Theta- und Atmung: Interaktion zwischen zwei verschiedenen Oszillationen in der zeitlichen Ordnung neuronaler Aktivität

• Antragsteller: Professor Dr. Andreas Draguhn
• Fachliche Zuordnung: Kognitive, systemische und Verhaltensneurobiologie
• Förderung: Förderung von 2019 bis 2023
• Projektkennung: Deutsche Forschungsgemeinschaft (DFG) - Projektnummer 426518848

• Erstellungsjahr: 2024

Zusammenfassung der Projektergebnisse

This project tackled questions at the interface of neuronal network oscillations and body-to-brain signaling. Network oscillations are well known to govern neuronal activity patterns throughout central nervous systems. They entrain single neurons or local sub-networks into common activity regimes and, hence, enable complex, precisely timed spatio-temporal activity patterns. With this, they are believed to constitute a fundamental neuronal mechanism of cognition, behavior, emotion regulation and even consciousness. Body-to-brain signaling, on the other side, has become an important line of research which (re)-integrates the brain into its interactions with the whole body and environment. This concept has been neglected in many neuroscientific research fields during past decades, resulting in an inappropriate reductionist view at the brain as an information processing machine. Recent evidence suggests that brain-body interactions are bi-directional, and that somatic feedback signals to the brain have important effects on cognition, behavior and emotion regulation. Our project builds upon previous work (much of it by our own group) revealing that the rhythmic nasal air flow of breathing entrains major portions of the mouse brain into rhythmic network oscillations. This respiration-related rhythm (RR) appears to have major effects on neuronal activity and synchronization. In the present project, we focused on the interactions between RR and theta (θ) oscillations, which cover similar frequencies but are mechanistically distinct. We wanted to look at their interactions (mutual, and with other network oscillations) and their (differential?) effects on neuronal activity. Using different electrophysiological methods in vivo we found intricate interactions between RR and θ: The strength of θ-γ-coupling depends strongly on respiration frequency, and θ activity has a causal impact on respiration frequency, while respiration frequency, in turn, determines the frequency of γ- oscillations. In a further study we performed an in-depth analysis of RR and θ-oscillations in the mouse parietal cortex. We revealed differences in the depth profile of both oscillations across the cortical layers, and in the entrainment of single neurons (units). Further studies revealed effects of sleep microstructure (short and long REM-sleep episodes) on breathing frequency and related brain oscillations, and activity- or vigilance-dependent entrainment of cortical neurons by breathing. Together, we significantly expanded the body of knowledge about interactions between breathing, respiration-entrained neuronal activity and interactions with other cortical network oscillations. Open questions remain regarding the cognitive, emotional and behavioral effects of this feedback, the underlying neuronal mechanisms, potential therapeutic applications, and interspecies comparisons, esp. with respect to humans.

Projektbezogene Publikationen (Auswahl)

• Alterations of distributed neuronal network oscillations during acute pain in freely-moving mice. IBRO Reports, 9, 195-206.
  Ponsel, Simon; Zhang, Jiaojiao; Pilz, Maximilian; Yanovsky, Yevgenij; Brankačk, Jurij & Draguhn, Andreas
  
• A New Apparatus for Recording Evoked Responses to Painful and Non-painful Sensory Stimulation in Freely Moving Mice. Frontiers in Neuroscience, 15.
  Zhang, Jiaojiao; Embray, Lee; Yanovsky, Yevgenij; Brankačk, Jurij & Draguhn, Andreas
  
• Temporal Relations between Cortical Network Oscillations and Breathing Frequency during REM Sleep. The Journal of Neuroscience, 41(24), 5229-5242.
  Tort, Adriano B.L.; Hammer, Maximilian; Zhang, Jiaojiao; Brankačk, Jurij & Draguhn, Andreas
  
• Theta-gamma coupling during REM sleep depends on breathing rate. Sleep, 44(12).
  Hammer, Maximilian; Schwale, Chrysovalandis; Brankačk, Jurij; Draguhn, Andreas & Tort, Adriano B. L.
  
• Body and mind: how somatic feedback signals shape brain activity and cognition. Pflügers Archiv - European Journal of Physiology, 475(1), 1-4.
  Draguhn, Andreas & Sauer, Jonas F.
  
• Breathing modulates gamma synchronization across species. Pflügers Archiv - European Journal of Physiology, 475(1), 49-63.
  González, Joaquín; Cavelli, Matias; Mondino, Alejandra; Castro-Zaballa, Santiago; Brankačk, Jurij; Draguhn, Andreas; Torterolo, Pablo & Tort, Adriano B. L.
  
• Differential modulation of parietal cortex activity by respiration and θ oscillations. Journal of Neurophysiology, 127(3), 801-817.
  Jung, Felix; Witte, Victoria; Yanovsky, Yevgenij; Klumpp, Matthias; Brankačk, Jurij; Tort, Adriano B. L. & Draguhn, Andreas
  
• Respiration and rapid eye movement (REM) sleep substructure: short versus long episodes. Journal of Sleep Research, 32(3).
  Hammer, Maximilian; Jung, Felix; Brankačk, Jurij; Yanovsky, Yevgenij; Tort, Adriano B. L. & Draguhn, Andreas
  
• Respiratory entrainment of units in the mouse parietal cortex depends on vigilance state. Pflügers Archiv - European Journal of Physiology, 475(1), 65-76.
  Jung, Felix; Yanovsky, Yevgenij; Brankačk, Jurij; Tort, Adriano B. L. & Draguhn, Andreas