subject>Experiments</subject><subject>Female</subject><subject>Geniculate Bodies - physiology</subject><subject>Hippocampus</subject><subject>Hippocampus - physiology</subject><subject>Homeostasis</subject><subject>Humanities and Social Sciences</subject><subject>Macaca - physiology</subject><subject>Memory</subject><subject>Memory Consolidation - physiology</subject><subject>Monkeys</subject><subject>multidisciplinary</subject><subject>Neuronal Plasticity</subject><subject>Occipital Lobe - 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1
. These changes require precise homeostatic control by subcortical neuromodulatory structures
2
. The underlying mechanisms of this phenomenon, however, remain unknown. Here, using multi-structure recordings in macaque monkeys, we show that the brainstem transiently modulates hippocampal network events through phasic pontine waves known as pontogeniculooccipital waves (PGO waves). Two physiologically distinct types of PGO wave appear to occur sequentially, selectively influencing high-frequency ripples and low-frequency theta events, respectively. The two types of PGO wave are associated with opposite hippocampal spike-field coupling, prompting periods of high neural synchrony of neural populations during periods of ripple and theta instances. The coupling between PGO waves and ripples, classically associated with distinct sleep stages, supports the notion that a global coordination mechanism of hippocampal sleep dynamics by cholinergic pontine transients may promote systems and synaptic memory consolidation as well as synaptic homeostasis.
Studies using multi-structure recordings in macaque monkeys show that distinct phasic pontogeniculooccipital waves modulate hippocampal network events similar to those that underlie the learning and formation of memories during sleep.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>33208951</pmid><doi>10.1038/s41586-020-2914-4</doi><tpages>7</tpages><orcidid>https://orcid.org/0000-0001-7728-4118</orcidid><orcidid>https://orcid.org/0000-0003-0025-2323</orcidid></addata></record> |
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| source | MEDLINE; Springer Nature - Complete Springer Journals; Nature Journals Online |
| subjects | 631/378 631/378/2649 692/698 9/30 96/63 Animals Brain stem Cholinergics Chromosome Pairing - physiology Coupling Experiments Female Geniculate Bodies - physiology Hippocampus Hippocampus - physiology Homeostasis Humanities and Social Sciences Macaca - physiology Memory Memory Consolidation - physiology Monkeys multidisciplinary Neuronal Plasticity Occipital Lobe - physiology Plasticity Pons - physiology Ripples Science Science (multidisciplinary) Sleep Sleep - physiology Sleep Stages - physiology Theta Rhythm - physiology Theta rhythms |
| title | Coupling of hippocampal theta and ripples with pontogeniculooccipital waves |
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