Breathing modulates gamma synchronization across species
Nasal respiration influences brain dynamics by phase-entraining neural oscillations at the same frequency as the breathing rate and by phase-modulating the activity of faster gamma rhythms. Despite being widely reported, we still do not understand the functional roles of respiration-entrained oscill...
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Published in | Pflügers Archiv Vol. 475; no. 1; pp. 49 - 63 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
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Berlin/Heidelberg
Springer Berlin Heidelberg
2023
Springer Nature B.V |
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Abstract | Nasal respiration influences brain dynamics by phase-entraining neural oscillations at the same frequency as the breathing rate and by phase-modulating the activity of faster gamma rhythms. Despite being widely reported, we still do not understand the functional roles of respiration-entrained oscillations. A common hypothesis is that these rhythms aid long-range communication and provide a privileged window for synchronization. Here we tested this hypothesis by analyzing electrocorticographic (ECoG) recordings in mice, rats, and cats during the different sleep–wake states. We found that the respiration phase modulates the amplitude of cortical gamma oscillations in the three species, although the modulated gamma frequency bands differed with faster oscillations (90–130 Hz) in mice, intermediate frequencies (60–100 Hz) in rats, and slower activity (30–60 Hz) in cats. In addition, our results also show that respiration modulates olfactory bulb-frontal cortex synchronization in the gamma range, in which each breathing cycle evokes (following a delay) a transient time window of increased gamma synchrony. Long-range gamma synchrony modulation occurs during quiet and active wake states but decreases during sleep. Thus, our results suggest that respiration-entrained brain rhythms orchestrate communication in awake mammals. |
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AbstractList | Nasal respiration influences brain dynamics by phase-entraining neural oscillations at the same frequency as the breathing rate and by phase-modulating the activity of faster gamma rhythms. Despite being widely reported, we still do not understand the functional roles of respiration-entrained oscillations. A common hypothesis is that these rhythms aid long-range communication and provide a privileged window for synchronization. Here we tested this hypothesis by analyzing electrocorticographic (ECoG) recordings in mice, rats, and cats during the different sleep-wake states. We found that the respiration phase modulates the amplitude of cortical gamma oscillations in the three species, although the modulated gamma frequency bands differed with faster oscillations (90-130 Hz) in mice, intermediate frequencies (60-100 Hz) in rats, and slower activity (30-60 Hz) in cats. In addition, our results also show that respiration modulates olfactory bulb-frontal cortex synchronization in the gamma range, in which each breathing cycle evokes (following a delay) a transient time window of increased gamma synchrony. Long-range gamma synchrony modulation occurs during quiet and active wake states but decreases during sleep. Thus, our results suggest that respiration-entrained brain rhythms orchestrate communication in awake mammals. Abstract Nasal respiration influences brain dynamics by phase-entraining neural oscillations at the same frequency as the breathing rate and by phase-modulating the activity of faster gamma rhythms. Despite being widely reported, we still do not understand the functional roles of respiration-entrained oscillations. A common hypothesis is that these rhythms aid long-range communication and provide a privileged window for synchronization. Here we tested this hypothesis by analyzing electrocorticographic (ECoG) recordings in mice, rats, and cats during the different sleep–wake states. We found that the respiration phase modulates the amplitude of cortical gamma oscillations in the three species, although the modulated gamma frequency bands differed with faster oscillations (90–130 Hz) in mice, intermediate frequencies (60–100 Hz) in rats, and slower activity (30–60 Hz) in cats. In addition, our results also show that respiration modulates olfactory bulb-frontal cortex synchronization in the gamma range, in which each breathing cycle evokes (following a delay) a transient time window of increased gamma synchrony. Long-range gamma synchrony modulation occurs during quiet and active wake states but decreases during sleep. Thus, our results suggest that respiration-entrained brain rhythms orchestrate communication in awake mammals. |
Author | Mondino, Alejandra Torterolo, Pablo Brankačk, Jurij Tort, Adriano B. L. Castro-Zaballa, Santiago Draguhn, Andreas Cavelli, Matias González, Joaquín |
Author_xml | – sequence: 1 givenname: Joaquín surname: González fullname: González, Joaquín email: joaqgonzar@gmail.com organization: Departamento de Fisiología, Facultad de Medicina, Universidad de La República, Brain Institute, Federal University of Rio Grande Do Norte – sequence: 2 givenname: Matias surname: Cavelli fullname: Cavelli, Matias organization: Departamento de Fisiología, Facultad de Medicina, Universidad de La República, Department of Psychiatry, University of Wisconsin-Madison – sequence: 3 givenname: Alejandra surname: Mondino fullname: Mondino, Alejandra organization: Departamento de Fisiología, Facultad de Medicina, Universidad de La República – sequence: 4 givenname: Santiago surname: Castro-Zaballa fullname: Castro-Zaballa, Santiago organization: Departamento de Fisiología, Facultad de Medicina, Universidad de La República – sequence: 5 givenname: Jurij surname: Brankačk fullname: Brankačk, Jurij organization: Institute for Physiology and Pathophysiology, Heidelberg University – sequence: 6 givenname: Andreas surname: Draguhn fullname: Draguhn, Andreas organization: Institute for Physiology and Pathophysiology, Heidelberg University – sequence: 7 givenname: Pablo surname: Torterolo fullname: Torterolo, Pablo organization: Departamento de Fisiología, Facultad de Medicina, Universidad de La República – sequence: 8 givenname: Adriano B. L. surname: Tort fullname: Tort, Adriano B. L. email: tort@neuro.ufrn.br organization: Brain Institute, Federal University of Rio Grande Do Norte |
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CitedBy_id | crossref_primary_10_1016_j_isci_2024_109364 crossref_primary_10_1016_j_cub_2023_09_030 crossref_primary_10_3389_fnins_2023_1164042 crossref_primary_10_1515_revneuro_2023_0152 crossref_primary_10_7554_eLife_83044 crossref_primary_10_1007_s00424_022_02778_5 crossref_primary_10_1523_JNEUROSCI_2075_22_2023 |
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Keywords | Cross-frequency coupling Gamma oscillations Respiration Sleep–wake cycle EEG Brain rhythms |
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SubjectTerms | Animals Biomedical and Life Sciences Biomedicine Brain Cats Cell Biology Chemical communication Cortex (frontal) Cortex (olfactory) Electroencephalography Gamma Rhythm Human Physiology Hypotheses Mammals Mice Molecular Medicine Neurosciences Olfactory Bulb Original Article Oscillations Rats Receptors Respiration Sleep Sleep and wakefulness Synchronization |
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Title | Breathing modulates gamma synchronization across species |
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